See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/31439318

Rethinking Mammalian Brain Evolution

Article  in  Integrative and Comparative Biology · July 1990

DOI: 10.1093/icb/30.3.629 · Source: OAI

CITATIONS READS

252 3,088

1 author:

Terrence W Deacon
University of California, Berkeley
141 PUBLICATIONS   11,242 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Emergent Dynamics View project

All content following this page was uploaded by Terrence W Deacon on 25 July 2014.

The user has requested enhancement of the downloaded file.

 Rethinking Mammalian Brain Evolution1

Harvard University, Peabody Museum, Cambridge, Massachusetts 02138

SYNOPSIS. A critical review of past and current theories of mammalian brain evolution
is presented in order to discuss conceptual problems that persist in the field. Problems
with the concept of homology arise because of the interaction of cell lineages and axonal
connectivity in the determination of structural features of the brain. Focusing on the
continuity of information represented by ontogenetic mechanisms as opposed to mor-
phological features avoids many of these problems and suggests homological relationships
that otherwise have gone unnoticed. Many apparently progressive trends and parallelisms
in mammalian brain evolution turn out to result from the influence of underlying devel-
opmental homologies. Confusions about evolutionary advancement, increasing architec-
tonic differentiation, and the evolution of new brain structures result from a failure to
appreciate how increasing brain size can bias developmental processes with respect to
axonal competition, increased cellular metabolic demands and decreased information
processing efficiency. Explanations of the evolution of novel structures and new connec-
tional patterns are criticized for their failure to consider the constraints of neural devel-
opmental processes. T h e correlations between structural neogenesis, functional special-
ization and size changes in brain evolution are explained by a theory of competitive
displacement of neural connections by others during development under the biasing
influences of differential allometry, cell death or axon-target affinity changes. T h e "dis-
placement hypothesis" is used to propose speculative accounts for the differential enlarge-
ment and multiplication of cortical areas, the origins of mammalian isocortex, the unusual
features of dolphin cortex and the dramatic structural and functional reorganizations that
characterize human brain evolution.

I NTRODUCTION required to even begin to grapple with the

Intrinsic difficulties questions in a meaningful way. T h e dis-
turbing correlate of this is that speculative
Despite the fact that the evolution of the
theories concerning brain evolutionó
brain-particularly the human brain-is
especially human brain evolution-are
of intrinsic interest to anyone curious about
widespread and often contain relatively lit-
the human mind and the origins of human
tle neuroanatomical or neurophysiological
nature, the scientific study of brain evo-
information. But even theories conceived
lution is not a major subdiscipline within
by neuroanatomists and neurophysiolo-
biology, psychology, anthropology or even
gists often reflect numerous unsupported
the neurosciences. T h e apparently poor
assumptions about the direction of evolu-
representation of this area of study in the
tionary trends, the nature of natural selec-
sciences can in part be attributed to the
tion affecting brain processes, the ways that
paucity of direct paleontological evidence
brains can vary from one species to another,
regarding brain evolution and the long-
the relationship between structure and
time inaccessibility of crucial comparative
function within the brain and even the
neuroanatomic details. T h e poor repre-
nature of intelligence itself. Although
sentation of information about brain evo-
paleoneurology is unlikely to experience
lution in disciplines outside the neurosci-
sudden advances in the years to come, many
ences is additionally limited by the
of the barriers to relevant neuroanatomi-
considerable sophistication in comparative
cal evidence have dissolved in the wake of
neuroanatomy and physiology that is
the introduction of many new experimen-
tal techniques in recent decades. Now that
many of the technical impediments stand-
' From the Symposium on Science as a Way of Know- i n g in the way of detailed knowledge about
ing-Neurobiology and Behavior organized by Edward
S. Hodgson and presented at the Centennial Meeting brain structure and function have been
of the American Society of Zoologists, 27-30 Decem- removed, many of these hitherto unques-
ber 1989, at Boston, Massachusetts. tioned assumptions are now open to test.
 Among colleagues in the neurosciences
one sometimes hears the criticism that,
unlike most other areas of neuroscience,
the study of brain evolution is limited to
theory because it is essentially beyond the
reach of experimental approaches.
Although brains of extinct species are not
available for direct inspection and analysis,
this does not necessarily mean that theories
of brain evolution are empirically untest-
able. Indeed they are every bit as suscep-
tible to experimental investigation and
testing as are other theories of brain orga-
nization and function. T h e approach must
necessarily be indirect, but it need be no
less effectual nor any less scientific o r
experimental. We should remember that
the vast majority of scientific data in any
field is indirect, irrespective of whether the
object under study is directly observable.
From tracks left by subatomic particles in
nuclear accelerators to the measurements
of minute amounts of unseen biochemicals
registered in scintillation counters, nearly
all of the "hard data" generated in the
laboratories of any field of the natural sci-
ences are indirect and circumstantial. It is
not the directness o r indirectness of the
data that is important, rather it is the
repeatability of the findings and the coher-
ence of many lines of evidence that are
crucial to scientific knowledge.
A good analogy t o the study of brain
evolution is provided by the study of gene
evolution. Modern techniques for analyz-
ing and comparing base sequences of DNA
molecules from living organisms are begin-
ning to provide a truly astronomical fund
of information concerning both molecular
and organismal evolution. Without analyz-
ing a single fossil specimen of DNA we are
nonetheless capable of reconstructing large
fractions of the genomes of extinct species,
characterizing major gene duplication and
reorganization events of the distant past,
and predicting the ancestral lineages of liv-
ing species and the approximate dates of
their divergences. Al this is available today
despite the fact that only miniscule por-
tions of the DNA in even the best studied
species are actually known and virtually
nothing is directly known about the DNA
of most species. This level of analysis is
made possible by the immensity and com-
plexity of the existing genomes. In many
cases even direct fossil evidence of appar-
ent phylogenetic relationships has been
abandoned in the face of contrary molec-
ular information. As nearly limitless sources
of correlative molecular evidence are fed
into phylogenetic analyses in the near
future they will become immensely more
reliable for the determination of phylog-
eny than the best of all possible fossil finds.
Living organisms are incredibly complex
systems at all levels of scale. Each molec-
ular and organ system within an organism
embodies within its design the ubiquitous
mark of its particular evolutionary history.
In addition, the processes of embryogen-
esis that direct the construction of these
systems are themselves products and symp-
toms of an evolutionary past that a t various
levels intersects with the ancestries of other
species. Comparisons of the differences and
similarities among molecular systems,
organ systems and developmental pro-
cesses in different species provide an almost
limitless source of information for inves-
tigating the evolution of biological struc-
tures. This is ultimately the final arbiter of
any analysis of evolutionary relation-
ships-even for paleontological data—
since the interpretation of fossils is only as
accurate and complete as the information
we have about living counterparts.
T h e complexity of the vertebrate brain
rivals or exceeds the complexity of all the
other organ systems of the body consid-
ered together. Because of this we should
expect that information derived from the
brains of living species will be more than
adequate to the task of investigating brain
evolution, so long as we are willing and able
to approach the task with the level of
sophistication demanded by it. Given this
complexity and our still primitive under-
standing of brain organizati'on and func-
tion, we must be prepared to integrate
information from a variety of subfields of
neuroscience and evolutionary biology in
order to begin to approach the problems
of brain evolution with any clarity.
Although numerous researchers since the
nineteenth century have pursued the study
of brain evolution, most have focused on
a single source of evidence to support their
theories, including: relative brain size (e.g.,
apparent trends in brain size increase); fea-
tures of cortical surface morphology (e.g.,
the appearance or reorganization of sulci);
relative sizes of macroscopic brain struc-
tures with respect to one another (e.g., the
apparent enlargement of isocortex with
respect t o limbic cortex in presumed
"advanced" brains); or cyto- and myelo-
architectonic features (e.g., the apparent
enlargement of association cortex in the
cerebral cortices of "advanced" species).
But uni-dimensional approaches are almost
certain to lead into one misleading cul-de-
sac after another. This has been the fate
of many past theories, just as it will surely
also be the fate of the corresponding uni-
dimensional theories of the present. T h e
only hopeful approach is to integrate rel-
evant information from many lines of neu-
robiological research that bear on the
questions of the patterns of variation and
constraint exhibited by the brains of dif-
ferent species.
Experimental approaches
A number of recent technical advances
have significantly augmented the infor-
mation previously available to comparative
neuroanatomists. Unlike many other organ
systems, the functionally relevant features
of brain anatomy are entirely microscopic
and for many decades were nearly impos-
sible to distinguish even under the micro-
scope. T h e axonal connections linking
neuron to neuron, though visible for short
distances in Golgi-stained material (avail-
able since the turn of the century), have
only become amenable to study in recent
decades. In the 1950s techniques were per-
fected for visualizing degenerating axons.
With these techniques it was possible to
identify the general patterns of long axonal
connections in the brains of experimental
animals. However, the resolution and sen-
sitivity of these techniques were insuffi-
cient t o resolve many of the finer details
of axonal connection patterns. Beginning
in the mid 1970s a number of axonal trac-
ing techniques were developed that took
advantage of the in vivo uptake and axonal
transport. of amino acids, macromolecules
and certain fluorescent dyes. These tech-
niques have now made it possible to inves-
tigate the organization of axonal circuitry
in full microscopic detail. In this regard
the most basic functional anatomy of the
brain has at last become available for study.
We are still far from possessing a complete
connectional characterization for even the
best studied of mammalian brains, yet
already the scattered details from compar-
ative studies have begun to provide a
remarkable array of new insights into the
patterns of brain diversity.
Now that tracer techniques have filled
this crucial gap in information about basic
neural functional anatomy, these data can
be integrated with data from physiological
and quantitative studies to provide all the
pieces of evidence necessary for investi-
gating the principles underlying brain evo-
lution. However, it is insufficient to apply
the analysis to adult brains only. Probably
the most crucial information for evolu-
tionary purposes is how connection pat-
terns and structural differentiation are ini-
tially established in a developing brain. New
techniques for labeling mitotic cells, mark-
ing cell lineages, and experimentally alter-
ing development in neonatal animals o r in
utero by removing o r transplanting embry-
onic tissues are also beginning to provide
detailed information about the develop-
mental processes that shape neural circuits.
Developmental information can play a cru-
cial role in settling questions of homology.
More generally, it can provide evidence for
the range of possible mechanisms available
for natural selection to modify and dem-
onstrates the constraints that limit possible
variation. Many scenarios of brain evolu-
tion conceived in the absence of critical
information about the development of the
structures in question turn out to be incom-
patible with these constraints.
This rapidly growing body of neuro-
biological information is providing an
unprecedented opportunity to discover new
patterns of similarity and variation in brain
evolution, and to test old and new hypoth-
eses about neural evolutionary processes.
It also provides impetus for a critical reex-
amination of the dogmas and unanalyzed
assumptions that currently dominate
thinking about brain evolution.
Conceptual problems
Most of the theories concerning brain
evolution in the early part of the 20th cen-
tury focused on its most studiable features,
size, gross morphology, and cytoarchitec-
ture. Crude connectional information was
available only from careful dissections and
what little could be discerned with Golgi-
staining. Despite the unavailability of cru-
cial categories of information, theories of
brain evolution have flourished. As a result
modern students entering this field will find
the literature replete with numerous well
accepted dogmas about the general char-
acter of brain evolution espoused by some
of the century's most brilliant comparative
neuroanatomists. Even more daunting is
the fact that many of these dogmas have
become seamlessly woven into the anatom-
ical and functional terminology of the rest
of the neurosciences as well. Terms like
paleocortex, neocortex, primary areas,
secondary areas, projection cortex and
association cortex all bear the stamp of an
evolutionary vision that appears beyond
question, a part of the unspoken common
knowledge of the neurosciences. But with
the recent advent of new tools and a flood
of new information concerning neural con-
nections, functions and ontogenetic pro-
cesses, there has been a growing disso-
nance between the new data and some of
the well-established principles of brain evo-
lution. My purpose here is to play devil's
advocate; to question even the most well
founded of these dogmas and adopt the
heretical stance that many-if not most-
of the traditional assumptions concerning
neural evolutionary processes are without
foundation. Hopefully, the introduction of
a healthy dose of skepticism will allow us
to look at the problem of brain evolution
with fresh eyes.
Four major conceptual problem areas will
be reexamined most carefully because of
their potential for misdirecting the study
of brain evolution and also because of the
influence they exert over contemporary
ideas about brain function in general. T h e
first of these is the concept of homology-
the relationship shared by structures by
virtue of sharing a common ancestry. T h e
second is the notion of evolutionary progress
o r orthogenesis-the idea that evolution
proceeds in a particular direction of
improvement or development. T h e third
is the significance of brain size-both in
absolute terms and relative to the body or
to component brain structures. T h e fourth
is the problem of identifying and explain-
ing neogenesis-the evolution of new struc-
tures and functions.
All four conceptual issues were familiar
to the 19th century pioneers in this field
whose major assumptions in all these areas
remain dominant in many contemporary
treatments of the subject. Contemporary
versions of these ideas are in the back-
ground of every theory of brain function
as well as every attempt to articulate a the-
ory of brain evolution. Despite a century
of advances in evolutionary thinking in
other fields of biology these ideas within
the neurosciences still carry the distinct
imprint of late 19th century evolutionism.
And despite a century of experimental
investigation of brain function these ideas
still reflect one or the other side of the 19th
century debates over associationistic and
holistic theories of mental function. Exor-
cising these influences is one of the central
purposes of this presentation.
The other major purpose is to present
an alternative approach to the study of
brain evolution that avoids many of'these
a priori assumptions. Many of these
assumptions have been derive'd f r o m
attempts to arrange the adult nervous sys-
tems of contemporary species in some sort
of evolutionary sequence o r cladistic den-
drogram so that any two may be linked via
some intermediate adult forms. While this
is a powerful heuristic it tends to imply the
misleading conclusion that the mecha-
nisms for evolutionary change can be accu-
rately described in terms of the modifica-
tion of adult forms. This, of course, misses
a crucial intervening level of analysis. Ulti-
mately, the mechanisms of evolutionary
change must be explained in terms of the
ontogenetic processes and developmental CLADlSTlC COMPARISON CLADlSTlC HOMOLOGV

constraints that build brains. Explanations C

of evolutionary change that are not cast in
developmental terms are merely disguised
comparative morphological descriptions.
Consequently, the reviews and criticisms
presented will constantly appeal to devel-
opmental data to test the plausibility and
PARALLEL HOMOPLASY CONVERGENT HOMOPLASY
consistency of some of the dominant the-
ories of brain evolution. Finally, in the last
two sections many of these developmental
insights will be utilized to outline an alter-
native ontogenetically based interpreta-
tion of the processes underlying brain evo-
lution in mammals. This interpretation of
brain reorganization events-called the FIG. 1. Homology relationships. T h e basic homol-
ogy relationships as outlined by Northcutt (1984). T h e
"displacement hypothesis"-suggests that arrows represent descent relationships. T h e vertical
there is an interdependent relationship axis represents comparison over time o r descent in
bdtween differential growth of particular evolution and the horizontal dimension represents
neural cell groups and competitive-regres- comparison of contemporaneous species. T h e geo-
sive processes in brain development that metric shapes represent similar o r different, ancestral
o r derived traits. In the case of parallel homoplasy it
constrain patterns of brain evolution, often is unclear whether the parallel divergence from the
resulting in parallel or converging trends. ancestral condition is a consequence of internal (ho-
Two particularly enigmatic cases are exam- mological) o r external (selectional) commonalities.
ined in t h e last section- dolphin a n d These same relationships can be applied equally t o
comparisons between lineages o r to homologous rep-
human brain evolution-and are inter- etition of parts within an organism. (Redrawn from
preted in terms of displacement processes. Northcutt, 1984.)
Features of these brains that previously
have been difficult to explain o r seemed
beyond study become understandable in applied to traits that exhibit structural o r
terms of the displacement hypothesis. functional similarities but which are not
derived from common ancestry. In other
H OMOLOGY words, their similarity is the result of influ-
ences extrinsic to the organism. T h e other,
The concepts of homology and homoplasy parallel homoplasy, has traditionally been
T h e concept of homology in some form termed parallelism and refers to cases where
is essential to any study of evolutionary there is similarity in both form and com-
morphology. It defines the warp of evo- mon ancestry but where the formal simi-
lutionary continuity with respect to which larity between traits is not shared in the
the weft of diverse adaptations can be common ancestral condition. I n o t h e r
understood. I n a useful summary of the words, the formal similarity of the (patris-
problems of homology in comparative neu- tically) homologous parts is presumed t o
roscience Northcutt (1984) distinguishes have arisen independently in the two lin-
patristic homologies (the actual descent rela- eages after divergence from the common
tionship between an ancestral form and a ancestor. In this case there is both a patris-
present form) from cladistic homologies (the tic homological relationship and a cladistic
comparison of extant forms with respect convergent homoplaseous relationship
to their possible common ancestral rela- involved. T h e parallel divergence of the
tionships) and then contrasts these with two two descendent traits from the common
forms of dishornology that may be con- ancestral condition is presumably the result
fused with homology. One of these, con- of common extrinsic selection pressures.
vergent homoplasy, corresponds to what has These relationships are schematized in Fig-
traditionally been termed analogy and is ure 1 (redrawn from Northcutt, 1984).
 Where the ancestral condition is the
unknown feature to be inferred from cla-
distic comparisons it can be quite difficult
t o distinguish homology from these two
forms of homoplasy. Northcutt, following
Wiley (1981) and others, suggests a num-
ber of guidelines for aiding this discrimi-
nation, including: (1) sharing deep similar-
ities of form (as opposed t o merely
superficial resemblances), (2) sharing com-
mon epigenetic precedence (i.e., derivation
from common ontogenetic precursor
structures), and (3) the existence of a con-
tinuity of intermediate forms in species
intermediate in relationship between the
two being compared. All there criteria are
versions of the identification of similarity
in some form.
In this discussion I will not review the
various problems encountered in attempt-
ing to determine neural homologies in
practice, nor will I discuss methodological
strategies for circumventing these prob-
lems and the multiple criteria that must be
satisfied to provide a convincing case. These
have been well reviewed elsewhere (Camp-
bell, 1982; Campbell and Hodos, 1970;
Ghiselin, 1976; Northcutt, 1984). T h e
point of this discussion is to analyze the
concept itself as it is applied to problems
of brain evolution because I think there is
reason to be suspicious of the assumptions
implicit in its common usage. It is not the
empirical determination of homology that
is at issue, but the concept itself. I will argue
that there is something fundamentally
wrong with the notion of homology as it is
applied to the comparison of morpholog-
ical features that can become especially
troublesome in the analysis of brain struc-
ture.
Problems with the concept of homology
Homological relationships a r e most
clearly exhibited in topological relation-
ships. A focus on topological continuity for
identifying homology dates back to the ear-
liest pre-evolutionary theories about the
vertebrate "Bauplan" (an insightful his-
torical discussion is provided in Russell,
19 16). Because organisms are spatially
organized systems, position within a net-
work of relationships is crucial to conti-
nuity of function. Although the particular
features of the individual components of
the organism may change over evolution-
ary time the systemic relationships among
parts, including their contiguity relation-
ships, are relatively stable. Even when
structures derived from a common evolu-
tionary precursor have diverged in form
so as to share no superficial resemblance
their relationships t o o t h e r structures
within the organism, both in the adult form
and at various stages of development, will
exhibit sufficient similarity to indicate their
homology.
T h e usefulness of topological criteria for
the determination of homological similar-
ities derives from the fact that many mor-
phological traits (although not the under-
lying genes themselves) are determined by
systemic interactions between morphoge-
netic fields (or other converging morpho-
genetic influences) and not by independent
local mechanisms. T h e information that
determines a morphogenetic field inevit-
ably derives from multiple genetic sources
interacting with one another sequentially
and simultaneously during ontogenesis.
T h e resultant morphological trait is a bit
like a node within a network that has no
independent existence apart from, its rel-
ative position. Such a node is defined by
its unique convergence of relationships with
other nodes. If some of these relationships
are lost or new ones are gained, continuity
with the previous state becomes ambiguous
and depends on whether you focus on the
relationships o r the nodes. Analogously, a
single morphological feature may become
two if interdependent morphogenetic pro-
cesses decouple in space o r time, but two
features may also fuse t o become one if
previously noninteracting morphogenetic
processes become subsequently linked and
interdependent.
This possibility is more likely in the brain
than in other organs by virtue of the fact
that brain traits are defined in terms of two
independent topological criteria: (1) cell
lineage relationships of local populations
that may determine local topological rela-
tionships, cell structure, and molecular and
neurotransmitter characteristics; and (2)
connectional relationships determined by
axons that link numerous separated tar-
gets, each likely derived from different cell
lineages, which may also influence mor-
phological, cellular and functional char-
acteristics of their various target struc-
tures. Both cellular and connectional
attributes interact during development to
determine the architecture and function of
a brain region.
Assuming that connectivity is capable of
changing during the course of evolution it
is not hard to imagine the kinds of diffi-
culties that might arise in interpreting
homologies. T h e position, cellular char-
acteristics and even embryonic origins of
a brain structure in a descendent species
may be derived from a corresponding
stricture in some ancestor, and the descen-
dent structure's connectional relationships
may also be derived from connection pat-
terns in that same ancestor. Yet the par-
ticular homologous circuit and homolo-
gous structure may not have been
associated with each other in the brain of
that ancestor. For example, it is conceiv-
able that qseries of evolutionary events can
cause afferents of one brain structure to
invade some other structure, replacing the
"ancestral" afferents of the new target—
similar effects can be induced experimen-
tally (see below). In this event a connec-
tional or circuit homology will have been
maintained, probably retaining its func-
tional characteristics, but the relationship
between cellularly defined homologues and
connectionally defined homologues will
have become dissociated. T h e structural
homology can no longer be defined with
respect to position within a network and
the connectional homology can no longer
be defined with respect to the structures
that are connected. Continuity with the
ancestral form can nonetheless still be
traced through the remaining descent rela-
tionships in each case, though the number
of topological criteria used to identify this
descent has diminished for each.
Further deterioration of homology cri-
teria can also be imagined. For example, if
the connectional relationships play a sig-
nificant role in determining the local
cytoarchitecture a n d neurotransmitter
characteristics of a target area (this appears
to happen in cerebral cortex, as indicated
by heterotopic transplantation experi-
ments) it might appear on these grounds
that an ancestral target has simply become
displaced to a new position, despite the fact
that cell lineages and some connectional
relationships did not follow this shift. With
a large number of criteria in agreement,
but cell lineage and a few connectional
relationships do not follow this shift. With
difficult to decide between the deaffer-
ented target o r the invaded target as the
appropriate homologue of the ancestral
structure. At the level of the whole struc-
ture the judgment is ambiguous and yet
each underlying trait has a homologous pair
that can be traced in unbroken series to a
common ancestral condition. It is not clear
that shifting the analysis to these under-
lying traits can escape similar problems at
a yet lower level. As we consider evolu-
tionary "interventions" that might alter
progressively earlier stages of ontogeny it
is possible to imagine increasing loss of
descent criteria in this manner.
A similar complication can arise in the
effort to identify homologous sulci in rel-
atively convoluted brains. Prior to the
development of techniques for unambig-
uously staining myelin o r neuron cell bod-
ies the interpretation of sulcal homologies
in different species brains was considered
the best clue to the structural homology of
underlying regions, and this approach
dominated throughout the early part of
this century (Ariëns Kappers et al. , 1936).
Although it has recently been abandoned
as unreliable for most comparative work,
it still remains the only evidence for paleo-
neurology (working with the casts of fos-
silized crania). In the study of human evo-
lution this has been t h e source f o r
continuing heated debates over the origins
of "modern" human brain traits (e.g., Falk,
1980, 1983, 1989; Holloway, 1981, 1984,
1985, 1988).
Most cortical sulci are probably the result
of the interactions between the mechanical
forces and constraints imposed by the cra-
nial cavity, differences in growth rates of
brain areas, and relative elasticity of dif-
ferent areas of the developing cortex and
underlying white matter. If the underlying
neural substrate influencing the formation
of a sulcus changes o r becomes displaced
with respect to cranial landmarks in sub-
sequent lineages it may cause the position
of the sulcus to follow. If this were the
typical case sulci might be relatively good
indicators of underlying brain structure
homologies. Alternatively, changes in bone
growth patterns of the skull o r changes of
the absolute size of the brain with respect
to the skull in subsequent lineages may pro-
duce changes in mechanical forces influ-
encing sulcal position and cause a sulcus to
shift to a new location without any corre-
sponding change in position of the original
neural substrate. In this case the link
between sulcal and neural homologies
would be broken. However, if the appear-
ance of a particular sulcus is dependent on
the combined influence of both extrinsic
mechanical forces and intrinsic growth
processes of the neural tissue, then spatial
separation of these two independent influ-
ences may cause a sulcus to disappear and
then reappear in some later lineage in
which these influences again become
realigned. This atavism would still be a case
of homology, despite the discontinuity in
descent. Finally, if a particular sulcus can
be induced by either influence alone then
spatial separation of extrinsic and intrinsic
factors may also produce two sulci where
one existed previously. I n this case,
although each is patristically homologous
with the ancestral condition, it is unclear
whether they can be said to be cladistically
homologous to each other. All of these pos-
sibilities demonstrate the dangers of treat-
ing sulci as definitive markers of underly-
ing neural homologies.
Similar problems with the strict descent
interprktation of homology have been
noted with respect to non-neurological
comparative problems, causing some
authors (e.g., von Cranach, 1976; Filler,
1986) to: suggest that the homology con-
cept should be entirely abandoned. But an
alternative approach is suggested by these
problematic examples. T h e crucial ques-
t ions we are trying to answer by identifying
homologies are questions about continuity
of information (Van Valen, 1982). A mor-
phological structure or any other manifest
trait is only the surface expression of
underlying information. This information
is encoded both in gene sequence and in
the topological and temporal conditions of
their expression in the developing organ-
ism. T h e confluence of multiple indepen-
dent sources and kinds of epigenetic infor-
mation to form a particular structure
implies that no particular individual thread
of information constitutes an indispensable
link between homologous structures. A
homology exists so long as some relation-
ships between the remaining sources of
information are maintained. Alternatively,
if separate threads of information are
passed down from generation to genera-
tion independently and only brought into
relation with one another in some descen-
dent where their interaction produces a
novel structure, we must consider the
structure as emergent and neoplastic (the
newly established relationships between
these threads of information is itself a bit
of information that is unprecedented) and
yet also recognize the complete homology
of underlying component morphogenetic
processes. T h e relationship is diagrammed
in Figure 2. Because ontogenetic processes
are multileveled, homological relation-
ships must also be multileveled (Alberch,
1982; Fasolo and Malacarne, 1988), with
homologies at higher levels not necessarily
reduceable to those at lower levels. In addi-
tion, homologies at every level above that
of the genes are to some extent ephemeral,
capable of dissolving and reconstituting in
the course of evolution because they are
determined only in relational terms. This
also implies that the same bit of epigenetic
information expressed in a different con-
text within the same organism must also
be understood as homological.
Homologies between the different
parts of a brain
T h e interpretation of homolo gy as com-
mon information is crucial to another clas-
sic use of the concept of homology: serial
homology or homological multiplication of parts.
Repeated similar parts in the segments of
a worm, similar vertebrae in different posi-
tions along the spinal column, similarities
in limb and digit structure, and bilaterally
symmetric parts of the body in general are
all examples of homologous repeated parts.
Although not descended from any single
ancestral structure, such homologous parts
undoubtedly inherit their similarities of
form from a single ancestral source of
developmental information. Within the
central nervous system there are examples
of classic serial homology in segmental
spinal cord circuitry, bilaterally symmetric
parts at all,levels, and multiple homologous
parts within every structure at many levels
of organization.
Starting on a small scale we recognize
that nearly all neurons exhibit homologous
axons, dendrites, synapses, etc.
within the same structure there are classes
of neurons with homologous patterns of
dendritic arborization, axonal targets and
neurotransmitters. Local circuit patterns
of nearby neuronal groups also exhibit
homologies, such as are found among cor-
tical lamina and cortical columns in iso-
cortex. Even distributed functional circuits
linking separate structures may be serially
homologous: e.g., projections from differ-
ent' thalamic nuclei to different cortical
areas. Even structures that are superficially
quite distinct may exhibit underlying
homologies at some levels but not others.
This might be the case for the relationship
between the hippocampus and the isocor-
tex, which exhibit many features in com-
mon at the cellular level and have homol-
ogous patterns of afferents and efferents
yet very different laminar architecture.
Homologies between different brain
regions might possibly develop as a result
of derivation from a common undifferen-
tiated ancestral structure, but descent
homology need not be defined at the struc-
tural level only. It may also result from
independent expression of the same under-
lying epigenetic information. Similarly,
during ontogeny homologies between cell
types may develop by descent from a com-
mon embryogenetic cell lineage a n d
homologies between complex structures
may develop because they were each
derived in a process of differentiation from
some common embryological structure.
However, because all cells share the same
genetic information, it is also possible that
ontogenetic interactions
morphological phenotypes
level
epigenetic
process level
morphological phenotypes
homoplasy
intervening
epigenetic
homologies
variables
producing
developmenlal
plasticity
FIG. 2. Developmental homologies. T h e multiple
level problem of developmental homologies is depicted
in a highly schematic form by representing interact-
ing morphogenetic processes as arrows and the resul-
tant morphological traits as geometric shapes. T h e
upper figure shows that the homological relationships
could be analyzed either at the morphological level
by comparing morphological (or even behavioral)
phenotypes o r at the epigenetic process level by com-
paring epigenetic mechanisms. Both are phenotypes
that indirectly represent underlying genotypes but
the higher level analysis condenses information rep-
resented at the lower level by distinct processes and
can thereby miss considerable underlying develop-
mental homology. Nonetheless the higher level anal-
ysis also takes into account conserved o r derived rela-
tionships between underlying developmental
mechanisms that may themselves be homologous in
two lineages but which produce non-similar diverging
phenotypes. Of course the actual condition involves
many more than two levels. T h e lower level "epige-
netic mechanisms" are likely themselves the products
of relationships between yet lower level cellular o r
molecular processes and the "phenotypic level" may
also be a set of epigenetic mechanisms of a higher
level of complexity. Hierarchic analysis cannot be
avoided.
homologous structures may appear simul-
taneously in development by independent
expression of the same underlying infor-
mation activated by some common molec-
ular trigger or internal timing mechanism.
Within a number of areas of the brain it
is likely that cell lineage is not the only and
perhaps not even the major determinant
of cellular, structural o r functional homol-
ogies. For a few brain areas there is now
evidence that a single precurser cell can
give rise to the multiple cell types within
that region (Rakic, 1988) and studies uti- cept of functional homology. It can be
lizing embryonic chimeras composed of two defined as the similarity and continuity that
immunologically distinguishable genomes exist between functions as a result of
demonstrate that cells from both lineages homologies between their substrates. T h e
are effectively scattered diffusely through- evolution of new functions by the modifi-
out all areas and representing all cell types cation of old structures is a common theme
(Goldowitz, 1987). Cell lineage probably in evolution. When the vertebrate fore-
determines many local biochemical char- limb evolved the capacity for flight in the
acteristics of neurons (Fasolo and Mala- evolution of birds, the skeletal, muscular
carne, 1988) and certain structural archi- and neural structures retained the general
tectonic features (e.g., Kuljis and Rakic, "Bauplan" of the ancestral terrestrial con-
1988) and it may provide gross areal dif- dition and also retained numerous func-
ferences distinguishing major morphoge- tional constraints. These have all played a
netic fields, but at the present time there role in shaping flying behavior in bird
is little positive evidence available on this species. Additionally, the peripheral motor
point and extensive evidence that extrinsic neural architecture (Sokoloff et al., 1989)
influences determine function and neural and even features of the central locomotor
connectivity to a large degree (O'Leary, "patterns" (Kaplan and Goslow, 1989)
1989). Timing of final mitosis and inter- exhibit strong similarities in birds and ter-
cellular interactions also appear to play sig- restrial quadrupeds, despite t h e o t h e r
nificant roles in determining neuronal cel- major functional differences that their
lular types and local structural and exclusive adaptations demanded.
functional characteristics. With the differentiation of new neural
In general, a major part of structural circuits from ancestral circuits and the
differentiation in the developing brain is elaboration of corresponding new func-
based on distributed information that is tional adaptations we can expect to trace
embodied systemically in its spatial-tem- functional homologies in the form of
poral organization and dynamically in the underlying functional similarities and con-
axonal interactions between indepen- straints. Even in extreme cases in which
dently derived neuronal populations. T h e neural structure is co-opted for new adap-
details of this process will be discussed in tations that are radically different than the
later sections, but in terms of homology ancestral function, the underlying homol-
this fact leads to an important conclusion. ogies will likely exert a major organizing
If the information distinguishing one influence on the form and range of vari-
region from others is not entirely embod- ability of the new function. This may eyen
ied within the cells of that region, but is be true of such a novel adaptation as the
expressed only as those cells are contacted syntactic structure of language (e.g., Reyn-
by invading axons and as its own axons olds, 1976; Lieberman, 1984; Deacon,
establish efferent terminations, then dif- 1990c), if some of the cortical systems that
ferent serially homologous structures came to serve language functions in the
within the brain (e.g., different cortical course of human evolution had been ante-
regions) do not ultimately determine their cedently adapted for other behaviors (e.g.,
own distinctions of structure and function. motor planning). Anatomical evidence for
Their unique specializations with respect such a view is presented by Deacon (1 988a,
to one another are instead derived from 1990c).
network relationships with other areas of Functional homologies should also be
the brain (both cortical and subcortical). exhibited by serially homologous struc-
tures within the same brain. For example
Functional homology the many homologous structural features
One last use of the concept of homology shared by all regions of isocortex suggest
tnust be introduced at this stage before that there should be strong functional
moving on to a discussion of some of the homologies shared by all of its functional
major theories of brain evolution: the con- subdivisions despite the radical differences
in modality of their input-output relation- we have appeared only recently after a long
ships (Diamond, 1979). T h e same may also period of brain evolution characterized by
be said of the different regions and sub- less intelligent species, our brain repre-
divisions of the basal ganglia (Alexander sents the pinnacle of some long evolution-
and Strick, 1986). Presumably, the affer- ary trend.
ents to each homologous area transmit dis- From these few assumptions a great many
tinct forms of information that are sub- predictions must follow, and so from the
jected to some common neural calculation outset we feel confident in assuming the
in each homologous area. For this reason, answers to a number of central questions:
different scenarios for the phylogenetic bigger brains are smarter brains; more
ancestry of brain structures that suggest complex brains are more developed brains;
different ancestor-descent relationships primates are smarter than other species;
bring with them different predictions con- our closest relatives, the great apes, are
cerning function. smarter than other primates; there is an
evolutionary trend toward increased intel-
PROGRESSION ligence; more intelligence is always a supe-
rior adaptation to less; brain evolution tends
The assumption of evolutionary progress toward increasing complexity and increased
T h e idea of progressive evolution is a relative brain size; earlier stages of brain
product of the uneasy marriage between evolution are characterized by more prim-
Darwinism and the scala naturae theories itive, relatively less differentiated and rel-
of the mid 19th century. It received its atively smaller brains than later stages; parts
clearest expression in the theories of Spen- of the brain that are relatively undiffer-
cer, Haeckel, Berg and Teilhard de Char- entiated are more primitive and parts that
din among o t h e r influential writers. are more complex are more recent; brain
Althou h evolutionary biologists in recent structures that enlarged most in ourselves
decades have learned to rigorously avoid and our close ancestors are the most highly
making such assumptions when thinking developed and most recent brain struc-
about a particular assemblage of fossils o r tures; the most recent human functions (i.e.,
a lineage of species, this habit of thought language) must be controlled by the most
is not so well entrenched in the neurosci- advanced, complex and recent structures
ences, nor in anthropology, psychology or in the brain; etc. All we need to d o is to
linguistics where theories and assumptions find out how the data concerning brain size
about human brain evolution are also likely and brain structure diversity demonstrate
to be found. T h e tendency is so pervasive these points! Presumably, whatever fea-
that evolution is often considered synon- tures of brain organization we use to com-
ymous with progress, whereas evolution- pare brains of different species, Homo sapi-
ary change without progress, even when ens should represent the extreme high end
directional, is often not considered evolu- of the scale (however this is defined in each
tion at all, merely "drift." case). I call this assumption the "Anthro-
T h e ubiquity of the idea of progress in pocentric Maxim."
brain evolution can be traced to what we T h e tenacious hold of anthropocentrism
believe we already know about our own on our thinking about brain evolution is
place in an intellectual chain of being. It great. What is needed is a biological equiv-
apparently goes without saying that humans alent of the "Copernican Revolution" to
are the smartest species to have ever lived---- finally shake it loose. Along with this
never mind that we are not sure what we implicit anthropocentrism we should also
mean by "smartest"-and it is also popular endeavor to root out the tendency to
knowledge that human evolution involved assume progressive trends in any aspect of
significant brain enlargement. Our brain brain evolution, unless and until all alter-
must also be the most complex, if for no native explanations have been exhausted.
other reason than the fact that our abilities There undoubtedly are progressive trends
are the most complex of any species. Since in brain evolution, but to clearly identify
them and to understand their significance and that more highly differentiated brain
we must demonstrate that they are not structures are more advanced than more
merely superficial correlates of other non- diffusely organized brain structures.
progressive trends. T o be able to do so Although we can probably assume that
requires that we first understand these there are some recent brains that a r e more
other trends. differentiated than any from fifty million
T h e a priori assumption of "advance- years ago, we cannot safely invert the logic
ment" in evolutionary sequences is a source and assume that the most undifferentiated
of many misunderstandings. Deacon contemporary brains are the least derived.
(1990a) reviews many of the assumptions Confounding variables such as absolute size
about brain evolution that derive from the and specific sensory-motor specializations
notion of evolutionary progress in brain may influence relative differentiation, and
size. Even theories that do not specifically problems in assessing homology as well as
invoke the notion of progression nonethe- sampling biases inherent in the phyletic
representation of species may introduce
less tacitly assume it in the process of iden-
tifying some structures as "advanced" and spurious correlates of differentiation that
others as "primitive." A primitive t o have nothing to do with primitiveness.
advanced ranking of living organisms o r In discussions of mammalian evolution
their structures must ultimately be based small bodied living insectivores are typi-
upon independent knowledge of the evo- cally treated as exemplars of the mor-
lutionary trend in question; otherwise the phologies of ancestral mammals. These so-
argument is circular. But when faced with called "basal insectivores" are assumed to
structures that leave no fossil evidence be "generalized" in their adaptation and
independent evidence is hard to obtain. "conservative" with respect t o evolution-
One possibility is to assume that the pro- ary trends, although caveats are usually
gressive ranking of soft-tissue structures suggested regarding the fact that each of
should correlate with other preserved indi- these groups represents some rather spe-
cators of the relative primitiveness o r cialized adaptations as well. T h e European
advancement of the organism as a whole. hedgehog (Elliot-Smith, 19 10; Ariëns Kap-
Overall similarity of traits from living pers et al., 1936; Filimonoff, 1949; Dia-
species to those in early fossil specimens ofmond and Hall, 1969; Valverde and López-
some lineage might suggest that the orga- Mascaraque, 1981; Sarnat and Netsky,
nization of brain structures is also equally 1981) as well as moles, tenrecs and micro-
comparable. It is of course necessary to chiropteran bats have all been cited as pos-
determine that the resemblances are not sessing conservative brain structure typical
superficial. and the result of convergent of an "initial" mammal brain (Sanides,
evolution. And even when this can be dem- 1969, 1970; Le Gros Clarke, 197 1; Glezer
onstrated there is never any guarantee that et al. , 1988). There are unfortunatel y a
the brain structures in question have been number of circular assumptions in the con-
as conservative as the rest of the mor- cepts of "primitive survivor" and "basal
phology. Even the external morphology of insectivore" (Martin, 1973) that also afflict
the brain, as may be revealed by endocasts, the concept of an "initial brain."
cannot be taken as a reliable indicator of Fossil specimens suggest that it is likely
underlying cellular a n d connectional that the eutherian mammal ancestor which
homologies. So a primitive external gave rise to the Paleocene-Eocene radia-
appearance of modern brains is an untrus- tions was of relatively small body size and
tworthy indicator of primitive brain orga- probably bore at least a superficial resem-
nization. blance to modern shrew-like insectivores.
In this regard there is considerable justi-
From simple to complex fication for selecting insectivores as exem-
It seems unquestionable that simpler plary of the ancestral condition. T h e pre-
brain structure precedes more complex sumption that the common ancestor was
brain structure in the course of evolution, somehow "generalized" or even that mod-
ern basal insectivores are "generalized"
species seems a little more puzzling,
although it is widely claimed. In many ways
members of these groups represent some
extremes of specialization. Consider, for
example, the echolocation specialization of
microchiropteran bats, the fossorial o r
nocturnal specializations of many shrews,
moles and hedgehogs, the aquatic special-
izations of some exceptional shrews, and
of course the insectivorous specialization
itself. These facts must certainly relate to
their neurological adaptation. Of course
there is every reason to suspect that the
common ancestor of eutherian mammals
was also specialized in some interesting
ways, but given the radical difference in
faunal context and likely niche specializa-
tion there may be no corresponding spe-
cialization represented in modern species.
T h e tree shrew Tupaia has been sug-
gested by some as an appropriate living
model for a Paleocene precursor to pri-
mates (Le Gros Clark, 197 1;Cartmill, 1972,
1974), In terms of its size and many of its
non-neurological features it too might serve
as a reasonable stem mammal model. But
it is usually disqualified as an "initial brain"
model because it possesses a number of
"advanced" brain features, including mod-
erate encephalization and a differentiated
striate cortex and visual association cortex.
T h e cortex of Erinaceus, the European
hedgehog, is often treated as a model of
an ancestral mammalian cerebral cortex.
Figure 3 depicts some of the known areal
divisions of the hedgehog cortex along with
an even more "primitive" tenrec brain.
Some notable features of the isocortex of
these species as compared to "advanced"
brains include: relatively small size com-
pared to olfactory and limbic cortex, poorly
distinguishable lamination, low level of
myelination, poor differentiation from area
to area, lack of a clearly distinguishable
agranular motor area, poorly granularized
koniocortical sensory areas, vagueness of
boundaries between architectonic areas,
the apparent adjacency of sensory-motor
projection areas with little interdigitated
association cortex, and a relatively thick
layer I (a limbic cortex characteristic) in all
areas of its isocortex. It seems unquestion-
able that these brains are near some
extreme in the spectrum of cortical orga-
nization among eutherian mammals, but
this may not be conservatism. In fact, on
the basis of brain traits selected for their
value in determining cladistic relation-
ships, Kirsch et al. (1983) find that hedge-
hogs do not appear t o exhibit a prepon-
derance of conserved traits, but just the
opposite, they appear to possess one of the
most derived mammal brains (Johnson,
1988).
It is clearly not the structure of the
hedgehog body that motivates its choice as
an exemplar. It exhibits highly specialized
spiny hairs for predator protection and has
developed the ability t o role into a ball with
only its spines exposed, it has relatively
short, stubby limbs specialized for digging,
it has very rudimentary visual abilities with
clearly reduced eyes that are appropriate
to its nocturnal-fossorial habit, and it has
a well developed specialized snout and pre-
sumably highly specialized olfactory abili-
ties for insect predation. Campbell (1988)
remarks that if the hedgehog were other-
wise the same but possessed a larger more
differentiated brain it would never have
been considered an exemplar of the "ini-
tial brain'' pattern. Gould (1977) notes that
in general it is unwise to choose the most
undifferentiated extant member of a group
as a representative of its stem ancestor pre-
cisely because small bodied fast breeding
forms are likely to be highly derived
r-selected species. T h e choice of species
with small undifferentiated brains is not so
much motivated by external similarities
with known fossil types as by a priori
assumptions about what is primitive and
what is advanced.
T o carry this paradigm to its logical
extension, the hedgehog is probably not
the most extreme case that could be cited.
Zilles and Rehkämper (1 988) point out that
Erinaceus is actually somewhat advanced
with respect to some other basal insecti-
vores and therefore might not be the ideal
exemplar of the "Grundtypus" for mam-
malian brain organization. They note that
the brains of the tenrec Echinops and the
geogaline Geogale exhibit even less enceph-
alization and exhibit fewer progressive fea-
lateral view

brain of a tenrec brain of a hedgehog

Centetes Erinaceus
FIG. 3. Hedgehog and tenrec brains as seen from above and the side labeled to show approximate positions
of the major sensory and somatomotor fields. Isocortex is indicated in gray in the left hemisphere of each
and limbic and olfactory cortex is white in the same hemisphere. Since most of the cortical representation is
unknown for the tenrec and only partially known for the hedgehog specific boundaries between areas are
not indicated. There is no intent to imply either undifferentiated cortex o r the existence of only single
sensory/motor fields. Note the low ratio of isocortex to limbic-olfactory cortex in these brains, especially the
small tenrec brain.

tures than that of Erinaceus. These authors
conclude that Erinaceus is probably "not a
typical representative of a real basal insec-
tivore" (Zilles a n d Rehkämper, 1988;
emphasis in the original). Only in a context
where evolution is presumed to progress
from simple to complex, from least en-
cephalized to most encephalized, and from
generalized, inflexible and inefficient in
function to specialized, flexible and highly
efficient in function, can the search for the
absolutely simplest mammalian brain be
equated with the search for the ancestral
brain.
There are two general attributes shared
b y essentially all the basal insectivores con-
sidered primitive in brain organization that
should cause us to be cautious about gen-
eralizing from them. First, each of the can-
didate exemplar species inhabits a noctur-
nal-fossorial niche. This is probably no
accident. This adaptation has likely pro-
duced secondary reduction or dedifferen-
tiation of the visual system and a corre-
spondingly heavy reliance on the olfactory
system. Evolutionary reduction or degen-
eration of an essentially unused sense
modality may induce dedifferentiation, but
this does not likely follow an exactly
reversed phyletic trend and may produce
structural features that are quite distinct
from ancestral features. How can we be
sure that the relatively undifferentiated
state of the cortex of these species is rep-
resentative of a retained primitive state
rather than a recent specialization?
Second, these exemplar species also rep-
resent the very lowest limits of mammalian
brain size. This is a problem because many
measures of structural complexity appear
to be strongly correlated with brain size
(Tower, 1954; Haug, 1987; Deacon, 1990a;
and see the following section). Nearly all
the attributes of "primitiveness" of mam-
malian brains are also typical attributes of
very small brains, while those of "advance-
ment" are only expressed in relatively large
brains. Progressivetrends measured with
respect to these small insectivore species
a r e significantly confounded with t h e
effects of differences of scale. Also if there
has been prolonged selection f o r size
reduction in these species there may also
be simplifications of brain structure of a
secondary character which d o not neces-
sarily follow a reverse phylogenetic trend.
Cladistic approaches
T h e cladistic approach to identifying
evolutionary trends offers some hope of
resolving these ambiguities and avoiding
the trap of implicit progressionism. By
replacing the assumption of evolutionary
deyelopment and increase in complexity
with a simpler empirically defined dichot-
omy between conserved and derived con-
ditions one can arrive a t a relatively
unbiased criterion for identifying evolu-
tionary trends. T h e particular character-
istics of the trait are irrelevant, only its
presence or absence in different groups is
important. By pairwise comparison of the
presence o r absence of traits between
species in progressively more distant out-
groups it is possible to decide which traits
can be operationally defined as derived and
which can be defined as ancestral o r con-
servative. Cladistic analysis has wide accep-
tance as a means for reconstructing phy-
ietic relationships between lineages, but it
has also been used extensively to trace the
ancestry of specific traits. It has been par-
ticularly useful for deciding between alter-
native accounts of a trait's evolution
because it provides a measure of parsi-
mony. For example, Northcutt (1984) uses
the number of mutational events that must
be postulated in order to explain the dis-
tribution of certain vertebrate brain traits
according to different theories to decide
which of these theories provide the most
parsimonious accounts.
T h e Achilles heel of this approach with
respect to brain evolution is that it will
inevitably tend to favor identifying rela-
tively undifferentiated forms as more
primitive and differentiated forms as more
derived. A structure lacking differentiat-
ing features will tend to be glossed as sim-
ilar across a wider range of species than
one exhibiting a number of easily discrim-
inated features. As a result, despite its
apparently unbiased definition of polarity,
the cladistic approach may be biased, so as
to pick out more generalized and less dif-
ferentiated traits as characterizing a com-
mon ancestor. Evolutionary regression in
certain lineages is potentially a source of
misleading bias as is the correlation of
absolute brain size with structural com-
plexity. Additionally, this approach is sen-
sitive to the effects of convergent or par-
allel evolution. It will be argued below that
parallelism is a major feature of mammal
brain evolution.
Nonetheless, the cladistic approach is in
some ways self-correcting in this regard. It
can be useful in discerning some of these
biasing influences by using multiple sources
of information pooled to establish most
parsimonious descent relationships and
then reanalyzing individual trends. For
example, the relative primitiveness of the
"basal insectivore" brain can be tested with
respect to three outgroups of mammals
whose phylogenetic affinities a r e well
known through other cladistic analyses: the
marsupials and the two living monotremes,
t h e platypus Ornithorhinchus a n d t h e
echidna, or spiny anteater, Tachyglossus.
Many of the characteristics of Erinaceus'
brain, including apparent adjacency of
projection areas, minimal association cor-
tex, high ratio of olfactory-limbic cortex
to isocortex, poor laminar distinction, poor
granularization and poor differentiation of
architectonic areas, are not exhibited in
the brains of larger marsupials and mono-
tremes. Have the apparently m o r e
advanced traits also found in these out-
groups evolved independently in the larger
brains of all the mammalian lineages? T h e
more parsimonious interpretation is that
many of these traits were present in some
form in the common ancestor of all mam-
malian groups long before the recent
eutherian radiations. T h a t they fail to be
exhibited by some of the brains in the
eutherian lineage (e.g., basal insectivoresj
and some brains in the marsupial lineage
(e.g., Didelphis virginiana) is not sufficient
evidence to assume that they are derived.
 Kaas (1989) applies an implicit cladistic
approach to determine which cortical areas
in all mammals can be traced via descent
from a common ancestor. He notes that in
all the major mammalian lineages (euthe-
rian and metatherian) there are distinct
visual, auditory and somato-motor projec-
tion areas within isocortex. H e concludes
that the common ancestor for all these lin-
eages likely also possessed these differen-
tiated projection areas and not just an
undifferentiated protoisocortex. Based on
this evidence he rules out a widely cited
theory of cortical evolution proposed by
Sanides (1970) that is based on the assump-
tion that generalized undifferentiated iso-
cortex preceded specialized sensory-motor
projection cortices in the course of cortical
evolution. However, to be more explicit,
what has been demonstrated is that dis-
crete somatic, auditory and visual projec-
tion areas are expressed in mammal brains
under all existing conditions and sizes,
whereas some areas, particularly many
association areas, fail to be expressed under
many conditions, specifically in small brains.
T h e classic view that association cortex
is new in comparison t o projection cortex
in part derives from the apparent lack of
association cortex in basal insectivore brains
(but this assumption is criticized below) and
its progressive domination of the cortical
surface in "advanced" mammals. How-
ever, some of the larger marsupials and
even the echidna appear to exhibit signif-
icant expanses of association cortex in
addition to primary sensory-motor projec-
tion areas. Apparently, under similar
developmental conditions- large brain
size-this trait is expressed in every lin-
eage of mammals. T h e common conditions
required for expression of this trait in all
three lineages also lends confidence to the
claim for homology as opposed to parallel
homoplasy.
T h e failure of basal insectivore brains to
exhibit distinctly segregated association
areas is not sufficient evidence to deny that
this trait is a shared ancestral trait. None-
theless the appearance of segregated visual,
auditory and somato-motor areas in all
mammal brains is sufficient evidence to
consider them as shared ancestral traits.
Lack of positive evidence is not sufficient
to deny homology but the availability of
positive evidence is sufficient to establish
it.
This can also be applied to questions con-
cerning the origins of somato-motor areas.
Lende (1969) demonstrated that in Didel-
phis the somatosensory responsive cortex
and the electrically excitable motor cortex
exhibited complete overlap and that in Eri-
naceus there was a large region of overlap.
More recently some degree of overlap has
also been demonstrated in rats (Donoghue
et al., 1979). In carnivores and primates
(and probably ungulates) these areas are
adjacent but completely segregated into
distinct parallel somatotopic and muscu-
lotopic maps. Lende also argued that there
was even some overlap of visual and audi-
tory cortical areas in the opossum (although
this finding has not been replicated). This
suggested to him that the ancestral state of
cortex was characterized by poor areal dif-
ferentiation in which all the sensory modal-
ities exhibited nearly complete overlap with
one another. However, at least one larger
Australian marsupial, t h e brush-tailed
opossum Trichosurus, exhibits considerable
segregation of somatic and motor fields
(Haight and Neylon, 1978, 1979) and the
monotremes appear to exhibit complete
segregation of somatic and motor areas.
All of these facts- argue against assuming
that the primitive condition was undiffer-
entiated and completely overlapping and
suggest that at least some degree of seg-
regation of these functional zones char-
acterized the common ancestor of all mam-
ma1 groups.
But negative evidence can be cited to
support the view that the segregation of
somatic and motor modalities is a conver-
gent trait. This evidence comes from vari-
ations in somatotopy of the sensory and
motor maps in the different groups. In most
eutherian mammals studied the two fields
are arranged as mirror images of one
another with respect to their common bor-
der, and exhibit this pattern even in species
where there is considerable overlap of the
two areas. However, in edentates and mar-
supials the two maps appear to be arranged
in parallel as well as overlapped (Dom et
al., 1971; Lende, 1963, 1969; Magalhães-
Castro and Saraiva, 1971; Royce et al.,
1975; Saraiva a n d Magalhães-Castro,
1975), and in a megachiropteran bat (Pter-
opus poliocephalus) the somatic map appears
inverted from that typical of most other
eutherian mammals (Calford et al., 1985).
T h e monotremes appear to exhibit char-
acteristics found both in some eutherian
and in som'e marsupial brains (Bohringer
and Rowe, 1977). Furthermore, the pat-
tern of thalamocortical connections to these
areas differs in eutherian and marsupial
brains.
This negative evidence is inconclusive
because the differentiation of map orien-
tation could occur independent of the seg-
regation of somatic and motor areas. T h e
unique status of the fox bat and edentate
somatic maps in comparison to other mam-
malian groups suggests that this is the case.
Map orientation appears to be a derived
condition in these species. Variation of this
trait occurs against the background of
somatic and motor map segregation as an
apparently older and more conservative
trait. T e only placental and marsupial
mammals that do not exhibit segregation
of somatic and motor projection areas also
have relatively small brains. This further
suggests that this is a derived condition
contingent on small size and not the ances-
tral condition.
Problems with these comparisons of cor-
tical areas stem from the fact that the traits
under consideration are not simple and the
variables that correlate with the differen-
tial expression of these complex traits have
not been controlled for in the analysis. T h e
most important of these variables is brain
size, but other factors are also clearly
involved with regard to more subtle fea-
tures, such as map topography. Failure to
control for these factors inevitably leads to
their being confounded with descent rela-
tionships despite the fact that cladistic anal-
ysis itself does not prejudge the primitive
or advanced status of a trait. T h e differ-
ential expression of a large number of traits
with respect to brain size or the differential
expression of traits in brains with respect
to sensory specializations can be a serious
problem for cladistic analyses because it
vastly increases the probability of conver-
gence and parallelism. In fact, many of the
"advanced" traits of eutherian mammal
brains could have been inherited from the
common ancestor of eutherian mammals
even if that ancestor failed to exhibit any of these
traits.
All three mammalian groups have likely
inherited neural developmental con-
straints and tendencies from a common
ancestor that are expressed differentially
in different contexts. It is possible that the
"initial" eutherian brain possessed the
developmental information for these traits
but failed to express them because certain
other conditions of their expression were
not met. Below it will be argued that the
small size of these brains precludes the
developmental expression of cortical par-
cellation processes necessary to produce
multiple highly differentiated cortical
areas. Also the regression of the visual sys-
tem in basal insectivores may f u r t h e r
undermine these processes. Despite the fact
that ancestral traits might not be expressed
in an intervening lineage there need be no
interruption of their descent t o subsequent
lineages, and their disappearance o r reap-
pearance in certain lineages cannot be
attributed to distinct mutation events and
treated as distinct derived conditions. We
should be especially wary of this possibility
in the choice of traits included for cladistic
analysis.
This again underscores the importance
of thinking of homologies in informational
terms. Even if we were to miraculously learn
the details of morphology of the brain of
the true eutherian ancestor we would per-
haps still be a long way from understanding
the initial conditions embodied in that initial
brain that still influence the structure and
the evolution of modern brains. What we
ultimately want to know is what information
was embodied in the initial brain and in
the developmental mechanisms that built
it.
Recapitulationism
During embryogenesis there is a definite
progression from smaller poorly differen-
tiated structures to larger highly differ-
entiated structures. Large species with rel-
atively differentiated brains must inevitably
pass through developmental stages in which
their brains are small and poorly differ-
entiated. Consequently, t h e embryonic
stages of larger more differentiated brains
will inevitably bear some superficial resem-
blance to the adult stage of small poorly
differentiated brains. Structures that dif-
ferentiate later in development will thus
appear to be added to an otherwise com-
mon substrate. Recapitulation assumes that
adult structures in primitive species are
homologous to embryonic structures in
advanced species. Subsequent modifica-
tions of brain structure have been added
in the more "advanced" species by extend-
ing the ontogenetic process to include
additional later stages. This process of ter-
minal addition was presumed to link the
evolution of species to development in such
a way that a scale of increasing complexity
in evolution was the inevitable outcome of
a progressive increase of developmental
information. Evolution is explained as an
augmentation of ontogenesis and more
"advanced" species are literally assumed to
be further developed.
Despite the enormous theoretical power
of this synthesis, the weight of comparative
and ontogenetic evidence that has accu-
mulated against this doctrine in the last
century is overwhelming. Ontogenetic dif-
ferences that distinguish different lineages
may occur at any stage of development and
are clearly not constrained to occur in lin-
ear sequence with increasing phylogenetic
.divergence. Although larger creatures tend
to exhibit longer ontogenesis than smaller
creatures, larger creatures d o not have
additional stages added on and highly
derived members of a lineage d o not show
more developmental stages than highly
conservative members; differences in
development appear at many correspond-
ing stages. However, despite the patent
failure of this paradigm, numerous unrec-
ognized recapitulationist assumptions still
persist in the literature about brain evo-
lution, primarily in the form of tacit ter-
minal addition assumptions.
Early recapitulationist theories of brain
development suggested that as children
matured they passed through stages of cog-
nitive and emotional development that
corresponded to distinct "grades" of ani-
mal consciousness from reptilian to mam-
malian, from primitive mammal to pri-
mate, from primate to primitive human,
and finally through the ascending stages
from "primitive savagery" to modern civ-
ilization (e.g., Spencer, 1870; Baldwin,
1895). Various primitive human societies
and criminals were viewed as arrested at
some prior stage of development. Although
the recapitulational structure of the brain
was assumed by many prominent 19th cen-
tury and early 20th century neurologists
(e.g., Paul Broca, John Hughlings Jackson,
Ivan Pavlov, John Sherrington, and Sig-
mund Freud) probably the major catalyst
for the formation of a comparative ana-
tomical version of this theory came as a
result of the synthesis of two sources of
neuroanatomical evidence just subsequent
to the turn of the 20th century.
Paul Flechsig's (190 1) analysis of myelin-
stained tissue from human fetuses at var-
ious stages of development demonstrated
a progression of myelination of isocortical
areas that began with primary sensory and
motor areas, continued to belt zones around
these areas and culminated in relatively late
myelinating association areas (see Fig. 4).
This sequence was presumed to correlate
with developmental trends in which basic
sensory-motor abilities mature early in
childhood and the "highest" intellectual
abilities only appear late in developmeht.
It was also presumed to correlate with an
evolutionary sequence from species with
only crude sensory-motor habits a n d
responses, to species with the capability of
complex and flexible associational learning
abilities. T h e most developed associated
areas were assumed to be the newest in
evolutionary terms and the last to develop
in ontogeny.
At roughly the same time .comparative
anatomists, using preparations that visu-
alized neuron cell bodies, produced maps
of the distinguishable cytoarchitectonic
areas of the cerebral cortex for a number
of mammalian species which appeared to
demonstrate homologues for primary pro-
jection areas in all species, but no homo- lateral view
logues for many human association areas
in monkeys and no homologues for many
monkey association areas in other mam-
mals (e.g., Campbell, 1 905; Brodmann,
1909). It clearly appeared as though the
developmental t r e n d recapitulated a
sequence of additions of new cortical areas
leading up to the human brain. New, more
developed 'association areas were appar-
ently added to the brain of succeeding
species at the end of their maturational
development. T h e unusually long postna-
tal brain development of humans could also
be explained on the basis of the extra stages
of brain development that were appended
to, human ontogeny.
These assumptions corresponded with
the neuropsychological doctrine of the
time. It was assumed that the moment to
moment processing of sensory input
retraced this same hierarchy, developing
from the crude registration of sensory
information in projection areas, to the con-
struction of a perceptual gestalt in sensory
psychic areas, and finally to the elaboration
of multimodal associations with respect to
different remembered vercevtions, actions
and emotional experiences in association medial view
areas. Primitive animals and young chil- FIG. 4. Flechsig's myelogenesis figure of the human
dren only progressed through the initial brain is redrawn from the original leaving out Flech-
stages of this cognitive hierarchy. Although sig's numerical designation of myeloarchitectonic
the developmental recapitulation assump- fields. T h e darker areas represent the areas that mye-
tion has been abandoned, a more elaborate linate earliest in development and the white areas
represent the areas that myelinate latest. Insular cor-
version of this basic hierarchic functional tex is partially exposed. Note the progression from
interpretation remains the dominant con- primary to secondary to association areas of cortex.
temporary theory of sensory processing Note also the early myelination of limbic cortical areas
(e.g., Mishkin a n d Appenzeller, 1987; and pathways.
Maunsell and Van Essen, 1983), despite
many growing inconsistencies and t h e
availability of alternative interpretations
(e.g., Brown, 1988; Deacon, 1989a; Dia- will primarily address the issue of the
mond, 1982; Optican a n d Richmond, developmental sequence, but will return to
1987). the issue of the terminal addition of cor-
However, in hindsight we can see fun- tical areas in a later section.
damental flaws in both forms of evidence An alternative explanation for the pri-
for this correlation of ontogenetic devel- mary-secondary-tertiary hierarchy of my-
opment with apparent phylogenetic devel- elination of cortical areas can be derived
opment. Ultimately I will argue that both from a correlation between the total level
derived from a failure to control for factors of adult myelination achieved by these
having more to do with brain size than with structures and their apparent develop-
phylogenetic progression. In this section I mental schedule. T h e early myelinating
areas are also the most heavily myelinated
in the adult and the latest myelinating areas
are the least myelinated in the adult
(Bishop, 1959; Sanides, 1970). This rule
also applies to noncortical structures: the
relatively poorly myelinated reticular for-
mation of the midbrain exhibits one of the
latest and longest cycles of myelination of
any system (Yakovlev and Lecours, 1967)
despite the fact that it is without doubt one
of the most conserved structures in the ver-
tebrate brain. This fact clearly contradicts
the recapitulationist assumption.
There are two possible interpretations
of this correlation between total amount
of myelination and the developmental time
course of myelination. First, since these
assessments of myelination are based on
myelin-stained tissue sections in which more
densely myelinated tissue stains darker,
there may be a level of nearly complete
staining opacity reached at an early devel-
opmental stage in areas that exhibit max-
imal myelination whereas this level of
staining opacity may never be achieved by
very poorly myelinated areas. In this case
the apparent heterochrony could be largely
illusory. Alternatively, the deposit of my-
elin on axons destined to be heavily myelin-
ated could take place at an absolutely faster
rate (which appears to be indicated by the
data of Yakovlev and Lecours, 1967) and
could begin earlier. It is probably an
important corollary that the most heavily
myelinated fibers are also often the largest
diameter axons that project relatively long
distances o r to highly specific targets.
There is also an important correlation
between brain size and primitive-advanced
comparisons. Small insectivore and rodent
brains appear to be generally less myelin-
ated overall and exhibit less myeloarchi-
tectonic differentiation from cortical area
to cortical area than the larger brains of
primates (Sanides, 1970). Therefore if
myelination is to be used as a ruler of pro-
gression then the least myelinated areas
should be considered the more primitive
areas and the most myelinated areas the
more advanced cortical areas (Bishop,
1959). This runs exactly counter to the
apparent developmental progression.
This apparent phyletic myeloarchitec-
tonic trend as well as other architectonic
trends led Sanides (1969, 1970, 1972) to
propose that the terminal addition of cor-
tical areas in mammalian evolution might
actually be the reverse of that proposed by
the traditional theorists—progressing from
association areas to secondary areas t o pri-
mary areas as the most highly developed.
Although not a recapitulationist theory,
because it makes no claims for develop-
ment, it does nonetheless assume terminal
addition in a phylogenetic sense, and an
implicit progression from primitive t o
advanced forms based upon the addition
of more highly differentiated structures.
T h e neuropsychologist Jason Brown (1977,
1988) has elaborated a self-consciously
recapitulationist theory of cortical func-
tion that is based upon Sanides' model of
phylogenetic progression, in which
"microgenetic" processes of sensory anal-
ysis proceed in a series of stages from lim-
bic to association to specialized cortical
areas rather than the other way around, as
is suggested in traditional models.
Both interpretations are based on mis-
leading correlations that confound a num-
ber of factors. T h e correlation between the
density of myelination in adults, the initi-
ation and rate of myelination in develop-
ment, and the overall level of myelination
in brains of different sizes suggests that all
of these apparent comparative trends may
have less to do with any evolutionary
sequence and more to do with certain con-
servative functional and metabo1ic rela-
tionships between axons of differing sizes
and the glia that form their myelin sheaths.
T h e developmental differentiation of the
brain occurs in the process of increasing
the size of the brain. T h e evolution of
increasingly differentiated mammal brains
also correlates with t h e evolution of
increasing brain size. The similarities
between brain development and brain evo-
lution may largely be the result of these
parallelisms. In both, the confusing role of
brain size and its many correlative struc-
tural scaling relationships underlies many
of the misidentifications of evolutionary
progress. T h e nature of some of these
underlying correlations will be the subject
of the next section.
 BRAIN SIZE
The influence of anthropocentrism
T h e significance of brain size is at once
the most broadly debated issue in the study
of brain evolution and probably also its most
ubiquitous, misunderstood and troubling
feature. More has been written about brain
size than about any other topic concerning
brain evolution. Like the notion of evo-
lutionary progress, interest in brain size
owes much to its apparent importance for
understanding human brain evolution.
With a brain roughly three times larger
than a primate of our size should possess,
it is natural to assume that brain enlarge-
ment must hold the key to human unique-
ness. But is brain enlargement symptom o r
cause in this transformation? Is relative
brain size alone the significant difference
o r is it a superficial consequence of more
fundamental changes in brain organiza-
tion? Size is also the easiest feature of the
brain to study and so lends itself to broad
comparative studies and studies of other
possible correlates to brain size that might
be of interest to researchers who otherwise
have little neuroscientific training. But the
tendency to terminate the analysis of brain
difference with measurements of brain size
is a significant impediment to progress in
the investigation of brain evolution, pre-
cisely because issues of brain size are insep-
arable from issues of function and internal
organization in some very fundamental
ways.
T h e role of brain size in brain evolution
appears deceptively simple. If the brain is
a computing device of some kind, then an
increase in component processing ele-
ments should correlate with an increase in
information processing capacity. This intu-
ition appears to be borne out by the unsys-
tematic observation that species with brains
at the small end of the size range for ver-
tebrates exhibit mostly simple and stereo-
typic behaviors compared to those with
brains toward the large end of the spec-
trum. This observation is not totally sat-
isfactory. Some mammal brains exceed the
human brain in total volume and neuron
number-for example, elephant and whale
brains. However, these species represent
the largest mammals on earth. If we think
of the brain as a computer and the body
as the many users that are on line, vying
for processing time and memory storage,
then it becomes obvious that the effective
information processing capacity available
for any particular function is constrained
by the number of competing demands from
other sources. This has suggested to many
that the ratio of brain to body is a more
significant measure of available informa-
tion processing capacity. Despite the fact
that they have absolutely larger brains, ele-
phants and whales have a much lower ratio
of brain to body than humans. But this
observation is also unsatisfactory. Very
small birds and mammals have a higher
ratio of brain to body size than humans
and an even higher ratio of neuron num-
ber to body size.
A satisfactory account of comparative
brain size that ranked humans on top (and
thereby preserved the intuition underlying
the Anthropocentric Maxim) was discov-
ered at the end of the 19th century in the
form of allometric analysis. Since that time
the use of "subtraction criteria" based on
empirical brain and body size trends have
been assumed t o define that portion of the
brain mass that is functionally correlated
with information processing demands of
the body. Deviations from these trends have
been assumed to respectively indicate
excess o r dearth of mental capacity (but
see criticisms below). T h e importance of
allometric analysis for the investigation of
patterns of relative growth and the sec-
ondary correlates of differences in size is
paramount, not just as a criterion of sub-
traction, but as a tool for drawing attention
to the ways that biological processes can
be affected by changes of scale. Allometric
analysis has produced some remarkable
insights into the problem of relative growth
and has demonstrated some remarkably
regular patterns of size-related brain vari-
ation from species to species and from evo-
lutionary epoch to epoch.
T h e more detailed pursuit of allometric
relationships has shown that differences of
brain size have consequences at every level
of neuroanatomical and neurophysiologi-
cal organization. Not all features of the
brain scale isometrically with size changes
in brain evolution. This has serious func-
tional consequences that have yet to be
appreciated-much less understood-and
serious methodological consequences for
comparative studies because it immensely
complicates t h e task of determining
homology. A failure to appreciate the
numerous architectonic and functional
consequences of differences in brain size
lies at the heart of numerous misunder-
standings about brain evolution, including
issues of progression and the question of
brain size evolution itself.
Is there a trend toward increasing
encephalization?
One of the earliest discoveries concern-
ing brain evolution in mammals was that
mean brain size and relative brain size have
increased with respect to our reptilian
ancestors and have increased since the
beginning of the great eutherian mammal
radiations. This seems to be a clearly pro-
gressive trend and suggests that brain size
itself may be an adaptation under selection.
But is it? If it is, then is there selection for
total brain size o r for relative brain size?
And what kind of evidence would be nec-
essary to demonstrate one o r the other?
T h e accepted answers to these questions
have been phrased in terms of the evolu-
tion of intelligence, and have changed little
in form since well before the turn of the
century.
Brain enlargement, both in absolute and
relative terms, has typically been referred
to as encephalization. Beginning with the
work of Dubois (191 3) the term became
associated with a specific mathematical
index: the measure of the relative devia-
tion of the ratio of brain to body size in a
species from the expected ratio for an aver-
age animal of the same body size, based on
trends for a given taxonomic group or for
some baseline comparison group (Bonin,
1937; Dubois, 19 13; Gould, 1966; Jerison,
1973: Stephan, 1969). Two major appli-
cations of these measures of encephaliza-
tion are the assessment of taxonomic and
phylogenetic differences of relative brain
size and the assessment of species differ-
ences in intelligence. Whether or not there
is any meaningful relationship between rel-
ative brain size and intelligence is open to
serious question. T h e r e are distinctly dif-
ferent brain-body trends for different
mammalian taxa that can all provide equally
valid-but not concordant-measures of
encephalization for an individual, t h e
somatic fraction of brain size that is pre-
sumed to be allometrically "subtracted" in
the estimation of encephalization cannot
be a simple linear factor as is often assumed,
and deviations from the empirical trend
cannot automatically be assumed t o cor-
relate with mental adaptation as opposed
to metabolic, ontogenetic o r somatic adap-
tations (Deacon, 1990a, b). More impor-
tantly, the assumption that intelligence—
much less comparative intelligence-is a
single measurable scalar quantity is highly
dubious from either a neurological o r an
evolutionary perspective and has never
been adequately supported by comparative
intelligence testing (MacPhail, 1982; Gard-
ner, 1983; Hodos, 1988; Deacon, 1990a).
This issue has been extensively discussed
and debated elsewhere and so will not be
reviewed here, except to point out both
the obvious progressionist and anthropo-
centric assumptions that are inextricably
bound up with the entire enterprise. Only
the issues surrounding phylogenetic inter-
pretations will be considered here.
Since the appearance of the first verte-
brates, brains and bodies in many lineages
have enlarged by orders of magnitude. T h e
relative sizes of brains and bodies have also
changed. For an animal of a given body size
the ratio of brain to body size has also
increased in a number of lineages, though
not all. These general trends are capped
by the evolution of mammal brains. T h e
largest brains ever to have existed are now
possessed by whales and the most extreme
values of encephalization ever to have
existed are now exhibited by dolphins and
primates-particularly humans. Within any
taxonomic group of living vertebrates there
is a negative allometric relationship
between brain size and body size, such that
adult individuals with larger body sizes tend
to exhibit lower ratios of brain to body size
than smaller individuals. T h e scaling rela-
tionship is approximately linear when ren-
dered in logarithmic coordinates but the
particular slope and y-intercept of this line
FIG. 5. Allometric patterns of comparative vertebrate brain size and mammalian brain growth. Graph A,
on the upper left, depicts convex polygons that enclose all points of brain and body size for four major
vertebrate classes (from Jerison, 1973) along with an approximation of the polygon that would have enclosed
the stem mammals. Note the incredible mammalian brain and body size expansion from this precursor group.
Note also the overlap of teleost fishes and lizards and of birds and mammals and the lack of a scala naturae
trend from fish to mammals. Graph B, on the upper right, shows the trend line for carnivores and for the
domestic dog breeds. Arrows indicate measures of encephalization o r somatization for a small dog with respect
to the carnivore trend. This is intended to show that "encephalization" differences do not necessarily imply
selection on brain traits. Graph C, on the bottom left, shows an ontogenetic developmental trajectory for
brain and body growth in two typical mammals of different body size. T h e prenatal phase overlaps completely
for most species. Graph D, on the bottom right, shows ontogenetic curves for different mammalian species
and their relation to interspecific trends. Note that ontogenetic lines overlap for different size species during
the early ontogenetic phase. T h e shift of ontogenetic curves that distinguishes primates, cetaceans and ele-
phants from other mammals is shown in gray.

differs depending on the taxonomic group
under consideration. Proposals for
explaining the regularity and slope of these
trends include the possibility that brain size
tracks body surface (Snell, 189 1; Dubois,
19 13; Jerison, 1973), that brain size is con-
strained by metabolic capacity which is also
negatively allometric (Martin, 198 1; Arm-
strong, 1983),that because brain is derived
from embryonic ectodermal tissue, the
same growth control mechanisms may con-
trol mitosis in brain and body surface struc-
tures (Deacon, 1990b), o r that target body
size is controlled by neuron number via a
mechanism common to all mammals, and
possibly all vertebrates (Deacon, 1990b).
Ultimately no single explanation can
account for the substantial differences in
scaling relationship exhibited at different
taxonomic levels of analysis. Within a
species the allometry is strongly negative
with slope on the order of 0.1 to 0.2,
whereas within a whole order o r whole ver-
tebrate class the allometric slope is often
in the range of 0.6 to 0.8. See Figure 5a
and b.
T h e brain-body allometries of the dif-
ferent living vertebrate classes appear to
be distributed bimodally. T h e homeo-
thermic classes-birds and mammals—
tend to scale together and the poikilother-
mic classes-fish, amphibians and rep-
tiles-tend t o scale together, with homeo-
therms exhibiting a much larger
percentage of brain to body a t any given
body size (see Fig. 5a). In the evolution of
birds and mammals there has clearly been
an increase in encephalization over the
ancestral reptilian condition as repre-
sented by modern reptiles. But using mod-
ern species as exemplars for ancestral rela-
tionships it cannot be said that there has
been a steady increase in encephalization
from fish to amphibians t o reptiles t o birds
and mammals. In fact, some of the most
"primitive" fishes, the sharks and rays,
comprising the Chondryichthes, exhibit
levels of encephalization that exceed all
other fishes, amphibians and reptiles, and
overlap the ranges for birds and mammals
(Bauchot et al., 1979) . There is no clear
scala naturae of encephalization. In con-
trast, relative conservatism of the enceph-
alization relationship is demonstrated by
the extensive overlap of encephalization in
different vertebrate classes.
Discerning the progressive encephali-
zation of mammals relative to their reptil-
ian ancestors involves more subtle distinc-
tions, but the major step across this gap
appears to have already been taken by the
time of the common ancestor of metatheri-
ans and eutherians (Ulinksi, 1986). In com-
parison with other mammalian lineages the
marsupials and the insectivores appear to
occupy the low end of encephalization, but
the monotremes appear on a par with the
mean for eutherian mammals. If the small
brained basal insectivores and marsupials
are characteristic in this regard of most
stem mammalian groups then most other
mammalian lineages have exhibited pro-
gressive encephalization. Such a trend is
demonstrated in the fossil record and has
been used as support for the claim that
there has been a progressive trend toward
increased intelligence in all these lineages
(Jerison, 1973).
T h e relatively lower encephalization of
many small bodied forms including basal
insectivores and rodents, may reflect ges-
tational trade-offs involving large litter sizes
and rapid reproductive rates characteristic
of small r-selected species. These repro-
ductive specializations have been corre-
lated with gestational constraints that affect
brain growth (Martin, 1983; Deacon,
1990b). Similar factors may also be impor-
tant for understanding marsupial brain size
development. It is possible that low esti-
mates of "basal" encephalization may be
misleading if they incorporate superim-
posed developmental trade-offs that sec-
ondarily reduce encephalization. We
should expect that progressive removal of
these constraints in lineages radiating into
K-selected, larger-body-size niches might
result in an apparent " rebound" of
encephalization. A similar "rebound" effect
has been suggested by Gould (1975) and
Deacon (1990b) in response to intense
selection for increasing body size in evo-
lution. Breeding experiments demonstrate
that selection on body size produces body
size increase in successive generations with
little correlated increase in brain size
(Atchley, 1984; Riska et al., 1984). Deacon
(1990b) argues that after an initial rapid
evolution of increased body size effected
by modifications of peripheral hormonal
mechanisms, continued stabilizing selec-
tion would tend to produce complemen-
tary brain size increase as a more stable
central determiner of target body size.
T h u s t h e rapid radiations into m o r e
K-selected, large-body-size niches t h a t
characterized many mammalian lineages in
the Eocene may have provided a biased
sample of species for comparison to more
modern lineages.
T h e case for an increase in encephali-
zation in primates, elephants and cetaceans
is strengthened by independent evidence.
From very early in embryogenesis all these
species exhibit approximately double the
ratio of brain to body size found in any
other mammal group at a comparable
developmental stage (Count, 1947; Sacher
and Staffeldt, 1974; Martin, 1983; Deacon,
1990b). This difference is evident at the
earliest stages in which brains are discern-
able in the developing embryo and so rules
out explaining this encephalization in terms
of the terminal addition of neural tissue
late in development (see Fig. 5c, d). Curi-
ously, the trajectory of brain-body growth
for all three groups closely overlaps for the
entire fetal period, suggesting a common
brain growth mechanism. T h e brain-body
growth trajectories of the remainder of the
eutherian mammals also all appear to share
a common fetal trajectory, suggesting that
they all share a different common mech-
anism for determining brain growth. As
with t h e encephalization difference
between homeotherms and poikilotherms,
this. embryological encephalization differ-
ence distinguishing primates, dolphins and
elephants from the remainder of the
eutherian mammals appears as a distinct
discontinuity without intermediates.
As a final comment on the encephaliza-
tion issue it should be pointed out that the
term itself reflects an underlying bias that
is part historical and part theoretical. Early
writers often did not clearly distinguish
absolute brain size from the relation of
brain size to body size in their discussions
of brain evolution (Gould, 198 1). T h e ulti-
mate interest has of course all along been
the explanation of human brain size. But
measures of brain size with respect to body
size are inherently relational. Increased
encephalization is also decreased somati-
zation, and vice versa (see Fig. 5b). One
need not necessarily assume neurological
explanations for differences in this rela-
tionship. Although breeds of dogs differ
enormously in degree of encephalization
(from small highly encephalized dogs to
large poorly encephalized dogs) no one
doubts that body size is the selected vari-
able and brain size the relatively less flex-
ible parameter. In fact, breeding experi-
ments selecting progeny on the basis of
either extremes of brain size o r extremes
of body size demonstrate that selecting for
body size produces a poor correlated
response in brain size whereas selecting for
brain size produces a highly correlated
response in body size (Roderick et al., 1976;
Fuller, 1979; Atchley, 1984; Riska et al.,
1984; Kruska, 1987). Given that a large
fraction of the variance in "encephaliza-
tion" within a species can be a consequence
of selection on body size, why should this
not also hold for cross-taxa comparisons?
Body size is a highly flexible and ecologi-
cally significant variable, whereas brain size
is a relatively inflexible and as yet poorly
understood variable that may o r may not
correlate with differences in behavior. T h e
search for changes in brain structure that
correlate with addition or subtraction of
neural tissue in evolution in order to
account for encephalization is for this rea-
son probably misguided; we might just as
well look for addition o r subtraction of the
many parts of the rest of the body.
Disentangling allometry and progression
When organisms get larger, either dur-
ing development o r in the course of evo-
lution, all features of the organism are not
scaled up isometrically. Even more trou-
blesome for the comparative anatomist is
the fact that homological relationships can
appear to change with evolutionary changes
in size. Different structures may radically
change size with respect to one another o r
alter their relative position, structures may
radically change shape due to unequal
growth rates among their parts o r single
structures may divide o r differentiate to
become two o r more distinct structures.
This is the source of one of the most insid-
ious problems in evolutionary theory: the
confusion of size related changes with evo-
lutionary advancement. T h e secondary
effects of change of size can include the
apparent addition of new structures to old
or the appearance of increased complexity
in existing structures. It may be difficult t o
tell whether an increase in size has caused
old structures to differentiate and subdi-
vide o r whether the addition of new struc-
tures has caused an increase in size.
As D'Arcy Thompson pointed out in his
classic treatise on the effects of growth o n
form (1917), most mechanical forces,
material properties and structural relation-
ships do not change isometrically with
changes in size. Geometric effects are most
obvious — e.g., surface area to volume— but
also there are changes in the relative vis-
cosity of fluids, diffusion rates of mole-
cules, structural plasticity o r rigidity of
materials, rates of chemical reactions, etc.
Many of these non-geometric scaling allo-
metries result from the fact that ultimately
some components of organisms are of fixed
sizes (e.g., molecules and cells). In order to
maintain isometry of functional properties
across major changes in size it is nearly
always necessary for structures to enlarge
at different rates.
Allometric analysis can help control for
the influence of size, allowing one to com-
pare quantitative traits with the effects of
size subtracted. This "criterion of subtrac-
tion" is most often assumed to indicate that
some functional relation has been main-
tained in the face of the change in size.
This does not mean that such changes are
merely passive effects induced by the mass
of t h e organism. T h e y a r e inevitably
"internal" facultative or genetic adapta-
tions to the imbalances or weaknesses
induced by the change in size. Many of
these secondary adaptations may b e
encoded in the genome of the organism.
However, a trait that is somehow expressed
facultatively, in a size graded manner,
would have obvious advantages over one
that is specific to a given range of sizes. In
these cases size change should be consid-
ered the "primary" adaptation and the
correlated reorganizations of structure can
be considered "secondary."
A genetically encoded, size-correlated
trait that has evolved in response to the
functional demands of size change is a par-
adigmatic example of a derived condition.
But it also represents a conservative fea-
ture to the extent that it is necessary to
preserve some ancestral functional rela-
tionship. Functional homology is main-
tained at the expense of structural homol-
ogy. T h e reverse scenario is also possible—
structural homology maintained by virtue
of change in supportive functions to keep
pace with the effects of size. Finally, it is
also possible for size change to be the "sec-
ondary" adaptation. A change in size can
be secondary to the production of some
correlated effect that has itself become the
trait of primary adaptive significance. This
latter possibility will be suggested in the
case of human brain size enlargement (see
last section).
In cases where size change is primary it
would be inappropriate to consider the
many secondary adaptations as progressive
trends. T h e fossil evidence clearly dem-
onstrates that with the demise of the dino-
saurs, small mammal species rapidly
adapted to fill niches for large bodied
forms. T h e mammalian radiations can be
seen as markedly asymmetric with respect
to body size (and correlated brain size). T h e
lower limit of mammalian body size has
probably not been significantly altered since
the Paleocene but the upper limit has prob-
ably been extended about a millionfold
compared to a typical basal insectivore!
Brain size necessarily followed this trend,
although the extension of the upper limit
of'brain size, due to its negative allometry
with respect to body size, has probably not
exceeded ten thousand times that of a typ-
ical basal insectivore brain. Parallel
enlargement trends characterized numer-
ous lineages of mammals.
I will argue that it is this remarkable par-
allelism, and not some progressive selec-
tion for increasing intelligence, that is
responsible for many pseudoprogressive
trends in mammalian brain evolution.
Larger whole animals were being
selected-not just larger brains—but along
with the correlated brain enlargement in
each lineage a multitude of parallel sec-
ondary internal adaptations followed.
Allometry of brain traits any levels
Mammalian brains range in weight from
around a gram to nearly ten thousand
grams. Even within a single lineage like the
anthropoid primates, in which individual
species share many strong similarities in
brain structure, there is more than a hun-
dredfold difference between the smallest
and largest adult brains. Yet most micro-
structural features change little in size from
brain to brain. T h e maximum sizes of neu-
ron and glial cell bodies increase slightly
from the smallest to the largest brains, but
nowhere near the thousandfold scaling of
the brains they comprise (Haug, 1987). T h e
functional constraints on cell volume no
doubt set an asymptotic upper bound on
cell size that the largest neurons are likely
approaching. T h e apparent tetraploidy of
the giant Betz cells of the human motor
cortex likely indicates that these cells are
already forced to come up with unusual
ways to circumvent certain functional lim- projection neuron rnyelin sheath

itations of their large size.

T h e constraints on neural size also affect
the scaling of higher-order multi-neuronal
structures. For example, the diameter of
cortical columns as well as the number of
neurons within each column seems to
remain almost constant across brain size
.
glial cell

smaller brain
variation (Rocket et al., 1980). This may
also be the reason that many larger scale
morphological features like cortical thick- larger brain
ness increase only slightly from the small-
est to the largest brains (Rocket et al., 1980).
As a cdnsequence the disparity between
microstructure organization and macro- rnyelin sheath
structure organization grows incredibly
with increasing size. Since the macro-
morphology of the brain, including
distinct homogeneous structures and their
various functional subdivisions, is derived
by ontogenetic processes that function at local circuit neuron
(e.g. granule cell)

the microscopic cellular level, this growing

scale difference is inevitably reflected by FIG. 6. Local relationships contributing t o cytoar-
changes of large scale structure. Some of chitectonic allometry are depicted in this figure from
these. morphological changes may reflect in Deacon (1990b). T h e top figure depicts the situation
a relatively small brain and the lower figure depicts
distinct adaptations to these new micro- these same relationships in a slightly larger brain. In
structural demands, but it is likely that the small as compared t o large brains projection neurons
majority are simply the inadvertent con- possess short, small diameter axons, with relatively
sequences of the same ontogenetic pro- less myelin, smaller cell bodies, lower neuron t o glia
ratio, higher neuron densities, lower ratios of local
cesses operating in a vastly larger brain. circuit neurons to projection neurons, smaller size
This is illustrated by what can be called differences between the smallest and largest neurons,
cytoarchitectonic and myeloarchitectonic allom- etc.
etry (Deacon, 1990a). T h e linear and vol-
umetric increase in scale of the brain with
respect to relatively more conservative lim- metabolic and neurotransmission demands
its of cellular structure impose new con- of such an enlarged axonal volume and sur-
straints on neural and glial functions. Con- face area the cell body of the neuron must
sider what must happen to homologous also be enlarged, but since it depends on
long projection neurons in brains of the glial cells surrounding it for its meta-
increasing size. In order to maintain sim- bolic support the relative number of glia
ilar transmission velocities and transmis- must also increase. T h e same constraints
sion integrity longer axons need to have are not experienced by small local circuit
larger diameters and thicker myelin neurons. Since local circuits remain rela-
sheaths. If the target area has also expanded tively constant in volume (increasing no
in volume (as is typically the case as well) more than a few hundred percent across
then the terminal arbor of a typical axon huge brain size differences) these neurons
must also increase. This can be a significant should have to change relatively little to
factor given the exponential differential compensate for size (see Fig. 6).
between linear dimensions and volumes Given these two extremes, it becomes
since it requires a tremendous increase in obvious that the local cyto- and myelo-
length and number of branchings of an architecture of many brain structures will
axon to fill a larger volume with the same reflect the influence of size. In general, in
density of synapses. T o keep pace with the large brains as compared to small brains
there should be a number of regular trends:
In large brains there should be (1) some
much larger cell types, but also a much
greater difference between the smallest and
largest cells, (2) a higher glia to neuron
ratio in most regions, (3) a decreased mean
density of neurons but an increase in the
range and variation of densities in different
areas and subareas, (4) a significant increase
in axonal and dendritic arborization to fill
the slightly increased volume of local cir-
cuits, (5) higher levels of myelination in
general but a greater difference from the
most to least myelinated areas and sub-
areas, and (6) since some areas may be spe-
cialized for longer projecting cells with
large soma and heavily myelinated axons
and other areas only for short projecting
cells or cells with small diameter, poorly
myelinated axons these differences will be
magnified between brain areas. T h e net
result will be greater architectonic differ-
entiation within an area and between areas
in large brains as compared to small brains.
Few if any of these changes are likely the
result of the evolution of new ontogenetic
mechanisms, but merely the local dynam-
ical responses of cells trying desperately to
do what they would do in any brain. We
can conclude from this that a n increase i n
architectonic complexity with size is not a reli-
able measure of progression and advancement,
either for comparison of the brains of different
species or for comparisons of different areas
within the same brain.
However, there are also a number of size
related changes for which architectonic
reorganization will be unable to compen-
sate. Probably the most significant among
these is a factor that can be called network
allometry (Deacon, 1990a). Network allom-
etry is essentially a geometric principle
analogous to surface to volume allometry.
T h e size of a network is a function both of
the number of nodes in the network and
the number of connections between nodes.
Networks with every node directly con-
nected to each other node can be consid-
ered to exhibit a high level of connectivity
whereas networks with each node directly
connected to only one or two others can
be considered low connectivity networks.
One measure of the average connectivity
of a network might be the average number
of nodes that must be passed through to
find a link between any two arbitrary nodes.
In all but the smallest o r lowest connectiv-
ity networks the number of connections
tends to vastly outnumber the nodes. If one
wants to increase the number of nodes in
a network while maintaining the same
average connectivity, then the number of
connections that have to be added with each
new node will grow factorially with each
addition. A factorial increase of this sort
will rapidly lead to astronomical numbers,
particularly in large highly connected net-
works, but even in networks with relatively
low connectivity very large changes in size
will produce the same result. Except in
minimally connected networks, it will
become increasingly difficult to continue
increasing the number of nodes within a
network and retain the same level of con-
nectivity. This concept in diagrammed in
Figure 7.
Now consider these facts about the cen-
tral nervous system: One neuron may be
connected to thousands of others, accord-
ing to some estimates; even in small mam-
malian brains there are probably b lions
of neurons; and there is a nearly tenthou-
sandfold difference in volume between the
smallest and largest mammalian brains.
These simple statistics make it clear that
network allometry must be one of the major
factors responsible for the differences in
organization and function that distinguish
large and small brains. But the brain is not
a maximally interconnected network. Even
in a brain with a billion cells each con-
nected to a thousand others at random the
average number of nodes se p aratin g any
two will be on the order of twenty, and
brains are not nearly so diffusely orga-
nized. Probably the majority of connec-
tions between areas of mammalian isocor-
tex and other cortical or subcortical areas
are reciprocal, and the connections within
the local circuits of the isocortex are prob-
ably highly re-entrant and relatively self-
contained within columnar modules. Also,
given the relative comparability of local
circuit structure of isocortex from species
to species, it is likely that intracortical con-
nections between columns may be limited
to neighboring columns and to specific tar-
get columns in other areas. It may then be network allometry network allometry
maintaining local maintaining global
a bit more useful to think of connectivity connectivity only connectivity

within the cerebral cortex in terms of

columnar modules as nodes rather than in
terms of individual neurons as nodes. A
separate network allometry might apply at
the columnar level since columns increase
in volume, number of axons and dendrites
but not neurons with increasing brain size.
Nonetheless, given the immense differ-
ences in scale that must be considered, even
a relatively poorly interconnected cortical
network will have to contend with connec-
tivity trade-offs in order to compensate for
network allometry.
There is clearly a significant increase in
the proportion of white matter to gray
matter in brains of ascending size, but this
is doubtless nowhere near what would be
required for connectional parity to be
maintained. I n order to evolve to significantly
larger sizes brains must decrease connectivity.
This trade-off undoubtedly has its costs.
The two most obvious costs of decreasing
IG. 7 . T h e problem of network allometry is rep-
connectivity with increasing size a r e Fresented by the example of a very simple network
reduced integration of distributed func- (figure from Deacon, 1990b). A series of nodes
tions and significantly increased transmis- (depicted as spheres) is connected reciprocally to each
sion and processing times. Larger brains are other (depicted by double arrows) in different size
not necessarily more efficient a n d more powerful networks with different extremes of connectivity.
Networks on the left exhibit low connectivity and
than smaller brains. In fact, these new func- those on the right exhibit maximum connectivity. N
tional costs of increasing size will demand = total number of nodes; C = total number of recip-
new secondary adaptations in order to rocal connections (note that in the nervous system
compensate in other ways. If a functional reciprocal connections are separate connections); Xn
area of cortex becomes enlarged in the = the number of other nodes to which any one node
is directly connected; Xc = the mean number of con-
course of evolution the mean interconnec- nections intervening between any two arbitrary nodes.
tivity of its columns will decrease. This will T h e growth of connections to nodes is a factorial
decrease the homogeneity and integrity of function of the number of nodes in a fully connected
activity patterns that can be maintained network and a linear function of the number of nodes
in a minimally connected network. Both low and high
within it and increase the time necessary connectivity networks require major functional and
for neural "calculations" involving the structural trade-offs with size increase.
whole area to be completed. These costs
can be minimized by breaking the one large
area into two relatively independent sub-
areas capable of processing the same infor- are necessary and both transmission time
mation in parallel, so long as they can be and integration costs will continue to
partially integrated with one another by mount. Of course there may also be advan-
specific interconnections. Although this tages, including the increased specificity
reorganizational strategy may compensate and reliability afforded by parallel redun-
in part for loss of local integration and pro- dant processing, o r alternatively, the pos-
cessing efficiency it cannot entirely com- sibility of subspecialization of different
pensate. And, if size continues to increase, subdivisions. T h e evolution of new struc-
additional parcellations into multiple areas ture and function as a result of such pro-
cesses will be discussed further in the next
section.
We can conclude that network allometry
may force a variety of secondary reorgan-
izations of cortical architecture, including
parcellation and multiplication of func-
tional areas, as brains enlarge during evo-
lution. This essentially forces large brains
to alter functional strategies for informa-
tion processing from those effective in small
brains. A further factor to be considered
is the fact that the receptor systems pro-
jecting to these cortical areas are also
enlarging along with body and brain size,
although these probably exhibit a negative
allometry with body size. This must also
play a significant role in determining at
what level of scale there will likely be
breakup and parcellation of cortical areas.
It is far from clear to what extent there is
net gain due to new functionality and
increased information storage or net loss
of efficiency and integration due to increas-
ing loss of connectivity as brain size
increases. We will need a better under-
standing of this trade-off before we will be
able to think clearly about the question of
comparative intelligence and its relation-
ship to brain-body allometry.
Size and parallelism in mammalian
cortical evolution
These complex allometric consider-
ations complicate the evolutionary inter-
pretation of comparative brain morphol-
ogy. It is not a simple matter to track
morphological changes and assign them
independent evolutionary causes. If in fact
many "emergent" architectonic changes
associated with brain size evolution are
simply the effects of common underlying
cellular mechanisms compensating for the
effects of size, then it can be misleading to
treat them as "new" features. T h e only
difference in the information utilized in
the ontogenetic process is difference in size
information-in the form of larger axonal
volumes, greater variance of metabolic
demands for different cell types, etc. If we
focus on the deep informational homolo-
gies rather than on the surface structural
homologies it is clear that developmental
mechanisms have not been altered, rather
one of the contextual variables to which
these mechanisms is sensitive has changed
value. These changes might be referred t o
as secondary facultative adaptations t o dis-
tinguish them from secondary adaptations
that actually involve the evolution of new
genetic and developmental information.
There is neither progression nor addition
in this sense, and the parallelisms that result
are not properly thought of as parallel
homoplasy.
It is possible that the ontogenetic mech-
anisms utilized in parcellation of cortical
areas are sensitive to the demands of net-
work allometry. T h e fact that axonal com-
petition plays the major role in determin-
ing area parcellation and afferent and
efferent relationships within the develop-
ing cortex (discussed in the next two sec-
tions) suggests that facultative mechanisms
may account for a considerable portion of
the structural and connectional response
to this functional demand. But it is likely
t h a t specific genetic adaptations also
become available to streamline the facul-
tative response (via genetic assimilation) to
these demands during the course of evo-
lution. T h e addition of new secondary
adaptations (derived conditions) is in order
to maintain the same function (conserved
condition), and can be seen as a sort of
"Red Queen effect" to the extent that the
system is working harder and harder to try
and stay in the same place. T h e parallel-
isms that have evolved to maintain func-
tional homology across a large range of
brain sizes are likely the result of a com-
bination of underlying ontogenetic homol-
ogies shared by all mammals and specific
genetically encoded biases that modify the
responses of these ontogenetic mecha-
nisms differently in different species.
But it is not necessarily safe even to con-
sider these microallometric changes as
facultative adaptations with respect to size
change. All that is demonstrated is a form
of morphogenetic plasticity that is affected
by size. In a related context, Smith-Gill
(1 983) distinguishes two general classes of
developmental plasticity that clarify this
point. The first he calls developmental con-
version and the second he calls phenotypic
modulation. In developmental conversion,
environmental cues activate alternative
genetic mechanisms that are expressed in
the organism's development. These differ-
ent genetic expressions may produce alter-
native morphs by activating o r inhibiting
growth processes affecting the structural
development of certain tissues, by chang-
ing cell surface affinities or messenger-
receptor sire relationships in intercellular
communication, o r even by inducing
regressive processes,such as programmed
cell death. In phenotypic modulation envi-
ronmental cues modulate but do not select
among'or alter genetic programs. This
produces variation and adjustment of the
expression of genetic information but not
the selection of different alternative genetic
programs. Smith-Gill notes that pheno-
typic modulation does not necessarily imply
an adaptive response, ". . . adaptiveness of
phenotypic modulation cannot be assumed
unless specific genetic mechanisms can be
demonstrated." It is unlikely that the onto-
genetic responses of neural tissues to the
influence of size are produced by specific
genetic alternatives, since these would have
to differ for each range of size and for each
brain' region. Rather, the facultative plas-
ticity of neurons in response to the local
effects of size must be a case of phenotypic
modulation. We cannot necessarily assume
that all aspects of this plasticity are adap-
tive, even in the broad sense of adaptive
with respect to local metabolic and infor-
mation processing demands. We can only
assume that significantly maladaptive plas-
tic responses will be strongly selected
against.
In conclusion, the evolution of mammals
is clearly characterized by a trend toward
increasing body size with a correlated
increase in brain size, but it is unclear to
what extent there has been additional inde-
pendent selection for increased brain size
and brain differentiation in different lin-
eages. Even if there is not independent
selection for brain size in a particular lin-
eage, body size correlated increase in brain
size can be expected to produce a series of
architectonic and functional changes due
to the plasticity of developmental processes
a t the neuronal-synaptic level. In general,
with respect to brain structure, we should
question the assumption that size increase
is caused by addition of new parts, since
the plastic responses of neural develop-
ment to size change inevitably produce dif-
ferentiation and subdivision of existing
structures at all supracellular levels of
organization. Although the majority of
architectonic trends in brain organization
in mammalian lineages give the appear-
ance of increasing differentiation and com-
plexity, we cannot disambiguate this from
the effects of local cellular plasticity and
secondary facultative adaptation which
cannot be considered progressive in any
sense. However, precisely because plastic
phenotypic modulation is not necessarily
adaptational, it cannot be assumed that it
will preserve any semblance of functional
isometry. And even if it is adaptational in
most cases it may fail t o be so at the
extremes of size, where otherwise predict-
able metabolic and information processing
demands may significantly diverge from
ancestral patterns. If such inadvertent
departures from functional isometry con-
tribute useful capabilities o r potentialities
they may contribute t o directional trends
in evolution. Alternatively, if the adapt-
ability of facultative responses induces
genetic assimilation of nongenetic pheno-
typic modulation mechanisms into genet-
ically based developmental conversion
mechanisms, the changes in response to
size may produce irreversible evolutionary
changes. In this way secondary adaptations
to size may inadvertently provide the raw
materials for the evolution of new func-
tional systems.
NEOGENESIS: THE EMERGENCE OF
N EW S TRUCTURE
The assumption that new adaptations
require new structures
In many ways the fundamental question
that evolutionary theory purports to answer
is how new species with novel structures
and functions come into being in the course
of time. If anything can be called evolu-
tionary progress it is the creation of totally
new adaptations, not just the augmentation
of existing adaptations. New brain areas
with distinct cellular architecture and con-
nectivity appear in some lineages but not
others, and it is almost certain that over
the course of mammalian brain evolution
the number of discrete brain areas in the
most complex brains has steadily increased.
This has suggested to many that new adap-
tations and the augmentation of existing
structures are accomplished by the addi-
tion of new structures t o an already func-
tioning brain. But new structure may also
evolve by co-opting or reorganizing exist-
ing structures in some way. In this case the
resulting structure may be radically differ-
ent than its antecedent, and yet combine
both novel attributes and pre-existing fea-
tures at different levels of organization.
How is it possible to distinguish between
uniquely derived structural additions and
previous structures that have become rad-
ically modified?
T h e history of vertebrate evolution in
general, including mammalian evolution,
exhibits a trend toward diversification of
adaptations. T h e invasion of new niches
inevitably requires adaptation of percep-
tual, behavioral and cognitive processes to
meet the new demands. T o some extent
these are acquired at the expense of mod-
ifying previous neural systems, trading one
function for the other. But the acquisition
of new abilities could also be achieved by
addition of new functions to old with a cor-
responding elaboration of the brain. Each
species is the culmination of a phylogenetic
sequence of adaptive changes that leave
their traces in the structure of its body and
brain. There is a natural tendency to envi-
sion this as an accretionary process that
progressively adds new structure to old.
This impression is supported by the appar-
ent increase in brain complexity that cor-
relates with the scala naturae hierarchy of
species leading from fish to mammals and
from "primitive" mammals to "advanced"
mammals. T h e definition of evolutionary
progress is at every step completely depen-
dent upon the identification of neogenesis.
One outstanding difference that is pre-
sumed t o distinguish primitive from
advanced mammalian brains is an increas-
ing number of architectonically and func-
tionally distinguishable cortical areas. T h e
increase in numbers of cortical areas has
often been cited as an example of both
neogenesis and of progressive evolution,
and is presumed to correlate with the
increased behavioral and cognitive abilities
of advanced species. T h e acquisition of new
functional abilities is also a central feature
of human mental evolution. We conceive
of ourselves as possessing all of the cog-
nitive abilities of other species and then
some. Particularly novel in the course of
evolution are human linguistic abilities. In
a behavioral sense this capability is clearly
an addition-functional neogenesis. It is
tempting to assume that the addition of
such an unprecedented function necessar-
ily implies the genesis of novel neurological
structures. With respect to apparent neo-
genetic trends in the evolution of cortex
in other mammals, the addition of human
language areas would seem to be a most
recent step in a long series of additions. In
this context it is clear that the assumed
ubiquity of neogenetic processes derives in
part from its presumed importance for
human mental evolution.
. .
Additive theories of cortical evolution
T h e most well known theory of mam-
malian brain evolution is the triune brain
hypothesis proposed by Paul MacLean (1970,
1973). It is an attempt to explain the dif-
ference between mammal brains and non-
mammal brains and how this difference
arose in the course of evolution. MacLean
argues that the mammalian brain can be
subdivided into three functionally and evo-
lutionarily distinct regions. T h e first divi-
sion, including the spinal cord, brain stem,
midbrain, diencephalon, corpus striatum
and olfactory apparatus are considered a
core structure common to all, terrestrial
vertebrates. He calls this the reptilian brain
or R-complex because, h e argues, this com-
prises the entire brain in reptilian species.
During mammalian evolution two addi-
tional structural levels are added in
sequence: the paleomammalian brain, com-
posed primarily of limbic cortex and its
associated forebrain nuclei and connec-
tions, and the neomammalian brain com-
posed of the neocortex. With the accretion
of each of these systems in the course of
evolution comes the emergence of new
cognitive abilities and behaviors. With the
paleomammalian brain come complex
parental care, vocal communication, play,
and the "higher" emotions of bonding and
caring. With the neomammalian brain
come higher order perceptual, motor and
generally enhanced learning abilities that
free the organism from reliance on fixed
action patterns and simple template based
perception. The scheme is hierarchic and
accretive. T h e reptilian brain is whole and
complete in and of itself (and presumably
can reassert itself as an autonomous force
in cases of high excitation or weakened
control from higher brain systems, as might
occur with brain damage), and therefore
the addition of new systems does not
require major reorganization, simply
superimposition of new axons into the cir-
cuitry of this otherwise complete system.
T h e additional connections need merely
play an inhibiting and modulatory role with
respect t o the pre-existing substrate.
Although this brain model has become
widespread in the popular literature and
in some psychological and educational the-
ories, its influence in comparative neu-
roanatomy is tenuous at best. T h e limbic
cortical areas that presumably comprise the
paleomammalian brain have been homol-
ogized to cortical structures in nonmam-
mals by comparative anatomists since early
in the century (e.g., Johnston, 1906; Crosby,
19 17; Elliot-Smith, 19 19; Dart, 1934;
Abbie, 1940). In addition, more recent
investigations have demonstrated that
nonmammals also exhibit forebrain struc-
tures and connections that undoubtedly
have homologues in mammalian neocortex
(e.g., Ebbesson, 1980; Karten and Shimizu,
1989; Ulinski, 1983). It also provides a sim-
plistic view of behavioral differences
between mammals and nonmammals. It
seriously underestimates the considerable
perceptual, motor and learning abilities of
nonmammalian species-particularly birds—
and ignores the many elaborate social
behaviors, modes of communication and
parental care that have been observed in
nonmammals. Nonetheless, t h e triune
brain theory has enjoyed a wide audience
in large part because it captures a central
anthropocentric intuition: that terminal
addition of higher order brain structures
must correlate with the appearance of
increasingly sophisticated cognitive abili-
ties and more flexible behaviors in the
course of evolution.
Ever since it first became possible to eas-
ily differentiate one cortical area from
another on the basis of cell architecture o r
myelin content it was recognized that the
cortex of some mammals exhibited many
more divisions into distinct areas than did
others. Efforts by the early comparative
anatomists, including Brodmann, Camp-
bell, Elliot-Smith, and others, to determine
homologies between these cortical areas in
different species suggested that apparent
homologies could be identified for a num-
ber of areas in most mammalian brains (see
Fig. 8). Apparently, the primary projection
areas for vision, audition, and tactile senses
could be homologized in all mammals but
the multitude of interdigitated "nonpro-
jection areas" that were evident in the
human brain could not all be homologized
to areas in monkey brains, and many of the
"nonprojection areas" in monkey brains
could not be homologized to yet smaller
and more "primitive" brains.
Flechsig's (1901) demonstration that this
precedence of areas was also approxi-
mately paralleled by maturational trends
(see Fig. 5) completed the evidence for a
grand synthesis. T h e evolution of ever
more complex associational abilities in
mammals was enabled by the elaboration
of additional higher order association areas
of cortex that were both progressively fur-
ther removed from direct peripheral input
and more interconnected with each other.
Just how these new areas of cortex became
interdigitated between old areas was not
clear to these authors, but the determi-
nation of homologies appeared to require
the progressive addition of new structures
in a particular order of appearance.
One obvious way to account for new
structure and new functional abilities
appearing in the course of cortical evolu-
tion is simply to hypothesize their insertion
into an already complete and functioning
cortex. T h e prevailing neuropsychological
theory of the early 20th century could
accommodate such a view. Like MacLean's
 flattened mouse flattened macaque
cortex cytoarchitecture cortex cytoarchitecture
FIG. 8. Comparisons of the number of cortical areas of small and large mammalian brains. T h e four drawings
depict unfolded views of mouse and monkey cortical surfaces. A (mouse cortex) and B (owl monkey cortex)
are redrawn from Kaas (1989) and depict area maps determined electrophysiologically in these species. C
(mouse cortex) and D (macaque cortex) are redrawn from Caviness and Frost (1980) and Jouandet et al.
(1989), respectively, and depict cytoarchitectonic divisions (Krieg's numerical designations following Brod-
mann). T h e differences in configurations largely represent different "unfolding" techniques, some of which
minimize area distortion at the expense of total map integrity whereas others maintain continuity of the map
at the expense of area distortion. All are drawn to equal size for comparability.

subsequent Triune Brain hypothesis, the orderly addition of cortical areas in evo-
theory of the accretion of new cortical areas lution and the progressive elaboration of
necessitated a hierarchic conception of sensory motor processes in "higher" mam-
brain organization and function; Flechsig mals. T h e associationist assumption at the
(1900) and Campbell (1905) clearly artic- center of this theory was that higher order
ulated this complementarity between the mental associations are built from lower
FIG. 9. A graphic depiction of Campbell/Brodmann/Flechsig, Bonin/Sanides and Lende/Poliakov scenarios
for the addition or differentiation of new cortical areas in mammalian evolution. Although none of the
individual schemes is exactly identical with any other (and may not exactly correspond with those depicted)
they have been grouped into three distinct categories for depiction because of their underlying theoretical
similarities. T h e relative sizes of these brains are depicted in column A and show that the increase in distin-
guishable cortical areas is not independent of size. Column B shows an accretive scheme in which projection
areas a r e primitive and association areas are added derived characteristics in later brains. Column C shows a
progressive differentiation scheme in which association areas are considered most undifferentiated and there-
fore primitive and more specialized sensory and motor areas are assumed to be later derived conditions that
have differentiated in a series of stages out of previous levels of association cortex. Sanides additionally argues
that there is a dual origin of most major sensory/motor fields that determines differentiation at the intersection
of a dorsocaudally originating archicortical and a ventrorostrally originating paleocortical trend. This is not
depicted here. Column D shows a progressive differentiation scheme based on the parcellation and retraction
of initially diffuse overlapping projection fields into eventually discrete non-overlapping fields. T h e boundaries
of the initially overlapping projection fields are depicted by dashed lines. Later parcellation and reduction of
diffuse projections within each projection field is depicted as progressively darker regions of gray. T h e notion
of reduction of diffuse projections within a field is from Poliakov and is not discussed as a possibility by Lende,
whose theory focused only on the earliest stages of cortical evolution in mammals.

order simpler associations, and compli-
cated and flexible skilled responses are
constructed by associations between sim-
pler reflex responses. They argued that
association areas of cortex only received
information from sensory projection areas
o r other association areas and served as the
locus for higher-order associations between
sense data and motor programs from pri-
mary areas. Association areas ultimately are
envisioned as an additional higher-order
reflex arc superimposed upon and elabo-
rating existing lower level reflex arcs
(Luria, 1980; Sherrington, 1906). There-
fore association areas could be added as
evolutionary after-thoughts with minimal
rewiring of other brain circuits. Each new
association area was one step removed from
the previous association area in the hier-
archy and provided an additional layer of
association processes superimposed upon
an already complete functional brain (see
Fig. 9).
Vestiges of this view are still widespread.
T h e pinnacle of this conception of the cor-
tical hierarchy is of course the addition of
language areas in the human brain-
inserted into an otherwise complete and
functional ape brain. T h e assumption that
Broca's area for speech is a new association
area peculiar to the human brain has been
represented in a number of schemes by the
identification of some region within the
third frontal convolution of the human
brain that is assigned no homologous coun-
terpart in the monkey brain. T h e possibil-
ity that Broca's area has no prehuman
homologue and could have been simply
added on to an otherwise complete brain
seems to be taken for granted in a number
of recent discussions of human brain evo-
lution (Passingham, 1981; Tobias, 1981;
Falk, 1983) and language evolution (e.g.,
Chomsky, 1972). Galaburda and Pandya
(1982) and Deacon (1984, 1988a, 1990c)
provide architectonic and tracer evidence
that a homologue for Broca's area exists
in the monkey brain, despite the fact that
it plays no apparent role in vocal commu-
nication in monkeys.
A similar argument was presented by
Geschwind (1964) and has been reasserted
by a number of later writers concerning
the inferior parietal lobule of the human
brain. Following the classic associationist
model of language processing, Geschwind
argues that this area plays a fundamental
role as an "association area of association
areas." Its placement at the temporo-pari-
eto-occipital juncture seemed to ideally suit
it for associating the outputs of association
cortices from different sensory modalities.
Since Geschwind conceived of word mean-
ings as complex associations between word
sounds and a multitude of other sensory
associations abstracted from sensory expe-
rience, an association area of association
areas would have to be the necessary sub-
strate for semantic processes. Posterior
temporal-parietal-occipital damage often
results in disturbances of semantic lan-
guage comprehension. Geschwind argued
that no homologue to this highest order
association area was evident in monkey
cortices. According to this logic the addi-
tion of this area during human evolution
was a necessary condition for language
evolution. Language evolution becomes the
natural end point of a progressive process
of adding association areas on top of asso-
ciation areas in the course of mammalian
brain evolution. This non-homology claim
has also been contradicted by subsequent
tracer experiments (e.g., Mesulam et al.,
1977; Seltzer and Pandya, 1980) and ani-
mal behavioral studies (e.g., Jarvis and
Ettlinger, 1977).
Recently, a more sophisticated version
of an accretion theory has been suggested
by Allman (1990) and Kaas (1987, 1989).
They argue that the multiplication of cor-
tical areas in many mammalian lineages
might be explained by the duplication of
existing areas. They suggest that a new
population of neurons could appear inter-
digitated in position between older popu-
lations as a result of some genetic accident
that caused redundant production of the
neurons from one of these regions (it is
compared by Kaas, 1987 and 1989, to the
addition of an extra body segment in the
evolution of lobsters; Gregory, 1935).
Recent studies of genetic mutants in fruit
flies has demonstrated that at least in these
species genetic mutations can cause the
production of whole duplicate body sec-
tions or limbs interdigitated between exist-
ing structures. Allman (1 990) suggests
that similar genetic mutations might
underly areal duplication events in mam-
malian cortical evolution. In fact, to account
for the number of such events that have
occurred this would have to be a somewhat
common sort of mutation.
It is unquestionable that new cortical
areas have evolved in some of the larger
mammal brains and that different lineages
(e.g., cats and monkeys) exhibit different
spatial arrangements and functional spe-
cializations of the cortical areas that have
been added (Kaas, 1989). But is it reason-
able to imagine that these areas have been
literally inserted between existing cortical
areas by the addition of new neural tissue
in that position? This claim depends on the
possibility that functional areas of cortex
are modular in their construction. T h e
neurons that comprise a new cortical area
would need to be added along with speci-
fications regarding intrinsic circuitry and
afferent and efferent connections with
neighboring areas and subcortical sites.
This requirement is contradicted by
developmental evidence that the afferent
and efferent connections of a cortical area
are not specified by the information that
is intrinsic to the cells in that area, but
rather by competitive interactions among
competing axons from many areas. Even
the transplantation of a section of cortex
into a novel position within a fetal brain
prior to the development of cortical con-
nections will not bring with it the functions
and connections appropriate to its site of
origin (O'Leary and Stanfield, 1989; Stan-
field and O'Leary, 1985; see discussion in
the next section). T h e transplanted area
will develop functions and connections
appropriate to its new position. Thus, even
if some new area of cortex miraculously
appeared interdigitated between older cor-
tical areas'in a developing brain it would
not bring with it any new connectional or
functional information.
Is there an evolutionary sequence of
new cortical areas?
An alternative approach is to conceive
of new cortical areas as differentiating out
of old areas rather than being created inde-
pendently adjacent to them. This has the
attractive property that new areas should
continue to bear some functional and con-
nectional interrelationship with their par-
ent areas. Because there is a parent-descen-
dent relationship between areas there will
also be an implicit sequential order of
regional .evolution, depending on assump-
tions about the "initial brain." Correlated
with t h e order of the proposed evolution-
ary sequence may also be an implied hier-
archy of increasing functional differentia-
tion and complexity.
T h e comparative cytoarchitectonic stud-
ies of Brodmann (1909) and others
appeared t o corroborate associationist
assumptions that association cortex was
newer than projection cortex and that some
association areas could only be identified
in the most "advanced" brains. T h e order
of regional evolution of the cerebral cortex
thus appeared to begin with primary sen-
sory receptive areas and motor output areas
and involve the progressive differentiation
of ever higher association areas. In the ini-
tial state sensory and motor areas were
thought to be directly connected to one
another to form direct reflex arcs. With
the differentiation of new areas inserted
between these primary areas the reflex arc
becomes more indirect and reflex action
gives way to more complex and variable
associations between sensation and action.
T h e more intermediate stages, the more
complex the analytic capabilities and the
less driven by reflex and habit. T h e newer
the area then, the more indirect its link
with the input and the more complex its
functional properties. In this way the dif-
ferentiation of association areas from asso-
ciation areas could be correlated with an
additive functional hierarchy as well.
It turns out that many of the assumptions
that initially supported this hierarchic
scenario have been subsequently under-
mined. T h e first difficulty to crop u p was
the discovery that association cortex did
not lack extensive subcortical connections
(Diamond, 1982; LeGros Clark and North-
field, 1939; Rose and Woolsey, 1949).
Association areas cannot be conceived as
added on top of a complete working sys-
tem, sending and receiving information
only from adjacent lower level cortical
areas. They have independent inputs and
outputs and are thereby completely inte-
grated into the whole brain at every level
every bit as much as are "projection" areas.
More problematic still is the nature of these
connections. T h e "highest" association
areas exhibit extensive connections with
limbic cortical areas (Pandya and Yeterian,
1985), whose evolution is presumed to pre-
date the evolution of primary projection
areas in all theories of cortical evolution.
Recent tracer studies have also suggested
that association areas project to core mid-
brain and tectal areas and receive indirect
projections from these areas relayed
through the thalamus. They may even
exhibit connectional topography that cor-
responds more to midbrain maps than to
cortical sensory o r motor maps (Deacon et
al., 1987). These features are also incom-
patible with the assumption that the "high-
est" association areas are only connected
with areas at the next hierarchic level down.
In many ways their principal links are to
some of the most primitive brain struc-
tures.
Finally, there is the problem of archi-
tectonic a n d functional specialization.
Probably the most extreme architectonic
and functional specializations anywhere in
cortex can be found in the primary visual
and motor areas of anthropoid brains. T h e
primate striate cortex, for example,
exhibits highly derived cytoarchitecture
with distinct sublamination of layer IV,
complex mosaic distribution of different
visual submodalities into a microscopic
matrix of architectonically distinct patches
o r "tufts" (Livingstone and Hubel, 1988),
and approximately double the number of
cells per cortical column of any other cor-
tical area in any other mammal (Rockel et
al., 1980). T h e s e a r e clearly recently
derived conditions that indicate a high
degree of functional and architectonic spe-
cialization. T h e architecture of association
areas is generally less variable from area to
area and species to species than is the
cytoarchitecture of specialized primary
areas (Sanides, 1970). This indicates that
structural and functional specialization is
not limited to and probably is less often
exemplified in "higher order" association
areas.
Some of these arguments against the
classic view have also served as support for
an almost exactly inverted view of regional
cortical evolution. Roughly inverted sce-
narios have been proposed by Bishop
(1959), von Bonin and Bailey (1961) and
Sanides (1969, 1970, 1975). Probably the
most ambitious and most widely adopted
of these is Sanides' theory of progressive
waves of cortical differentiation o r "Ur-
trends." Sanides infers the sequential evo-
lution of cortical areas from a trend toward
increasing architectonic specialization that
culminates in the evolution of specialized
primary projection areas (see Fig. 9). Fol-
lowing the lead of Abbie (1942) and Dart
(1934), Sanides argued that isocortical areas
evolved from undifferentiated periallo-
cortical zones along the borders of primi-
tive hippocampal and olfactory cortex in a
series of stages of increasing differentia-
tion. T h e trend is envisioned as a series of
"growth rings" (Sanides, 1970) constituted
by progressively more specialized cortical
areas differentiating out of relatively less
differentiated areas. Areas that correspond
to the highest level association cortices in
the classic view comprise some of the most
primitive ancestral areas in this view. T h e
most highly specialized areas in advanced
brains are envisioned to be the result of
specialized core areas developing within
more generalized areas, and subsequently,
further specialized core areas developing
within these specialized areas, and so on.
T h e ancient status claimed for association
areas could account for their extensive
connections with limbic structures and their
prominent links to midbrain systems. T h e
progressive stages of differentiation also
appear to correlate with connectional rela-
tionships between cortical areas (Pandya
and Yeterian, 1985). If it is assumed that
cortical areas only retain connections with
their immediate precursors but not second
generation precursors, this model could
explain the links between association areas
and limbic cortex as well as the lack of
connections between limbic areas a n d
either primary sensory-motor areas or their
adjacent belt areas.
As noted earlier in this discussion, the
most serious argument against Sanides'
evolutionary sequence is the apparent exis-
tence of specialized visual, auditory and
somatic projection areas in all mammal
brains, even in marsupials and mono-
tremes (Kaas, 1987). Even the primitive
cortex of turtles exhibits representation of
visual and somatic responses in distinguish-
able regions crudely appropriate to their
topological position in mammalian cortex.
An ancient status for these specialized sen-
sory areas contradicts Sanides' model.
One possible counter-response is to argue
that the apparent homology between the
specialized primary sensory areas of
advanced brains and the primary sensory
areas of ancestral and conservative brains
is incorrect. For example, von Bonin and
Bailey (1961) argue that the presumed
homology between the hedgehog visual
cortex and monkey primary visual cortex
is not supported by the cytoarchitectonic
criteria Brodmann (1909) originally sug-
gested. They conclude that it is far more
similar to the more generalized areas of
visual association cortex. This interpreta-
tion is supported by the fact that in the
visual systems of the opossum and hedge-
hog the thalamocortical projections of the
lateral geniculate nucleus (corresponding
to primary visual cortex projections) and
pulvinar nuclei (corresponding to extra-
striate association cortex projections)
extensively overlap (Diamond et al., 1985;
Kaas et al., 1970). Although the so-called
projection areas are specialized for receiv-
ing relatively more direct information from
peripheral sensors, all adjacent areas com-
prising a single modality receive indepen-
dent sensory afferents from the thalamus
and all share some thalamic connections in
common (Caviness and Frost, 1980; Dia-
mond, 1982).
Hierarchic scenarios of cortical evolu-
tion are appealing both because of their
agreement with tacit assumptions about
mental progress and mental processes, and
because of the way they simplify the
assumptions about connectional and func-
tionaI integration associated with the addi-
tion of new parts to a complex brain. Add-
ing the new parts to the terminal end of a
growing hierarchy limits the presumed
problems of integration with all lower
levels. It also provides an explanation for
the evolution of complex structures by
demonstrating plausible intermediate steps
in complexity, differentiation and special-
ization. One serious problem with both
hierarchic schemes for explaining regional
evolution of cortex is the constraint of the
linear sequence itself. Ultimately, both the-
ories'are terminal addition theories. T h e
arguments in support of both are analo-
gous to those for terminal addition in gen-
eral: addition of new structures to systems
that were complete in an adult of the pre-
ceding evolutionary stage; avoiding the
complication of inserting structural
changes in the middle of a complex pro-
cess; and the assumption that additional
structures augment the function of the pre-
ceding structures. As a result they are prone
to similar criticisms. It is not at all clear
that cortical areas within any one brain are
organized according to simple linear hier-
archies, nor is it obvious how cortical areas
in different lineages can be homologized
with respect to a strict number of steps in
the evolutionary sequence. For example,
the primate visual system exhibits at least
two, and probably three or four, distinct
processing pathways for different aspects
of visual perception that diverge from
striate cortex into distinct groups of asso-
ciation areas. Like a branching tree struc-
ture, one would assume that multiplication
of areas should be highest at its terminal
end. If areas are capable of differentiatin g
out of other areas in the course of evolu-
tion there should be an increasing number
of bifurcations as the process continues.
Each sense modality contains multiple asso-
ciation areas at the same level of the cor-
tical hierarchy but only one primary sen-
sory area. This would not be likely if these
specialized areas represented a terminal
end in the evolutionary differentiation pro-
cess. And yet the extreme other end of the
spectrum-paralimbic association areas—
is not the level of the highest multiplicity
of cortical areas either. In the visual modal-
ity it appears that the most diversity and
multiplicity of cortical areas is found at
middle levels in the processing hierarchy.
This is likely true of other modalities as
well. This pattern is implausible in either
of the two general terminal addition sce-
narios.
Strict hierarchical terminal addition is
not the only possibility, nor is it necessarily
less complex than are non-hierarchic sce-
narios. Given that most cortical areas are
connected to more than one other area and
that all are connected with distinct sub-
cortical structures, there is no obvious sense
in which a new cortical area can be thought
of as superimposed on an already complete
and functioning system-it must inevitably
emerge in the middle of a complex inte-
grated network. Terminal addition con-
tributes no additional explanatory power
toward solving the problem of the pre-
established integration of new areas.
Models of cortical evolution that make
no assumptions about the order of appear-
ance of cortical areas have been outlined
by Allman (1982,1990) and by Kaas (1987,
1989). They each argue that the multipli-
cation of cortical sensory areas of the visual
system can be explained by duplication of
existing cortical areas followed by subse-
quent differentiation of function in the new
area. Presumably the new area will initially
share the same connections and cell types
as its older twin and gradually will come to
gain o r lose connections and exhibit mod-
ifications in cellular architecture associated
with its changes in function. It is often the
case that adjacent cortical areas serving the
same sensory modality also exhibit con-
nections with similar structures elsewhere
in the brain-sometimes to separate divi-
sions of these structures, at other times
overlapping in connectivity, and it is not
unusual that neurons in common afferent
sources will send collateral branches of the
same axon t o adjacent cortical areas.
Duplication of this sort would also account
for the many striking homologies between
all isocortical areas.
T h e duplication of an existing area is
presumed to be a relatively innocuous acci-
dental mutation. However, the availability
of redundant areas frees one of the two
from the constraints of the primary adap-
tation so that it is able to develop some
additional, complementary visual function.
In the primate visual system it is clearly the
case that distinct visual areas seem to be
specialized for different submodality func-
tions in vision, such as color, form and
movement perception. Thus, by duplica-
tion and subsequent differentiation of
function the entire collection of interde-
pendent visual areas could have been pro-
duced. T h e apparently hierarchic arrange-
ment of these areas is not explicitly
explained in either model, but probably it
could be argued that the one area that
retains the ancestral function becomes the
more primary area and the differentiated
one becomes more secondary. Progression
from one to the next in sequence could
then be explained simply on the basis of
the influence of adjacent areas.
Allman (1990) and Kaas (1987, 1989)
assume that new areas are added to an oth-
erwise complete visual system, inserted
between existing cortical areas. This is con-
sistent with their focus on advancement and
augmentation of function as the prime
mover in the evolution of new cortical
areas-duplicated areas become recruited
to some new adaptive function that aug-
ments o r complements existing functions.
This argument is used to explain how dis-
tinct cortical visual areas have become spe-
cialized for distinct visual submodalities,
such as color, movement, or form percep-
tion. A major criticism is that the separate
functional specializations of the different
visual areas, which Kaas (1989) suggests
might be too complex to be handled effi-
ciently by a single large visual area, do
appear to be handled by only a few visual
areas in small brains. T h e r e is n o evidence
that "new" functions have evolved, only
that existing functions have become seg-
regated and distributed to parallel visual
processors. If processing all these modali-
ties together in a single area is merely an
efficiency problem, we should expect that
at least some very small brains would also
segregate visual functions into the almost
two dozen visual areas that endow large
primate brains and that at least some large
brains would collapse visual processing into
only one o r two visual areas, but this is not
seen. There are clearly size factors involved.
Accretion assumptions are not essential
to explain the appearance of new cortical
areas in mammalian evolution. A scenario
for the early stages of mammalian cortical
evolution was presented by Lende (1963,
1969) that does not make any assumptions
about evolutionary precedence of cortical
areas. He argues that the pattern exhibited
in the common ancestor to all mammals
(including marsupials and monotremes)
included cortical projection fields that were
extensively overlapping a n d t h e r e f o r e
poorly differentiated from one another. By
a gradual process of differentiation over
the course of evolution each projection field
retracted with respect to the other until in
most modern species each projection field
is exclusive of all others. In Lende's view
the marsupial and basal insectivore cortices
represent a state where the retraction into
separate territories is nearly complete, with
only somatic and motor areas still overlap-
ping. Because it is purely a differentiation
model there is no addition of areas and no
distinction between old and new cortical
fields, just old and new patterns. A closely
related theory of the evolution of connec-
tional differentiation has been proposed by
Ebbesson (1980, 1984) and will be dis-
cussed in the next section.
Lende's model was only intended to
explain the earliest stages of mammalian
cortical evolution (better resolution phys-
iological recording techniques have largely
contradicted his claims about the lack of
differentiation in primitive brains; Kaas,
 isocortical evolution
by areal differentiation
FIG. 10. Depiction of a scheme of progressive differentiation of cortical areas from one another that does
not assume an evolutionary sequence in which some coexisting areas are older than o r ancestral to others.
T h e figures are meant to represent flattened cortical hemispheres with limbic cortical areas representing the
white perimeter of each and isocortical subareas represented by the gray areas contained within. Below each
of the three brains of increasing size is a block diagram of the ancestor-descendent relationship for the
progressive generation of new cortical subdivisions. T h e use of diverging shades of gray is intended to represent
the differentiation of both descendents of a subdivided ancestral area from the architectonic and functional
characteristics of this ancestor.

1987). However, a simple differentiation hierarchic terminal addition scenarios of

theory suggests some interesting alterna-
tive interpretations of area multiplication
problems in more differentiated mamma-
lian brains. In these brains all the projec-
tion areas are differentiated from one
another and, with the exception of the
somatic and motor areas, they have also
been separated by interdigitated associa-
tion areas. T h e idea of progressive differ-
ential retraction of previously diffusely
overlapping projections might account for
differentiation of previously undifferen-
tiated association areas within each sensory
modality. A single sense modality might be
conceived as becoming progressively seg-
regated into differentiated submodalities.
This hypothesis (represented in Fig. 9) does
not necessarily predict that the interdigi-
tated cortex between primary areas should
be any more or less complex than projec-
tion areas nor that it should be performing
any higher function.
T h e assumption that one structure has
to be older or more conserved than another
is actually not even a necessary premise for
regional cortical evolution. If multiple new
areas result from the differentiation of pre-
viously unitary areas it is not necessary that
one of the resulting areas be considered
the homologue of the ancestral area and
the other o r others be considered derived.
If we assume either that a new cortical area
results from duplication of an existing area
o r that it differentiates out of some sector
of a pre-existing area and eventually takes
on a function that is somehow comple-
mentary to that of the other area, then it
should follow that both areas will be
changed in the process.
In this regard, the primary visual cortex
in primates cannot even be strictly homolo-
gized to the primary visual cortex in the
squirrel because in the squirrel many of the
visual functions handled in the primary
visual area are in the primate partially dis-
tributed to some of its many more numer-
ous nearby visual areas. In a hypothetical
"initial brain" with only one visual area all
the distinct submodality analyses would
have to be performed within that area—
luminosity, movement, color, form, spatial
relationships, local features, etc. There is
no visual area in a brain with many visual
areas that performs all these functions.
Even a duplicate area and its progenitor
should be expected to change with respect
to one another, in the course of subsequent
evolution, so that neither resulting area will
be directly comparable to the original. Thus
it is probably more accurate to view the
multiplication of cortical areas in terms of
progressive differentiation of all areas with
respect to one another. Both areas created
after the subdivision of some previous area
will differ slightly from one another and
from ancestral structure, and these differ-
ences will likely increase over time (see Fig.
10). From this perspective it does not mat-
ter where in a cortical hierarchy the new
division appears, the differentiation pat-
tern will be essentially the same.
It cannot automatically be assumed that
there is any strict hierarchy from function-
ally and architectonically simple to com-
plex cortical areas or from phylogenet-
ically old to new cortical areas. A ranking
of areas with respect to relative phyloge-
netic age or functional complexity is not
unambiguously reflected in neuroanatom-
ical data and may not be consistent with
developmental considerations of cortical
differentiation. Nor are we justified in
assuming that the addition of new func-
tional subdivisions of cortex correlates with
an enhancement of function. T h e addition
of new cortical areas still needs to be exam-
ined with respect to the influence of brain
size. Extensive multiplicity of cortical areas
is never seen in small brains, and the most
extensive multiplicity of areas appears only
in very large brains (e.g., the human brain).
This suggests that areal multiplication
might be the result of facultative devel-
opmental responses to brain size and not
distinct genetic adaptations.
Reorganization and the neogenesis of
neural circuits
Whether we explain area multiplication
and functional differentiation in terms of
addition or differentiation there is still a
major problem area that must be addressed:
How are the neural connections of these
areas determined? This rewiring problem
is most troublesome for addition o r dupli-
cation hypotheses. If an area is completely
new its connections must presumably
invade territories in other structures that
are occupied by projections from pre-exist-
ing areas, and it must itself be invaded by
axons from other structures that would
otherwise have found other targets in the
brain. But area duplication does not escape
these problems. A duplicated area may have
all the afferent and efferent specificities
appropriate t o the original area but there
still must be overlap in efferent projections
from the duplicate and the original area as
well as a dividing o r sharing of afferents.
Any subsequent differentiation of t h e
duplicated area from its progenitor likely
also involves changes of connections,
including both the loss of many of those
shared with the original area as well as a
shift of its efferents to new targets.
T h e possibility of connectional reorgani-
zation also suggests other options for neo-
genesis. If connectional organization can
be altered then it is not necessary for ,new
structure to be added for new functional
areas to emerge, it is only necessary for
their underlying connections to change.
Since ultimately the patterns of connection
determine function within the nervous sys-
tem, all theories of neogenesis of cortical
structure and function must address this
issue. A theory that fails to explain how
underlying connectional reorganization
takes place is fundamentally incomplete.
T h e most obvious hypothesis for
explaining the evolution of new connec-
tions is that they are simply added. Because
this hypothesis requires axons to enter
novel target areas that are occupied by
other connections and ultimately displace
some of those connections o r form new
synapses in that area, it has been called the
invasion hypothesis. T h e basic features of this
process are diagrammed in Figure 11. Cells
from one area either change their target
o r produce collateral branches that invade
a new target area. This idea has had a long
history in comparative neuroanatomy (e.g.,
Ariëns Kappers et al., 1936; Herrick, 1920)
and seems essential to explain the appear-
ance of certain neural pathways that occur
 simple accretion hypothesis axonal invasion hypothesis

before duplication-addition after duplication-addition before axonal invasion after axonal invasion

/','
. . parcellation hypothesis equivalent cell population hypothesis

diffuse connectivity differential connectivity

before parcellation after parcellation before cell migration after cell migration

FIG. 11. Four commonly cited o r assumed rewiring hypotheses are depicted with source nuclei indicated by
shaded ellipses, cortical (or other nuclear) targets indicated by shaded boxes, and connections indicated by
black arrows connecting them. Antecedent and consequent conditions a r e shown in neighboring boxes. 'The
simple accretion hypothesis is depicted at the top left, in which a new structure is added t o the brain including
its own new connections. T h e invasion hypothesis is depictedat the top right, in which a new set of connections,
or connections originally targeting some other area, invade and establish synapses in a novel brain structure.
The parcellation hypothesis is depicted at the bottom left, in which previously diffusely interconnected
structures lose some of their diffuse connections in a complementary fashion so as to produce subdivisions of
each that are connectionally distinct. T h e "equivalent cell" hypothesis is depicted at the bottom right, in
which cells from one region migrate into another structure and attract their afferents t o this new structural
position.

in relatively recent lineages but not ances- comparative evidence demonstrates a

tral lineages (Northcutt, 1984). Invasion
was long thought to be the explanation of
the progressive development of telence-
phalic specializations in vertebrate evolu-
tion. However, many of the telencephalic
connections that were formerly thought
absent in anamniotic vertebrates have
turned out to be demonstrable with axonal
tracing techniques (Ebbesson, 1980;
Northcutt, 1981). I n support of this
hypothesis Northcutt (1984) argues that the
presence of a spinothalamic pathway in all
reptiles, birds and mammals but in no other
group but cartilaginous fishes and the pres-
ence of palliospinal pathways only in birds
and mammals are each best explained by
invasion.
However, Ebbesson (1980) questions the
plausibility of invasion on the grounds that
remarkable conservatism of connection
patterns within all vertebrate brains despite
radical differences in size, morphology and
differentiation. T h e overwhelming major-
ity of major pathways seem to be evident
in all vertebrates and probably represent
an inheritance from the common protover-
tebrate ancestor. Ebbesson argues that
there are no developmental or compara-
tive cases that would require the assump-
tion that axons must have invaded an
unusual target (although his own theory
has been called unfalsifiable in this regard).
All connection changes in the course of
vertebrate evolution can b e explained
entirely in terms of changes in the relative
numbers of preexisting connections-
sometimes complete loss of connections-
in prior lineages. Ebbesson (1980) refers
to this as the parcellation theory of brain evo-
lution. Invasion, he argues, either simply
does not occur o r else is extremely rare.
A schematic depiction of the parcella-
tion hypothesis is presented in Figure 11.
Parcellation theory presumes that t h e
ancestral condition consists of a relatively
undifferentiated pattern of connections
between two given structures. It is pro-
posed that progressive loss or retraction of
a selected subpopulation of these fibers is
responsible for subsequent differentiation
of each ancestral structure into two, con-
nectionally and functionally distinct sub-
divisions. In the course of time further par-
cellations of these separate projection
systems can result in yet further functional
specialization. This process would account
for increasing multiplication of areas and
increased differentiation of functions in the
course of brain evolution. It also explicitly
predicts many details of connectional orga-
nization that should correlate with areal
multiplication and differentiation in cor-
tex. Because subdivided areas originate
from a single area they each will inherit
most but not all of the connections of that
ancestral area. For example if an extrastri-
ate visual area in some ancestral lineage
becomes subdivided in its descendents we
should expect that the lateral posterior
(pulvinar) thalamic source of the ancestral
afferents would be the same for the descen-
dent subareas although perhaps subdi-
vided into new subdivisions, and we should
expect that the tectal targets of its efferents
should likewise be the same structure o r
some new subdivisions of that structure.
These predictions appear to be reflected
in the organization of afferent and efferent
connections of brains with relatively few
visual areas as compared to those with many
visual areas (Diamond et al., 1985; Kaas and
Huerta, 1988), as well as in other systems.
Ebbesson further argues that the evo-
lutionary history of parcellation events is
recapitulated in developmental processes.
Parcellation must occur at some particular
stage in the development of existing con-
nections in any organism and subsequent
further parcellation processes must be pre-
ceded by this first parcellation. Following
von Baer's principle of character prece-
dence (i.e., that members of two or more
closely related taxa will follow the same
course of development to the stage of their
divergence), this would mean that two
species' developmental patterns would
coincide to the point of the first parcella-
tion event that distinguished them, and
therefore that parcellation events that fol-
low others in evolutionary time, and fur-
ther parcel the same projection. system,
should also be expected t o occur subse-
quent to the first in development. This pre-
dicts that early stages of brain development
should be characterized by the presence of
diffuse axonal projections and later stages
would proceed through progressive par-
cellation processes.
In general terms this pattern of pro-
gressive culling of initially diffuse connec-
tions is indeed exhibited in brain devel-
opment. Initial axonal projections appear
to be less selective and more exuberant than
the projections that survive to adulthood,
and as a result fetal axons contact many
more targets and a much wider variety of
targets than do adult axons. During sub-
sequent development these superfluous
connections are culled, resulting in. con-
nections that are far more specific and
topographically organized (Jacobson, 1978;
Purves and Lichtman, 1980, 1985). T h e
details of this process will be discussed in
the next section.
Ebbesson (1980) argues that this devel-
opmental pattern recapitulates the ances-
tral sequence of differentiation of each
brain area and its connections. These tran-
sient connections within the fetal brain are
therefore viewed as "fossils" of earlier pat-
terns of brain organization. Viewing cer-
tain transient events in neural. develop-
ment as "fossils" may also help explain the
appearance and subsequent elimination of
whole classes of neurons during develop-
ment that serve as transitory targets for
projections ultimately destihed for other
targets. However, this strictly recapitula-
tionist interpretation is not critical to the
parcellation hypothesis and weakens its
generality and predictive power. Although
Ebbesson's (1980) initial examples com-
pare the adult organization of connections
in primitive fish to embryonic connections
in terrestrial vertebrates (and therefore
have earned the criticism that it assumes a
crude scala naturae view of living species
as well as strict terminal addition), the
underlying assumptions of parcellation
theory do not require terminal modifica-
tion. T h e relative timing of fetal parcel-
lation events need not be an exact reca-
pitulation of evolutionary events and the
hierarchic 'dependency of one parcellation
event on another during development does
not necessarily imply a corresponding phy-
logenetic order as well.
A more flexible version of the theory can
be articulated if we assume that a new par-
cellation process can affect connections at
any stage of brain development during the
course of evolution. Parcellation processes
that alter connections early in ontogeny
will operate on less differentiated connec-
tion patterns than parcellation processes
that occur later in ontogeny. Presumable
parcellation processes during development
depend on earlier parcellation processes,
and so a subtle change at an early stage
might have radical consequences for adult
structure. A wider range of reorganiza-
tional effects should result from mutations
that influence parcellation early in devel-
opment, particularly if subsequent parcel-
lation events are undermined or biased by
the earlier changes. But if changes in par-
cellation processes can occur at any devel-
opmental stage, then brain development
cannot be a strict recapitulation of the order
of phyletic events in brain evolution. A very
early change may have been very recently
acquired whereas a relatively late parcel-
lation change may date to a much earlier
evolutionary epoch. Recently acquired
parcellation changes that affect an early
stage of development could fundamentally
alter the pattern of all subsequent devel-
opmental events so that they no longer
reflect any meaningful phyletic series.
T h e parcellation hypothesis is the inverse
of the invasion hypothesis both in its mech-
anism and in the assumptions that it makes
about ancestry-descent relationships of
brain structure. In more general terms, the
invasion hypothesis is an example of an
additive theory a n d t h e parcellation
hypothesis is an example of a differentia-
tion theory. Each of these two mechanisms
for connectional change correspondingly
supports. additive versus differentiational
theories of brain structure evolution. T h e
parcellation hypothesis is most consistent
with area addition scenarios involving dif-
ferentiation of new areas from old areas
and is inconsistent with simple addition
hypotheses that presume the invasion of
new axons. It is probably also inconsistent
with area duplication scenarios, since it
would reject arguments about projection-
map duplication as invasion hypotheses.
But in addition, parcellation is also
inconsistent with many of the existing dif-
ferentiation theories of cortical evolution
because it does not predict that ancestral
cortical areas can remain unchanged as new
areas differentiate out of them. For this to
happen the older of the two areas would
have to maintain all of its previous con-
nections and the newer area would be dis-
tinguished only by its lack of certain con-
nections and not by the possession of
connections not also present in the older
area. Considering either thalamic afferents
o r subcortical efferents, it is clearly not the
case that there are cortical areas that pos-
sess all the connections of any of their
neighbors; each has slightly different
although often partially overlapping affer-
ents and efferents. T h e adjacency of affer-
ent sources and efferent targets of neigh-
boring cortical areas as well as the partial
overlap in some of these is strong support
for the parcellation hypothesis.
Invasion is a necessary hypothesis for
both additive and recapitulational theories
of regional cortical evolution. Structural
addition is doubly challenged by the par-
cellation hypothesis because the latter de-
nies both the possibility that new structures
can arise from nothing and the possibility
of invasion of new structures by axons that
did not contact it ancestrally. Even though
they do not assume structural addition,
sequential differentiation theories, such as
the traditional evolutionary hierarchy from
projection to association areas o r Sanides
inverted hierarchy from association areas
to specialized sensory and motor core areas,
are also both tied to the assumption that
axon invasion events have been common-
place. If Ebbesson is correct in assuming
that these are rare events in evolution then
all of these hypotheses must be abandoned.
It is important to recognize that the par-
cellation hypothesis is a stronger claim
about what can and cannot happen in brain
evolution. Invasion hypotheses do not deny
the possibility that parcellation may play a
major role in brain evolution. Invasion is
an additional assumption beyond parcel-
lation. One difficulty with denying any pos-
sibility of invasion is that to do so often
requires hypothesizing many more con-
nectional changes in order to explain a
phylogenetic difference that can otherwise
be explained by only one o r two invasion
events (Northcutt, 1984). Although Ebbes-
son's argument for the ancient status of
preset axon-target affinities is also corrob-
orated by evidence of the ancient and
highly conservative nature of molecular cell
communication and recognition mecha-
nisms (Fasolo and Malacarne, 1988), such
specificity may be determined by complex
relationships of timing and hierarchically
organized interactive effects that render
this specificity somewhat degenerate (Edel-
man, 1987).
A more fundamental criticism of par-
cellation theory in its strong form is that
it is preformationist (see numerous com-
mentaries following Ebbesson, 1984).
Either some initial protovertebrate brain
(possibly long antedating the vertebrates)
must be considered to have been com-
pletely undifferentiated in connectivity and
therefore totipotential from an evolution-
ary standpoint, or some of the initial con-
nection patterns must have been pre-
formed from t h e start and require
explanation in some other way, e.g., inva-
sion. T h e first possibility is more consistent
with the exclusivity assumption of parcel-
lation theory.
There is no stage of brain development
that exhibits a corresponding totally inter-
connected undifferentiated state. Although
there is some degree of initial overproduc-
tion of projections and poor differentiation
of target sites in the fetal brain these con-
nections are neither totipotent nor com-
pletelv undifferentiated. Most pairs of brain
structures never pass through a stage where
they are connected. Target sites are under-
determined but probably not undeter-
mined by genetically pre-established
molecular affinitiesbetween growing axons
and potential target cell substrates. During
embryogenesis axons do in fact grow out
from their cells of origin to invade differ-
ent structures distantly located in the brain.
En route to their genetically underdeter-
mined target zones they also may pass
through structures with which they estab-
lish no synaptic contacts o r only transient
contacts. Both the active "exploratory"
nature of embryonic axons and the pre-
specification of initial target zones are
potentially troublesome for parcellation
theory. However, permanent loss of many
connectional affinities over the course of
vertebrate evolution is entirely consistent
with the theory.
Both the invasion hypothesis and the
parcellation hypothesis can probably be
used t o explain almost any possible
arrangement of connections in the living
vertebrates. T h e invasion hypothesis makes
many more assumptions regarding each
individual rewiring event, whereas the par-
cellation hypothesis makes some other
rather troubling assumptions about the ini-
tial condition of vertebrates and often
requires considerable theoretical, circum-
locution to explain what could be explained
by a single invasion event. Each handles
certain examples better than the other.
A third alternative hypothesis, that to
some extent can serve as a bridge between
these two polar opposites, is the equivalent
cell hypothesis suggested by Karten (1969;
Nauta and Karten, 1970). On the assump-
tion that the connectional relationship
between two different cell groups within
the brain is specified by some features spe-
cific to those cells, their connection should
be maintained even if one of these cell pop-
ulations became displaced o r actively
migrates to an entirely different location.
Karten (1969; Karten and Shimuzu, 1989)
proposes this as a possible explanation for
the apparent homologies between thalamic
projections to the dorsal ventricular ridge
in birds and to the isocortex in mammals.
He argues that cells which in avian and
reptilian brains are destined to form the
dorsal ventricular ridge may take a differ-these trends and the theoretical assump-
ent migratory pathway in mammals and tions about homologies, progression, size
ended up in cortex. In the process they increase and cortical neogenesis have been
would also attract their thalamic afferentsshown to be seriously flawed. Although
to this new target site. T h e general formpatterns are evident it cannot be decided
of the equivalent cell hypothesis is sche- o n the basis of comparative evidence
matically diagrammed in Figure 1 1. With whether they are merely secondary archi-
respect to mammalian cortical evolution it tectonic adaptations to differences in brain
has the advantage of also accounting for size, adaptations for sensory-motor spe-
the significantly increased number of cellscialization, o r independent macroevo-
that occupy mammalian as compared to lutionary tendencies for increased cogni-
bird and reptile cortex. This hypothesis tive complexity and diversity. However, the
could thus explain the apparent "invasion" predictable relationships between these
of new thalamic afferents into the cerebraltrends and differences in brain size as well
cortex and also the apparent "invasion" of as the parallelisms exhibited in distant lin-
new subcortical targets by cerebral cortical
eages suggests that many of these patterns
cells without requiring the appearance of may instead be the result of underlying
any new connections or any change in the developmental homologies that a r e
underlying topology of connection pat- expressed differentially with respect to
terns. However, the theory makes strong brain size o r certain sensory-motor spe-
assumptions about the specificity of devel-cializations (e.g., regression of vision in
oping connections that may limit its gen- echolocating bats).
erality. A considerable body of new data is
Increasing the amount of comparative emerging concerning the development of
data will not by itself be able to help us the brain that can help sort out which evo-
choose between these alternative hypoth- lutionary hypotheses are tenable and which
are not. Obviously brains d o not evolve
eses. T h e homological ambiguities limit our
from one adult form to another, although
ability to clearly discern what is a new con-
nection and what is a modified ancestral this is often how brain evolution is por-
connection. And since each of the different trayed. In fact, most of the well established
hypotheses a r e sufficiently flexible t o theories of cortical evolution make no
account for nearly any pattern, we have assumptions at all about brain develop-
only parsimony assumptions to rely upon. ment processes (except possibly the
Unfortunately, the capricious nature of theerroneous assumption that they should re-
evolutionary process suggests that we capitulate phylogenetic trends). But phy-
should not place too much confidence in logenetic change in brain structure is the
parsimony arguments. Each of the alter- result of changes in the process of brain
native theories proposed to account for development a n d ultimately must be
connectional reorganization depends on explained in terms of developmental
specific assumptions about the ontogenetic mechanisms. T h e importance of ontogeny
processes that ultimately determine con- to the understanding of brain evolution is
nectional specificity. We can thus turn t onot that it recapitulates phylogeny-it
the ontogenetic data to look for develop- almost certainly does not-but that it con-
mental constraints that can rule out certain
strains the possible modes of variation that
versions of these hypotheses and develop- phylogenetic changes can exhibit (Alberch,
mental patterns that might suggest alter- 1982; Katz, 1982; Smith-Gill, 1983). If
native mechanisms. there are only certain ways that cell pop-
ulations, functional areas o r connections
ONTOGENY CONSTRAINS PHYLOGENY can develop within a brain, then patterns
Ontogeny of neural populations, of phylogenetic change will tend to be lim-
connections and functional areas ited accordingly and the possibility of par-
There are clear trends in mammalian allel evolutionary trends arising in inde-
brain evolution. However, the evidence for pendent lineages will be increased.

mature
connections
F IG . 12. Fetal cortical transplant experiment in rats
in which either a frontal cortical sector is transplanted
to the posterior cortex of a host or a posterior cortical
sector is translated to the anterior cortex of a host.
In either case, when the animal matures it is found
that the cortical efferents from these transplants proj-
ect to the appropriate targets for their new position
rather than the target specified by their original posi-
tions (i.e., rostral sensory/motor areas send efferents
to the brainstem and spinal cord whereas posterior
visual areas send efferents to the tectum).
A number of features of the neural
developmental process in mammals are
incompatible with scenarios of cortical evo-
lution which assume that cortical areas can
appear, differentiate, or even change their
relative sizes as independent units during
the course of evolution. This is because the
information that specifies the size, archi-
tectonic organization, afferent and effer-
ent connections and therefore the basic
function of a cortical area during its devel-
opment is determined by factors extrinsic
to the cells that comprise that area. T h e
neurons that comprise the fetal cortex are
nearly all produced prior to the stage at
which the cortex is invaded by thalamic
afferents and prior to the stage at which
axons originating from cortical neurons
reach their targets. At this stage the cell
groups in different positions on the cortical
mantle a r e effectively totipotent with
respect to their ability to assume any of the
different functional roles exhibited by cell
groups in the adult cortex (O'Leary, 1989).
T h e most striking evidence for this comes
from fetal transplantation studies where
sectors of fetal cortex are removed from
one area of a donor's cortex and trans-
planted to a different area of a recipient's
cortex (Fig. 12). In the mature brain the
transplanted cortical tissue takes on the
sensory or motor functions, assumes the
cytoarchitecture and even develops the
appropriate afferent and efferent connec-
tions characteristic of its new cortical posi-
tion rather than its place of origin (O'Leary
and Stanfield, 1989; Stanfield and O'Leary,
1985). T h i s relatively late, interactive
determination of cortical structure and
function has very significant implications
for the evolution of isocortical subdivi-
sions. T h e evolution of a new cortical
region must therefore be a systemic pro-
cess and not the result of the isolated local
expression of genetic mutations.
T h e structural and functional differen-
tiation of any cortical area is thus not spec-
ified by the specific local cell lineages that
constitute it, and takes place considerably
after neurogenesis has been completed for
all cortical areas. T h e determination of
what constitutes a distinct functional area,
where its boundaries are, how big it is with
respect to neighboring areas, the local spe-
cializations of its myelo- and cyto-architec-
ture and its connections with other' areas
are all largely independent of which cells
constitute that area. New cortical areas that
appear in the course of evolution cannot
have been added as whole units corre-
sponding to specific populations of new
cells.
Classic theories of additive cortical evo-
lution are clearly inconsistent with this
constraint of cortical development because
it undermines any possibility of discrete
terminal addition. It also undermines addi-
tive theories of differential area expansion
as well (e.g., differential addition of cells to
association cortex with respect to primary
cortex during cortical advancement). T h e
addition of cells to one sector of cortex
rather than another does not determine
which of the cells will or will not be included
within the functional regions that develop
in that sector. T h e enlargement of the cor-
tex cannot be thought of in piecemeal
terms. Addition of new cortical areas can-
not be the direct cause of the addition of
new brain mass. Given the fact that there
is no specific topographic information rep-
resented in the developing cortex, cortical
expansion must be considered as a whole
and area by area size determination must
be a consequence of secondary processes.
T h e expansion of the total cortical man-
tle is probably not determined by a simple
increase in neurogenesis either. T h e target
size of the cerebral cortex is likely deter-
mined prior to neurogenesis for the struc-
ture as a whole. During neurogenesis pre-
curser cells in a germinal layer deep to the
developing cortex divide to produce neu-
rons that leave this zone and migrate along
the length of special radial glial guide cells
that gxtend from the germinal layer to the
surface of cortex. These guides effectively
limit tangential migration (although see
Walsh and Cepko, 1988, for discussion of
exceptions) and serve to align succeeding
cells along this radial column occupying
ever more superficial positions. Radial
guides and the germinal zone at their base
probably form distinct proliferative units,
or ontogenetic columns (Rakic, 1988). All
cell types within that columnar unit of cor-
tex are derived from a common polyclonal
precurser. Earlier it was noted that the
number of cells within a column of cortex
of t h e same tangential dimensions is
approximately the same in species with very
different size brains (Rockel et al., 1980).
This indicates that neurogenesis within an
ontogenetic columnar unit is invariable
across species and irrespective of brain size.
Cortical expansion must therefore be
understood in terms of the addition of more
ontogenetic columns as opposed to the
increase of cell production within these
columns (Rakic, 1988). Since the multipli-
cation or germinal precursors which will
establish ontogenetic columns occurs prior
to the terminal differentiation of neurons
from these precursors, the determination
of the size of the cortical mantle must be
determined prior t o neurogenesis within
the cortex.
T h e determination of area dimensions
and boundaries within the developing cor-
tex must occur subsequent to neurogenesis
by virtue of o t h e r mechanisms. This
appears largely to be the result of afferent
and efferent interactions. In the discussion
of parcellation theory it was noted that the
first axonal connections during develop-
ment are over-exuberant and relatively
unselective. These initially diffuse project-
ing cortical afferents and efferents com-
pete for dwindling synapses within their
target areas. This competition results in a
significant culling of axons and axon col-
laterals and some cell death. T h e relative
correlation of the neural activity of an axon
with others in the near vicinity which relay
similar information to an area is thought
to play a significant role in determining
which axons will be retained and which will
be eliminated (Purves and Lichtman, 1985).
T h e resultant parcellation of connections
largely determines which structural and
functional characteristics will develop.
This is demonstrated dramatically in the
case of cortical efferents. In an infant rat,
cells in layer V of all regions of the isocor-
tex appear t o give rise to axons that extend
into the spinal cord, but in the adult rat
only rostrally located somatomotor areas
contain cells with spinal projections. More
caudally located areas, specialized for visual
o r auditory modalities, lose these spinal
connections but retain connections to the
tectum (see Fig. 13). This explains why het-
erotopic cortical transplants take on the
connections and functions appropriate t o
their new cortical position. A similar pat-
tern of overexuberant and relativelv undif-
ferentiated connections followed by later
culling of a large number of these connec-
tions has been extensively documented for
thalamocortical projections and for corti-
cocortical connections, among many other
systems (see reviews in Jacobson, 1978;
Purves and Lichtman, 1980, 1985; Purves,
1988).
Connectional interactions must also play
the major role in determining the size that
a source o r target structure will attain. T h e
elimination or reduction of afferent con-
nections to a cortical area during fetal
development can cause it to be reduced in
size, can cause neighboring areas to be-
come enlarged, and can cause a corre-
sponding displacement of t h e cortical
boundary between them (Rakic, 1988).
Deafferentation does not seem to diminish
the numbers of cells per cortical column

immature
connections
mature
connections
FIG. 13. Exuberant efferent cortical projections and
culling of connections in development is depicted with
respect to frontal somatomotor areas and posterior
visual areas. Early in the development of an infant rat
pyramidal cells from layer V of nearly all cortical
regions have axons that reach these targets. These
exuberant axons are later culled in a parcellation pro-
cess driven by dynamic interactions between com-
peting axons and their targets.
in that area, only the number of columns
that are contained within a projection area.
In other regions of the brain, more limited
in their possible sources of afferent input
o r efferent targets, a loss of connections
can induce significant cell death. This
appears to be the case with many periph-
eral afferent targets (e.g., the lateral genic-
ulate nucleus, Rakic, 1988) and efferent
sources (e.g., brain stem motor nuclei, Alley,
1974; Sohal, 1976). This cell death is pre-
sumed to play a role in the functional
matching of peripheral afferents to target
neuronal populations without the need for
genetic changes in order to specifically
match afferents and cell populations in
every instance of size change in evolution
o r of peripheral homoplasy (Cowan, 1973;
Cowan et al., 1984; Finlay et al., 1987; Wil-
czynski, 1984). T h e multipotentiality of
cortical cells both for afferent and efferent
connections probably accounts for the lack
of significant cell death due to loss of con-
nections. It appears that alternative pro-
jections inevitably will substitute for the
lost afferents. However, some degree of
cell death-particularly at early stages—
may play a role in cortical parcellation and
distinguishes certain cortical areas from
others (Finlay and Slattery, 1983).
The displacement hypothesis
An alternative general model of connec-
tional reorganization processes that takes
into account both allometric effects and
the competitive parcellation process that
sculpt cortical areas can be derived from
these developmental considerations. As a
result of investigating different problems
in comparative neuroanatomy, Deacon
(1984, 1988b), Finlay et al. (1987), Purves
(1988) and Wilczynski (1984) have each
suggested that ontogenetic factors play a
central role in the reorganization of neural
circuits in response to differences in neural
populations, regressive processes and per-
turbations of maturation schedules, o r
homoplaseous changes in peripheral sen-
sory o r motor structures. These views are
similar enough t o be capable of synthesis
into a single general model of the struc-
tural reorganization processes underlying
most brain evolution.
T h e displacement hypothesis, as it can be
called, argues that loss of connections,
acquisition of additional connections o r
replacement of one class of connections by
another occurs when competitive axonal
interactions are biased by contextual events
during development. This can happed as a
result of changes in relative size relation-
ships (an extreme example of which might
be complete cell death for a particular tar-
get or source), changes in the amount o r
intercorrelation of afferent information to
one system as opposed to another, or
changes in the relative importance of ini-
tial axon-target affinities, or, changes in
developmental timing. Four possible modes
of connectional displacement are depicted
in Figure 14. Although the figure depicts
size relationships, this can be understood
metaphorically to represent competitive
biases of all kinds. For example, synchro-
nization of target cell maturation and
axonal arrival would increase the likeli-
 axonal connectivity after axonal displacement axonal connectivity after
efferent target expansion efferent target reduction
hypothesis

ancestral condition

axonal connectivity
before allometric
reorganization

axonal connectivity after axonal connectivity after

afferent source expansion afferent source reduction

FIG. 14 . T h e displacement hypothesis is depicted with four possible interpretations of invasion-like effects.
In each case either the effective enlargement or reduction of targets or afferents (depicted by the size of the
structure) is invoked to explain the source of bias driving the displacement of connections from one target
to another. An analogous pattern could be produced by relative increases o r decreases of axon-target affinities
or by heterochronic advantages of some afferents over others that mature at different times. These could
also be depicted in this manner by assuming that the relative size of the structures depicted represents afferent-
target biases in general. Although displacement can also explain parcellation processes, these are not depicted
here. They would roughly follow Ebbesson's schema with the added provision that parcellation is not spon-
taneous, but must be induced by a change in the relative numbers of target synapses with respect to competing
axons o r changes in axon-target affinities. Even if enlargement of both afferent and target populations during
generalized size increase is isometric, there may be limited collateral extent of correlated axon activity such
that diffuse overlap of connectivity could not be maintained and axons from the same source would have a
better chance of eliminating interdigitate axons from more diverse origins.

hood of synapse formation with respect to hypothesis it assumes that the basic molec-
axons arriving out of synch with cell mat- ular affinities between initial connections
uration. As a result heterochronous and their targets a r e essentially conserva-
changes in developmental time schedules tive, and if anything, only change in
for different systems may be a source of response t o prior displacement events,
developmental bias analogous to differ- under selection to stabilize a newly adap-
ences in size of competing projections. T h e tive circuit against the regressive influ-
increased affinity for synchronously arriv- ences of competing biases. What is missing
ing axons should have the same effect as from both invasion and parcellation the-
relative enlargement of one source or tar- ories is a cause. Displacement theories
get area with respect to another. introduce cause in the form of regressive
Both invasion-like and parcellation-like processes (e.g., cell death or reduction of a
processes are explainable in this way. What peripheral sensory o r motor system) o r dif-
is different about displacement hypotheses ferential growth processes (e.g., unequal o r
is that they propose that all such events are hyperplasic neuron production, expansion
driven by competitive biases between dif- of some peripheral organ, o r hetero-
ferent axon populations and their pro- chronic change in maturation schedules for
spective targets and not by instructional different structures).
processes such as might be encoded in Finlay et al. (1987) suggest that regres-
molecular affinities. T h e strong form of sive events during development, such as
the displacement hypothesis denies both cell death and axon retraction, may account
the possibility of spontaneous axon inva- for total brain size variation, the elabora-
sion and also the possibility of spontaneous tion of specialized sensory, motor or cog-
parcellation. But like the parcellation nitive adaptations, and allometric dispro-
portions of specific systems during brain
evolution. Widespread cell death appears
to be a normal developmental mechanism
for sculpting cell populations of intercon-
nected structures. T o a limited extent cell
death may be exaggerated or eliminated
by variations in afferent populations o r
efferent associations. These effects are,
however, buffered in systems with multiple
afferent sources and efferent targets, and
so can be expected to be most significant
in systems with highly limited connectional
relationships. Neural populations of
peripheral sensory and motor projections
a r e generally entirely dependent o n
peripheral structures as afferent sources or
efferent targets, respectively, and provide
the most notable examples of variation in
cell death.
A number of the changes in CNS orga-
nization in response to the evolution of
novel sensory organs o r motor systems may
thus be the result of such a sculpting pro-
cess. Wilczynski (1984) reviews evidence
for the neural reorganization of CNS cell
populations and connections in response to
some major vertebrate sensory and motor
specializations (e.g., auditory, electrical and
infrared reception) that show relatively
subtle differences centrally in response to
major changes of the periphery. Despite
homoplaseous peripheral changes, central
reorganization often recruits homologous
systems for similar perceptual processes.
H e argues that the interlocking of periph-
eral and central reorganization in these
cases arises out of competitive develop-
mental processes that match peripheral
functional requirements to central func-
tional predispositions and match cell pop-
ulations to one another. Although there
may be major changes in cell number in
peripherally specialized nuclei as a conse-
quence of cell death there appear to be no
"cascading" effects on cell death through-
out the remainder of their functional con-
nections within the CNS.
T h e main point of the cell death hypoth-
esis proposed by Finlay et al. (1987) is to
account for quantitative allometric changes
in the brain and brain structures. How-
ever, there are a number of reasons why
cell death is unlikely to be a significant fac-
tor in major allometric changes. First, in
order to play a significant role it must be
able to account for at least a major part of
the many thousandfold differences in brain
size. Small brains are simply not analogous
to large brains that have experienced 99%
cell death. T h e role of cell death is clearly
limited to secondary "fine tuning" of inde-
pendently developed functionally inter-
dependent systems (although it may reach
80% in peripheral receptors). Second, as
compared t o peripheral systems, the evi-
dence suggests that the total amount of cell
death is relatively small in most forebrain
structures, even if peripheral structures
relaying information to them are signifi-
cantly reduced (Rakic, 1988). This prob-
ably correlates with the fact that forebrain
structures receive afferents from and send
efferents to diverse cortical and subcortical
structures rather than just one, as in
peripheral structures. T h e cell d e a t h
reported in areas like cortex appears t o be
associated with cells maintaining transient
synapses during early phases of develop-
ment that may serve a preliminary organ-
izing role for later stages. If there was sig-
nificant cell death in t h e normal
development of cerebral cortex it would
have to be relatively uniform because of
the remarkable uniformity of cell numbers
per area in all areas and all species. T h e
initial production of neurons (or the initial
production of "ontogenetic units" with
fixed neuron production patterns) is prob-
ably much more important in determining
populations in most structures.
Finlay et al. (1987) also point out the pos-
sible significance of heterochronous mat-
urational processes for both cell death and
connectivity patterns. They argue that ear-
lier maturation or delayed maturation of
areas may introduce competitive biases in
normal axonal competition. Since some
competitive processes may extend for only
a few days, significantly delayed o r pre-
mature connections may be left out of the
competition, with cell death o r connec-
tional replacement resulting. Although
Gould (1977) argues for the widespread
presence of heterochrony in other systems
(e.g., somatic growth and puberty) there is
little evidence concerning variance of mat-
uration schedules in the mammalian ner-
vous system at this time. However, time
scale effects may be significant in mam-
malian brain evolution. T h e maturation of
a small mammal brain may b e completed
within the space of weeks whereas that of
a large brain may take many years. This
means that the absolute time scale of com-
petitive-regressive events during matura-
tion can differ enormously despite the like-
lihood thqt, at the synaptic and cellular scale
the trophic processes that underly these
effects are the same for all mammal brains.
T h e prolongation of these events in larger
species might affect variability, degree of
differentiation o r sensitivity to extrinsic
influences. In non-mammalian vertebrates
where neurogenesis may persist through-
out the lifespan heterochrony may be a
more significant factor.
In previous papers I have also proposed
that axonal competition and other regres-
sive processes play crucial roles in brain
evolution (Deacon, 1984, 1988b, 1990c),
but I have focused largely on the possible
influences of size relationships. If the
determination of initial cell number in most
structures takes place prior to major axonal
invasions, the major role of competitive and
regressive processes must be the subdivi-
sion of these neurogenetic fields with
respect to each other. Even though no cell
death nor substantial cell saving may result
from increases o r decreases of specific
afferents o r efferent targets of a multiply
connected structure within the CNS, such
changes can substantially alter local axonal
competition processes. Rather than axonal
competition determining the size of brain
structures via cell death (probably only sig-
nificant for peripheral structures), the rel-
ative sizes of interconnected brain struc-
tures should be a major determinant of
patterns of axonal connection.
Allometric effects are probably the most
common sources of bias, given the enor-
mous range of brain sizes and the great
ranges in the relationships between central
and peripheral systems. These effects are
not limited t o unusual reorganization
events. Deviations from isometry with phy-
letic size increase is the rule among brain
structures as in peripheral organs (e.g.,
Armstrong, 1985; Campos and Welker,
1976; Deacon, 1988b; Gould, 1975; Pas-
singham, 1975; Sacher, 1970; Stephan,
1969). T h e systematic differentials in neu-
ronal production in different structures in
brains of different sizes should determine
correlated differences in structural parcel-
lation throughout. For example, the reg-
ular increase in proportion of visual asso-
ciation cortex with respect to visual
koniocortex in brains of increasing size may
reflect a growing competitive disadvantage
for primary projections in the recruitment
of cortical space determined by a growing
disproportion between the retina and its
potential thalamic and cortical targets.
As we examine species differences in
neural organization we should expect to
see certain necessary correlations between
changed connection patterns and the allo-
metries of the various structures involved.
For example, in cases where an invasion
event is suspected to have taken place one
would expect to find some corresponding
deafferentation of the new target by a for-
mer projection source that has regressed
in size with respect to its target, o r some
unusual size increase in the new source
structure relative to its normal target, o r
significant regression of its normal target.
In cases where loss of connection is sus-
pected either cell death in the source or
target or, alternatively, displacement by a
projection from a disproportionate com-
peting afferent source would be expected.
Failure to find these correlates either in
adult brains o r during development would
falsify a displacement interpretation.
Displacement hypotheses are falsifiable
in ways that parcellation o r invasion
hypotheses are not because a displacement
explanation is an account of a mechanism
not merely of a change in structure. T h e
displacement hypothesis is essentially an
extension of well studied mechanisms of
developmental axonal plasticity. T h e pro-
duction of topographic functional and con-
nectional organization within a developing
area induced by reduction o r over-exag-
geration of input from some outside source
is the limiting case for developmental dis-
placement. T h e extension of this concept
to incorporate allometric influences as a
major source of bias on major projection
patterns completes the synthesis of allo-
metric effects, neogenetic processes and
developmental processes.
Displacement interactions can also con-
ceivably account for true invasions of axons
into targets that even exuberant projec-
tions would not otherwise contact. It is not
necessary to assume any changes in the
actual affinities of axons for their targets,
only t h e reduction of t h e specificity
requirements for target affinity. This may
occur under some extreme conditions. In
an earlier section it was noted that the ini-
tial target specificity of many neural con-
nections is significantly underdetermined.
This has been best documented for cortical
afferents and efferents but has also been
noted widely in the developing nervous sys-
tem. As a result, initial axonal projections
invade a multitude of diffuse targets and
may establish numerous transient synapses
that will later be eliminated. There prob-
ably are some predetermined affinity gra-
dients involved because these initial pro-
jections are far from entirely random.
Edelman (1987) has argued that this initial
affinity between axons and potential target
cells is the result of specific cell surface
molecules that exhibit a range of interac-
tion o r "recognition" strengths (analogous
to immunological binding relationships).
In order to produce distinct connections
these affinities need not be highly specific
so long as there is either a significant
threshold difference between nearby
potentially competing projections or a
means for dynamic parcellation of rela-
tively nonspecific projections, as is found
in cortex. Extremely weak axon-target
affinities can likely only exhibit themselves
when all competing affinities are essentially
eliminated o r when extremely strong com-
petitive biases are introduced. Elimination
of alternative stronger affinity competitors
can occur if the majority of normally
occurring transient and permanent affer-
ents to an area are eliminated, o r if a nor-
mal target is essentially eliminated, forcing
axons to compete for alternative low affin-
ity targets. Strong biasing may also occur
if a weak affinity afferent source becomes
disproportionately large with respect to
both its normal target and nearby low affin-
ity targets.
An experimental example demonstrates
this possibility. Frost and Metin (1 985) and
Sur et al. (1988) have demonstrated the
possibility of inducing optic afferents to
project to inappropriate thalamic nuclei
and thus relay inappropriate sensory infor-
mation to their cortical target areas. T o
accomplish this in a developing rat they
destroyed all the normal targets of the optic
projections (including lateral geniculate,
superior colliculus and visual cortex) and
additionally deafferented another tha-
lamic nucleus (e.g., either the ventrobasal
o r the medial geniculate nucleus) by cut-
ting ascending (spinothalamic o r tecto-
thalamic) fibers. One of these procedures
is diagrammed in Figure 15. Despite the
fact that the misrouted connections inner-
vate anomalous thalamic targets which
project t o non-visual cortical areas, cells in
these areas exhibited response properties
appropriate t o visual cortex. This dem-
onstrates that fundamental rewiring is
achievable by displacement and that the
new connections thereby established can
differentiate their targets appropriate to
their new functions. However, it may be
significant in these cases that the alternate
thalamic and cortical targets are homolo-
gous with the normal targets at some level.
Similar natural experiments appear to be
exhibited by different breeds of Siamese
cats. These cats all have abnormal routing
of ipsilateral projections to the contralat-
era1 lateral geniculate with the result that
the visual field maps are misaligned. When
the lateral geniculate projections reach the
cortex they are dealt with in one of two
ways depending on the breed: 'they are
either inactivated so as not to interfere with
the remainder of the map o r form an iso-
lated independent map that' is inserted
adjacent to the otherwise normal map (Kaas
and Guillery, 1973; Guillery, 1974). What
factors bias the axonal competition toward
one o r the other option are not known.
Analogous competitive processes may
underly the evolution of new cortical areas.
Simple invasion is astronomically unlikely
because it can only occur when there is a
significant loss of target affinity in one set
of axons and simultaneously a significant
increase in affinity for that same target area
by other axons that have also simulta-
neously lost affinity for their own target.
Each of these conditions involves an inde-
pendent mutational event that alters the
respective cell surface molecules or causes
certain whole classes of cells to die. In con-
trast, invasion by displacement need not
involve any changes in affinity o r signifi-
cant cell death. T h e only conditions
required are either significant allometric
disproportions between areas or the elim-
ination of some target area o r the elimi-
nation of some projection as a result of
some. degenerative event in evolution.
These conditions are probably not at all
uncommon in the course of evolution. Sig-
nificant allometric changes in proportions
between different structures and projec-
tion systems is the rule in all mammalian
and nonmammalian lineages where brain
size has changed by many orders of mag-
nitude. Such a principle may account for Normal connections
the parcellation trends in neocortical areas
seen in larger mammalian brains.

DISPLACEMENT THEORIES OF CORTICAL

EVOLUTION: FOUR EXAMPLES
Multiplication of cortical areas and their
differential allometry
T h e enlargement of the entire cortical
mantle with increasing brain size may influ-
ence cortical differentiation indirectly by
altering competitive interactions among
cortical afferents. There may be limits to
the size of a single projection field deter-
mined by the number of specific afferents
that are available o r bv intrinsic functional
constraints. If changes in the size of the
cortical mantle a n d different thalamic
nuclei are not isometric in the course of
evolution then there may be correlated
changes in the relative size of correspond-
ing projection fields. Changes in propor-
tion may also be influenced by network
allometry influences that impose func-
tional costs on enlarging areas. Such con-
straints might contribute to the break-up
and duplication of cortical fields in brains
of increasing size. T h e multiplication of
areas and the differential expansion of some
Rerouting of connections
after fetal lesions of visual
targets maintains visual
function in aberrant targets.
FIG. 15. Misrouting of axons by target elimination
.
is demonstrated by, experiments in which the normal
targets of one projection a r e eliminated by lesion in
fetal development and the projections t o a different
(serially homologous) target a r e prevented from
forming. In the case depicted here from Frost and
Metin (1985) the targets of the optic nerve- the lat-
eral geniculate nucleus of the thalamus [LG] and the
superior colliculus [SC]— and the target of the lateral
geniculate nucleus-the visual cortex [Vis]— were
damaged by fetal lesions as were the ascending somatic
sensory afferents of the medial lemniscus which would
normally synapse in the ventrobasal nucleus of the
thalamus [VB]. Consequently, t h e optic fibers were
thereby induced t o invade the ventrobasal nucleus of
the thalamus. T h e otherwise normal projection of this
nucleus t o the location of somatic cortex induced this
area to behave as though it were visual cortex.
cortical areas with respect to others may
also be influenced by the total size of the
entire cortical mantle with respect to the
sizes of other brain structures that are con-
nected with it. This indirect influence is
suggested by the predictable allometric
scaling of the sizes of cortical areas with
the total size of the isocortex across many
species (Passingham, 1975; Deacon, 1988b).
Probably the most significant determin-
ing factor in such cases is the relative size
of the afferent projection as compared to
its cortical target zone. A cortical target
area that has expanded with respect to its
afferent projections is in some ways anal-
ogous to a cortical area with a reduced
afferent projection. Either should produce
a decreased density of adjacent correlated
inputs which may impair the ability of spe-
cific inputs to successfully out-compete and
eliminate diffuse inputs. In the case of
depleted afferents (Rakic, 1 988) the size of
the differentiated area is reduced and space
is given u p to neighboring areas. Neigh-
boring cortical areas would also face the
same difficulty. Parcellation of afferent
projections to form duplicate adjacent pro-
jections may thus be a result of reaching
some threshold of competitive instability
determined in part by the size of the affer-
ent map (which may itself be matched in
size to its peripheral representation by cell
death) and in part by the independently
growing information processing costs of
network allometry within the cortex.
The increasing proportion of association
cortex to projection cortex that correlates
with increasing brain size could reflect pro-
gressive competitive disadvantages for
direct peripheral projection systems in
some modalities, both in recruiting tha-
lamic targets and in recruiting cortical tar-
gets via these thalamic projections. This
would follow if the proportion of periph-
eral axons to central axons competing for
targets declined with size. This kind of tar-
get expansion would have parcellation
effects analogous to partial deafferenta-
tion. Visual deafferentation experiments
in monkeys have demonstrated both a
reduction in striate cortex area and an
expansion into this territory by adjacent
visual association projections (Rakic, 1988).
T h e relative negative allometry of the pro-
jection nucleus of vision (the lateral genic-
ulate nucleus) with respect to the volume
of the corresponding visual associational
nuclei (the pulvinar complex) as well as with
respect to the rest of the thalamus (Arm-
strong, 1979; Hopf, 1965; Stephan et al.,
198 1) lends further support to a displace-
ment explanation for this evolutionary
trend. Figure 16 diagrams the major fea-
tures of this hypothesis in comparison to
deafferentation experiments. Deafferen-
tation as a result of adaptational loss o r
reduction of a peripheral sense organ-as
in blind cave dwelling species, o r to a lesser
extent in fossorial o r nocturnally special-
ized species-should also produce this sort
of effect in cortical areal architecture, but
in a brain that is unusually small for this
pattern in that modality. Studies of such
naturally deafferented species has dem-
onstrated reduction of cortical represen-
tation of these sensory areas but the issue
of projection area to association area ratio
has not been investigated.
I t is possible that the process of area sub-
division may be a gradual evolutionary
event in areas with relatively diffuse topo-
graphic organization. Area boundaries may
not be discrete and connectional differ-
ences may exhibit a gradient-like organi-
zation in these cases. Such incipient area
divisions should be more likely in associa-
tion areas lacking clear sensory o r motor
topographic organization and we should
expect to see increased individual variation
in these areas if this is the case. This pat-
tern should contrast with that of cortical
areas that map topographically organized
representations of some peripheral modal-
ity. In these cases area differentiation
should tend to be more discrete and pre-
dictable. T h e border between visual area
17 and 18 and between 18 and 19 is easily
distinguishable and correlate's with func-
tional map boundaries but the multiple
retinotopic maps within area 19 of the
monkey cortex are not easily correlated
with any architectonic borders. T h e appar-
ent tendency for middle level cortical asso-
ciation areas to exhibit the greatest level
 of subdivision and functional diversity from
species to species may be a correlate of the
relative fluidity of these divisions.
If the tendency for cortical circuits to
subdivide and differentiate their cortical
targets with respect to one another in
development is exaggerated by brain size
increase and brain size increase is corre-
lated with the evolution of increased body
size, then neither selection for augmented
specialized functions nor selection for gen-
eralized brain size increase (and increased
general intelligence) needs to b e involved
in order to explain cortical enlargement
and complexification. Multiplication of
cortical areas might be accounted for, not
as augmentation of function, but as a
response to a growing size differential
between peripheral projections and cen-
trally originating projections as well as a
response to deterioration of integration and
processing efficiency caused by the con-
comitant reduction of connectivity in a
larger cortex. Advancement of function is
not necessary to explain the multiplication
and differentiation of cortical areas. Func-
tional adaptation is not precluded, but to
demonstrate it requires more than dem-
onstrating an increase in cortical areas and
differentiation of functions within those
areas. These other correlates of size must
FIG. 16. Displacement theory of association area be "subtracted" before a proper assess-
expansion is depicted for visual areas in two hypo- ment of functional advancement can be
thetical brains of different sizes but receiving input made. Nonetheless, with the addition of
from eyes that differ little in size. T h e geniculo-striate duplicate areas o r with the differentiation
pathway is depicted by solid black arrows and dark
gray targets and the tecto-pulvinar-extrastriate path-
of functions into independent component
way is depicted by dashed gray arrows and light gray processes, new possibilities for specializa-
targets (assuming homology of the pulvinar and lat- tion arise that could not coexist in a com-
eral posterior nucleus). In the expanded brain of B mon area. This must certainly be a rich
there has been an expansion of the thalamus and the source for "preadaptations."
cortical target field potentially available for both pro-
jections but because the direct retino-thalamic pro- Once adaptive alternative connection
jection is not significantly larger it is not capable of patterns are established by whatever means
recruiting a correspondingly larger LGN from the there may be selection for changes in axon
expanded thalamus and may also be at a competitive affinities and other biasing factors that limit
disadvantage in competition for space within the supe-
rior colliculus as well with respect to other possible
competing inputs. However, the size of the afferents
to the pulvinar are appropriately enlarged and recruit
a large portion of the thalamus. T h e consequence for expansion of the pulvinary projection field may fur-
cortical parcellation is that the geniculo-cortical affer- ther induce its parcellation because of increased
ents are at a disadvantage in the competition for cor- regional differentiation of correlated activity, but also
tical territory with respect to pulvinar afferents and possibly because the information arriving in the pul-
so the striate cortex will occupy a reduced proportion vinar may include inputs that reflect the effects of
of the entire visual projection field. T h e additional partially displaced retino-tectal projections.
variability. Because of these develop- also seem to respect the general "level" of
mental biases, parcellation patterns will cortical area. Both origin and termination
become increasingly resistant to rever- patterns are more diffuse across lamina in
sions, even if the conditions that originally association areas (Barbus, 1986; Deacon,
induced parcellation are undermined. This 1 989a). Similar laminar connection pat-
suggests that size-induced parcellation pat- terns have also been identified in some areas
terns may persist even if brain size decreases of cat (Bullier et al., 1984), tree shrew
in subsequent lineage. Retention of corti- (Semsa et al., 1984) and rat cortex (Deacon
cal features consistent with a much larger et al., 1989), but there is too little infor-
brain has been documented in a number mation for non-primate species to be sure
of dwarf species (e.g.,Warren and Carlson, of its generality.
1986). This suggests that there may be T h e consistent association of termina-
functionai costs associated with brain size tion patterns with the architectonic and
reduction in evolution. T h e possibility for functional gradient between association
irreversible changes and corresponding areas and sensorimotor areas clearly indi-
asymmetrical selection against size reduc- cates that this hierarchy, which has been
tion brings us full circle to a possible pro- the central feature in all additive theories
gressive or directional tendency in brain of cortical evolution, must also be
evolution. accounted for in terms of parcellation and
displacement processes in evolution. Else-
where (Deacon, 1989a) 1 have referred to
Laminar segregation of afferents: these reciprocally directed pathways as
Implications for areal parcellation centrifugal (limbic-association-sensory/
and the origins of cortex motor cortex) and centripetal (sensory/
Connectional patterns between cortical motor-association-limbic cortex) projec-
areas appear to parallel the cytoarchitec- tions because they are oriented with respect
tonic differentiation of cortical areas. to areas specialized for peripheral infor-
Because of this regularity they may provide mation at the one extreme and areas con-
some insights into the connectional dis- cerned more with internal states of arousal
placements, invasions and parcellations that a t the other (see Fig. 18). This hierarchic
constitute area differentiation in evolu- chain of cortical areas within each func-
tion. Tracer studies of corticocortical con- tional modality increases in number of areas
nections in monkey brains have revealed and corresponding synaptic links as brains
characteristic laminar origin and termi- enlarge in evolution, yet replicates the same
nation patterns that seem to be general- systematic pattern of laminar connectivity
izable to many if not all regions of cortex with each addition. A number of research-
(Barbus, 1986; Deacon, 1985; Galaburda ers have linked this asymmetric reci p rocal
and Pandya, 1983; Jones et al., 1978; connectivity pattern to Sanides' evolution-
Maunsell and Van Essen, 1983; Primrose ary sequence of cortical differentiation (e.g.,
and Strick, 1985; Rockland and Pandya, Barbus and Pandya, 1982, 1987; Gala-
1979; Tigges et al., 1973, 1977). In gen- burda and Pandya, 1983; Pandya a n d Yet-
eral, connections that originate from asso- erian, 1985). This asymmetry is presumed
ciation areas and project to areas more spe- to be explainable as a terminal addition
cialized for a peripheral sensory o r motor process whereby new areas are always con-
function tend to originate largely from cells nected t o their immediately adjacent
in layer V of cortex and terminate in layers ancestral area by one sort of laminar con-
I and VI. Connections that originate from nection pattern and are reciprocated by its
specialized (e.g., primary) sensory a n d complement. Despite the rejection of San-
motor areas and project to association areas ides' theory on a number of grounds, the
tend to originate largely from cells in layer correlations it suggests must be accounted
I II of cortex and terminate predominantly for. With the repudiation of theories claim-
in layers III and IV (see Fig. 17). There ing terminal addition o r terminal differ-
are also subtle gradation differences that entiation of cortical areas, we are forced
 parcellation of cortical laminar connectivity
in the process of areal parcellation of isocortex

corticocortical laminar connectivity before parcellation

corticocortical laminar connectivity after parcellation

FIG. 17. Laminar segregation of corticocortical connections due to functional parcellation of cortical areas
is depicted on the assumption that both the ancestral and developmentally prior state are an undifferentiated
laminar termination pattern. The hypothesized undifferentiated state is depicted in the upper figure as a
single cortical area with intrinsic connections. The subsequent loss of selected classes of connections with area
parcellation is depicted in the lower figure. Note that the culled connections are asymmetric with respect to
their directional orientation. Possible sources of competitive bias that might drive this asymmetric parcellation
during development are discussed in the text.

to explain this correlation between archi-
tectonic gradients, asymmetrically pat-
/
terned reciprocal connections, inverse
maturational gradients, and the apparent
functional hierarchy of cortical areas in
terms of competitive biases and displace-
ment processes in cortical development.
At the present time there is no devel-
opmental information concerning corti-
cocortical laminar differentiation pro-
cesses. Nonetheless, speculation concerning
the possible mechanisms involved can be
concentrated on a few plausible factors. For
corticocortical connections within a corti-
cal area there does not seem to be this level
of laminar specification (Rockland and
Pandya, 1979). T h e differentiation of a new
cortical subdivision out of a single ancestral
area must therefore correlate with a loss
of projections to certain cortical lamina.
Furthermore the loss is different depend-
ing upon whether the projection is in the
centrifugal o r centripetal direction. Since
the appearance of a new cortical division
must be a consequence of the competitive
parcellation-displacement processes, these
systematic connectional losses likely cor-
relate with competitive asymmetries
between different afferent populations.
This suggests that we should look for cor-
responding biases, either in terms of het-
erochronic, allometric o r functional dif-
ferences, that distinguish association areas
from specialized sensory/motor areas. In
fact, all three possible sources of bias can
be identified and are probably not inde-
pendent.
Another important clue concerning the
particular cortical lamina that distinguish
these different cortico-cortical projections
comes from the finding that different
classes of thalamo-cortical projections also
appear to segregate according to termi-
nations in these same lamina. Multiple tha-
lamic nuclei project to each cortical area
but tend to terminate in different lamina
within the same area. It appears that prin-
cipal thalamic projection nuclei, whose
projections are generally limited to a single
architectonic area, tend to terminate in
columnar fashion within layers III and IV,
usually coinciding with the distribution of
granule cells in those layers (Diamond,
1982; Frost and Caviness, 1980). Intralam-
inar thalamic nuclei, which exhibit rela-
tively non-specific projections to many cor-
tical areas, tend to terminate in layer VI
(Frost and Caviness, 1980; Herkenham,

centripetal
centrifugal
FIG. 18. Centrifugal and centripetal corticocortical
projections are depicted on idealized flattened maps
of the cerebral cortex of one hemisphere. Areas
depicted in darkest gray are koniocortical areas o r
specialized motor cortex, those in lightest gray are
association cortex, and the white perimeter repre-
sents limbic cortex. T h e arrows represent multisy-
naptic pathways from area to area extending either
from koniocortex (or motor cortex) to intermediate
association cortex to paralimbic association cortex to
limbic cortex (centripetal) or from limbic cortex to
paralimbic association cortex to intermediate associ-
ation cortex to koniocortex (or motor cortex). T h e
terms centripetal and centrifugal are chosen not
because of their spatial connotations (which may be
somewhat confusing in this depiction) but because of
the orientation of these projections with respect to
the gradient between areas specialized for peripheral
systems and those representing regulation of internal
state.
1980; Rausell and Avendano, 1985). Other
nonspecific nuclei that project to many
areas within the same modality and midline
"limbic" nuclei, which also exhibit wide-
spread paralimbic cortex and association
cortex projections, tend to terminate in
layer I (Diamond, 1982; Friedman et al.,
1987; Frost and Caviness, 1980; Rausell
and Avendano, 1985). T h e non-specific and
limbic nature of thalamic projections t o
layers I and VI and the specific projections
to layers III and IV can be interpreted as
functionally analogous to their counter-
parts among cortico-cortical projections in
a number of ways. Middle layer projections
appear always to introduce information
associated with a source that is more
directly connected with the peripheral ner-
vous system than are their target, whereas
deep and superficial layer connections
appear to convey information that ulti-
mately derives from systems involved more
with the regulation of internal state, as well
as attentional and emotional arousal (Dea-
con, 1989).
Two important heterochronic matura-
tional factors differentiate cells and axons
in these cortical lamina. These correlated
heterochronic differences may account for
which lamina tend to be associated with
which afferents by virtue of their biasing
influence on axonal competition. Neurons
occupying positions that would be super-
ficial to layer II and deep to layer VI in the
adult brain mature before the cells of the
cortical plate and form a single primordial
cortical layer. Cells in the outer layer called
Cajal-Retzius cells exhibit two large
"extraverted" dendrites that extend up
toward t h e pial surface a n d laterally,
whereas cells in the deep layer called Mar-
tinotti cells are of a distinct bi p olar shape
with dendrites extending more superfi-
cially a n d deeper. Cortical plate cells
migrate into position in an inside-out pat-
tern between these two cell layers. T h e ear-
liest cortical plate cells to mature are the
deep layer V and VI pyramidal cells and
the very last cortical plate cells to mature
are the most superficial pyramidal cells of
layers II and III and the granule cells of
layer IV. Prior to the appearance of the
cortical plate neurons both primordial cell
types appear to establish transient synapses
with early afferent projections (Marin-Pa-
dilla, 1978). Although there is some dis-
agreement on the ultimate fate of these
early maturing cells most argue that they
are eliminated by programmed cell death
in most isocortical areas (although they
appear to pqrsist in entorhinal cortex and
in paralimbic isocortex in small species, and
in all cortical areas in cetaceans; see next
section).
Although it is not known what structures
give rise to the afferent projections that
synapse on the transient cells above and
below the developing cortical plate, it is
reasonable to assume that they arise from
the same structures that will later inner-
vate' the corresponding deep and superfi-
cial lamina in the adult. T h e fact that the
thalamic afferents terminating in layers I
and VI are nonspecific projections and do
not appear to respect cortical boundaries
(Caviness and Frost, 1980; Diamond, 1982)
may reflect their arrival prior to cortical
plate afferents that subdivide the cortex
into-:discrete functional regions. If the
transient 'cells to which these early axons
/
contact are later eliminated, these axons
may be displaced onto adjacent pyramidal
cell dendrites in the deepest and most
superficial lamina of cortex (see Fig. 19).
Since different target cells within the cor-
tex mature at different times and different
projections arrive at different times, tem-
poral correlation may play an important
role in biasing laminar connection patterns
from both thalamic and cortical sites. Early
maturing cells located deep and superficial
to the cortical plate may correlate with the
early maturing projections and late matur-
ing small cortical plate cells in layers III
and IV may correlate with relatively late
maturing projections. Differences in the
relative maturation times of cells and axons
from one cortical area to another might
additionally contribute to areal differences
in laminar organization.
Another possible heterochronic bias that
may influence the asymmetric direction-
ality of these projections can be discerned
in the differential myelination of thala-
mocortical fibers from principal thalamic
nuclei projecting to these areas. Since my-
elination appears to precede from special-
ized areas to association areas the compe-
tition for synapses in the middle cortical
lamina may be biased by earlier myelina-
tion of ai-eas that are more peripherally
specialized.
An allometric bias is reflected in the
expansion of association areas relative to
sensory/motor specialized areas in larger
brains. As noted above, this suggests that
primary projection areas, which are more
directly linked to peripheral systems, are
competitively constrained by the size of
their afferent projections, whereas affer-
ents to association areas have no such
extrinsic constraints. This may also be the
reason these areas appear to exhibit less
clearcut cytoarchitectonic divisions. T h e
gradient in architectonic specialization is
one of the primary bases for Sanides' argu-
ment.
Functional differences are also consis-
tently correlated with this gradient. For
example, neurons in striate cortex appear
to be precisely "tuned" to specific, highly
localized stimulus attributes and are orga-
nized according t o precise retinotopy
whereas neurons in inferotemporal visual
association areas, at the extreme opposite
end of the hierarchy, seem tuned to global
stimulus attributes and exhibit very large
receptive fields with no obvious topo-
graphic organization. This is undoubtedly
also a correlate of the relative directness
or indirectness of their respective retino-
cortical afferent circuits (Kaas, 1989). At
the sensory end of the spectrum of areas
input from the periphery is highly variable
and functional correlation is only exhib-
ited over very short distances, whereas at
the association end input is primarily lim-
bic and likely highly intercorrelated over
relatively larger distances. Since functional
specialization of cortical areas can be sig-
nificantly affected by sensory experience
during early development it is almost cer-
tain that differences in the correlation of
afferent signals among adjacent axons play
a major role in determining which con-
nections persist into adulthood.
Finally, the issue of network allometry
should be considered. Given the fact that
break-up of previously integrated func-
tional areas effectively distributes process-
ing across a number of areas, functioning
to some extent in parallel, cortico-cortical
 Pattem of isocortical neurogenesis
and probable programmed cell death

prior to the early invasion addition of cortical probable elimination of cells

cortical plate cortical plate cells plate cells to outside the cortical plate and
external layers specialization of granular layer

Hypothesis to account for development of

laminar specificity of cortical afferents

early non-specific displacement of non-specific

thalamic (+?) projections projections from eliminated
cells to cortical plate cells and
invasion of specific thalamic projections
FIG. 19. A theory of the displacement processes involved in laminar parcellation of cortical afferent con-
nections and a possible explanation of their relationship to neocortical origins. T h e upper figure diagrams
the events of corticogenesis assuming programmed cell death of cells that precede the formation of the cortical
plate (it is also possible that some of these precursor neurons are converted into neurons with different
morphologies in the mature cortex). Note that neurons forming the cortical plate migrate into position
between the two groups of cortical precursor cells above and below it and deposit in the uppermost layers of
the developing cortical plate. T h e lower figure depicts a displacement theory for the laminar segregation of
cortical afferents during cortical development. It is hypothesized that axons from early maturing non-specific
thalamic nuclei and possibly early maturing limbic areas establish synapses on the two populations of cortical
precursor cells and maintain them as cortical plate neurons are added and the two cell groups are forced
apart. After the formation of the cortical plate selective cell death of the precursor cells forces the axons
attached to them to seek alternative synaptic contacts. They are displaced onto the dendrites of cortical plate
neurons of the same lamina. These axons may have a competitive advantage because of their numbers and
functional maturity compared to the later arriving principal thalamic afferents that target cortical plate cells
in middle layers. T h e two independent populations of neurons, superimposed by the migration of the cortical
plate cells, with different maturation schedules and distinct classes of afferents, suggest the possibility that
t hey derive from independent phylogenetic origins-the precurser cells from the dorsal cortex and the cortical
plate cells from the dorsal ventricular ridge of a reptilian ancestor.
connections should be competitively about these brains that causes them to
selected during development that maxi- diverge from these otherwise ubiquitous
mize intercorrelated function and most trends will unquestionably provide impor-
efficiently distribute processing demands tant insights into the causes for the general
throughout the network. Such an inter- trends.
pretation is suggested by the "counter-cur- Some of the most striking exceptions can
rent" organization of these cortico-cortical be found in the dolphin brain (and pre-
connections (see Deacon, 1989). sumably in all cetacean brains). Many of
This analysis of laminar maturation and the unique architectonic features of the
connectional differentiation suggests an dolphin brain have been meticulously doc-
alternative interpretation for the origins of umented in a series of recent papers (Jacobs
mammalian isocortex that combines both et al., 1971, 1979, 1984; Morgane and
the equivalent cell hypothesis and invasion Jacobs, 1972; Morgane et al., 1982, 1985,
by displacement. My suspicion (also sug- 1986a, b, 1990). These findings concern-
gested in Marin-Padilla, 1978) is that these ing the dolphin brain are paradoxical in
transient cells are the homologues of the the context of traditional theories of mam-
cells of the ancestral dorsal cortex of rep- malian brain evolution because they sug-
tiles and that the cortical plate cells rep- gest that dolphin brains combine features
resent a phylogenetically later intrusion that are considerably highly advanced with
(following the equivalent cell hypothesis) features that are considered quite primi-
perhaps from ancestral dorsal ventricular tive and conservative (Glezer et al., 1988).
ridge positions. T h e death of the reptilian T h e highly advanced features of the dol-
dorsal cortex homologue cells in mam- phin brain are largely macroscopic mor-
malian ontogeny induces the displacement phological features, including a large brain
of their afferents onto the apical dendrites size, a high degree of encephalization, a
of these recently juxtaposed nonhomolo- highly convoluted cortex, a high ratio of
gods cells of the cortical plate. T h e cortical neocortex to total cortex (and therefore a
plate cells also maintain their original high ratio of neocortex to limbic cortex),
afferents and thereby establish a novel and apparently (although this is difficult to
integration of these ancestrally separated assess accurately) a large percentage of
and independent circuits. In this sense the association cortex. Dolphins also are con-
laminar termination pattern of centrifugal sidered to be among the most behaviorally
pathways links them with the ancestral dor- advanced species by many behavioral
sal cortex system (which has always been researchers (Herman, 1980; Würsig, 1989;
linked with limbic cortex) and the laminar but see critique by Gaskin, 1982). In con-
pattern of centripetal pathways links them trast, their conservative traits are largely
with the ancestral dorsal striatal (dorsal microscopic features, including relatively
ventricular ridge) system. thin and poorly laminated isocortex, essen-
tially agranular (and some would argue,
Cetacean brain evolution nonexistent) layer IV and therefore no typ-
In the preceding sections I have referred ically definable koniocortical areas, appar-
to a number of general trends in mam- ent lack of a gigantopyramidal cortex (i.e.,
malian brain evolution that appear to be architectonically specialized primary motor
strongly correlated with brain size. These cortex; although some evidence of this can
include both microscopic and macroscopic be discerned in the form of larger layer V
features of brains, all of which ultimately pyramidal cells), remarkably thick layer I
have to be understood in terms of biases with respect to the rest of the cortical lay-
and constraints that modify developmental ers, a well developed layer VI, densely
processes, and most particularly, axonal packed layer II, large "extroverted" cells
competition/parcellation processes. It is in layer II, poorly defined columnar orga-
therefore important to consider excep- nization, indistinct architectonic bound-
tional cases where these correlations do not aries, and apparent adjacency of sensory-
seem to hold. Understanding what it is motor projection areas with respect to
 dorsal view association areas (see Fig. 20). Glezer et al.
(1 988) are compelled to designate a special
"conservative-progressive mode" of cor-
tical evolution to account for this anoma-
lous combination of features.
T h e dichotomy between macroscopic
morphological features and microscopic
cytoarchitectonic features is undoubtedly
significant for understanding this apparent
paradox. If gross morphological traits were
the only available evidence then the dol-
phin brain would be ranked along with the
human brain as a highly advanced brain.
Such traits as the ratio of neocortex t o lim-
bic cortex follow expected allometric pre-
dictions of a brain the size of a dolphin
brain. It is in fact even more convoluted
than might be expected from a terrestrial
brain of such size, but this can probably be
explained on the basis of its relatively thin-
ner cortex (compared to terrestrial mam-
mal brains of similar proportions—e.g.,
primate and human brains). Thus, with
respect to the production of initial cell pop-
ulations the dolphin brain probably shares
common mechanisms with all mammals.
But the production of cell populations and
the parcellation of those populations .into
distinct functional divisions and architec-
tonic fields occur independently at sepa-
rate developmental stages. The cortical
architectonic parcellation process occurs
subsequent to the production of the cor-
tical mantle. T h e allometric proportions
that will determine the proportion of iso-
cortex to limbic cortex and projection cor-
tex to association cortex are already estab-
lateral view lished, but the competitive interactions
which will subdivide and specialize these
FIG. 20. Drawing of the dolphin brain shown in sim-
plified form from above and from the side with an cortical targets have not begun at this stage.
indication of the topographic position of the different We must look to this latter process for a
sensory and motor projection fields. Although the clue to the peculiarities of the dolphin
areas depicted are presumed to be the primary pro- brain.
jection areas for these modalities, I prefer to reserve
judgement on this homological relationship. Assum-
T h e hypothesis I will suggest to explain
ing that the indicated areas are representative of the these architectonic peculiarities focuses on
proportion of neocortex occupied by primary areas the agranularity of dolphin cortex. T h e
it would appear that most of the dolphin isocortex is lack of layer IV granule cells throughout
composed of association areas. Limbic cortex is not the cortex of the dolphin brain is partic-
visible from the lateral view and is a relatively small
proportion of the total cerebral cortex as is appro- ularly remarkable because the origin of
priate for a mammalian brain of this size. Information granule cells is far more ancient than the
for this drawing is derived from Morgane et al. (1986a, divergence of Cetacea from the rest of the
eutherian stock. Despite the fact that small
brains are in general less "granularized"
(a feature that may in part be attributed to
the fact that the size difference between
granule cells and pyramidal cells in small
brains is relatively slight), even the appar-
ently primitive brain of the North Amer-
ican opossum Didelphis virginiana exhibits
a clearly defined and even subdifferen-
tiated layer IV that receives dense princi-
pal thalamic afferents (Johnson, 1988;
Walsh and Ebner, 1970), so the common
eutherian ancestor of cetaceans and other
eutherian mammals doubtless also pos-
sessed layer IV granule cells. Complete loss
of this cell type and cell layer must be con-
sidered a rare derived trait.
The absence of granule cells is of pri-
mary significance with respect to the pro-
cess of architectonic parcellation of corti-
cal areas. During development of cerebral
cortex, it is the competition between invad-
ing axons from the major thalamic nuclei
that is largely responsible for the specifi-
cation of topographic maps and establish-
ment ,of functional a n d architectonic
boundaries. As is well demonstrated by
studies of the formation of somatosensory
barrels in the rat and ocular dominance
columns in the cat and monkey, the ter-
minations of these critical projections and
the principal layers in which this compe-
tition takes place are layers III and IV,
corresponding to the distribution of gran-
ule cells in those layers (Jacobson, 1978).
Experimental destruction of these tha-
lamic afferents at an early stage (Rakic,
1988) or even elimination of peripheral
sensory information t o these afferents
(Woolsey and Wann, 1976) is capable of
profoundly altering the structure of the
resultant cortical map and even causing
functional-architectonic boundaries to be
displaced (Rakic, 1988).
Given the developmental importance of
this thalamofugal-granule cell relationship
for architectonic differentiation, it is clear
that elimination of this cell type and dis-
placement of many or all of the thalamo-
fugal projections to other layers and other
cellular targets in the developing cerebral
cortex of the dolphin brain is bound to
profoundly alter all features of its tangen-
tial and radial organization. T h e relatively
thick layer I likely results from the dis-
placement of thalamic afferents that lack
their "normal" primary affinity targets.
T h e presence of unusual "extroverted"
cells in layer II whose large dendrites reach
up into layer I may also be explainable in
this way. These cells are present in fetal
mammals brains but are eliminated early
in development and are the targets for
transient synapses during the early stages
of cortical differentiation (see discussion in
the previous section). T h e displacement of
axons lacking their principal target into
this layer at an early stage of development,
prior to the "normal" elimination of these
cells, may allow them t o persist by estab-
lishing permanent synapses with t h e
orphaned principal thalamic afferents.
Since columnar organization is established
by competitive exclusion processes within
layer IV and deep layer III, the lack of
clearly delineated columnar organization
undoubtedly results from the absence of
axonal competition in this layer. T h e lack
of clear architectonic boundaries and the
apparently clustered projection areas all
reflect this significant reduction of axonal
competition processes. However, the pres-
ence of differences in relative cell sizes in
different layers and differences in the den-
sity of pyramidal cells in different areas
(e.g., between somatosensory and motor
areas, Morgane et al., 1986a), that corre-
spond to similar differences in terrestrial
mammals, indicate that these features are
probably controlled by factors other than
thalamocortical connections, most proba-
bly their efferent terminations. T h e s e
hypothetical effects of granule cell elimi-
nation are depicted in Figure 2 1. Neuro-
logical mutant mice that completely lack
cerebral cortical granule cells should also
exhibit many of these same characteristics.
Study of these could serve as an informa-
tive test case, although because of the great
size difference many of the most unusual
features of the dolphin brain might not
express themselves so obviously in a mouse.
How and why cetacean brains lost their
granule cells is a mystery. It is a trait that
is probably shared by all cetaceans and so
was inherited from their common ancestor
subsequent to their divergence from ter-
restrial mammals. T h e r e is some trace of
 Monkey Dolphin

thalamic afferents thalamic afferents

FIG. 21. Granule cell degeneration hypothesis of the dolphin isocortex is depicted in comparison with the
pattern typical for terrestrial mammals represented by the monkey brain. In the diagram of monkey cortical
architecture the droplet shaped cells represent pyramidal cells the small spherical cells in middle layers
represent granule cells and other small interneurons and the ellipsoid cells represent small layer II cells. T h e
same shapes are used to depict cells in the diagram of the dolphin cortex with the exceptions that there are
no granule cells and some of the layer two cells are assumed to be embryologically retained "extraverted"
cells. Principal thalamic afferents that normally would target the granule cell populations in the cortical plate
are induced to establish alternative targets in the dolphin cortex in which granule cells are strangely absent.
These afferents without normal targets may establish synapses with embryonic cells in layer II that would
otherwise be eliminated after cortical plate formation in terrestrial mammals. These retained layer II extraver-
ted cells and the displaced thalamocortical axons cause layer I to be disproportionately thick and layer II to
be more densely packed than is observed in terrestrial mammal brains. Middle layers are also prevented from
normal competitive parcellation into columnar units, that otherwise would distinguish specialized koniocortical
areas. This suggests that dolphin cortical organization is neither conservative nor atavistic, but highly derived.

this degenerative process left because
immature dolphin brains do exhibit a tran-
sient but thin layer IV that disappears by
maturity (Garey and Leuba, 1986). It seems
unlikely that this loss can be rationalized
as an adaptation. Given the total break-
down of cortical differentiation processes
that resulted one would presume that this
is a costly mutation, although even in the
mutant Reeler mouse, with its totally dis-
rupted cortical architecture (but not lack-
ing granule cells), the cortex still functions
and allows for adequate perceptual and
motor functions. T h e fixation and survival
of this trait in cetaceans as opposed to any
other terrestrial lineage may be related to
their unusual and relatively complete adap-
tation to the aquatic habitat. T h e lack of
"granularized" competitors (e.g. , pin-
nipeds) in this niche until much later in
mammalian evolution may have been cru-
cial to the persistence of this trait. Consider
the significance of the regression of many
specific sensory and motor systems in these
species associated with their aquatic adap-
tation. They are anosmic, they have sig-
nificantly reduced visual requirements (and
in this regard are comparable to fossorial
species and echolocating bats with second-
arily reduced visual systems), and they
exhibit significant reduction of the distal
limbs, shoulder girdle and pelvis (which in
terrestrial vertebrates comprise the pre-
dominant afferent and efferent represen-
tation of the primary somatdsensory and
motor fields). Although many species have
highly developed echolocation systems, this
appears far more substantially represented
by collicular specialization (evidenced by
the immensely expanded and highly dif-
ferentiated inferior colliculus) than by cor-
tical specialization. All these regressive fea-
tures appear to coincidentally correlate
with the inability of the dolphin cortex to
architectonically differentiate.
In summary, this exception appears t o
prove the rule in a rather striking and
unambiguous way. T h e problems of deter-
mining whether the dolphin brain is con-
servative or advanced o r conservative-
advanced are irrelevant. T h e dolphin brain
is none of these. It is highly derived. These
problems that arose in the analysis at the
level of comparative morphology and com-
parative cytoarchitecture dissolve once we
approach the question from the perspec-
tive of developmental homologies.
Human brain evolution
Assumptions about human brain evolu-
tion are the ultimate source for many of
the misleading ideas that have haunted the
study of brain evolution, so it is fitting that
the exorcism of these ideas in this paper
should conclude with a discussion of the
uniqueness of human brain evolution. Two
unique characteristics of the human brain
stand out as central. T h e human brain is
roughly three times larger than would be
predicted for an anthropoid primate of
human body size, and human brains are
capable of acquiring an unprecedentedly
complex and flexible communication sys-
tem- language. T h e s e two facts a r e
undoubtedly linked.
Beginning with the issue of human brain
size, it is important t o find out if this
increased cell production follows trends
that are typical in other members of the
primate order. This can be ascertained by
comparing the relative sizes of the various
major structural divisions of the human
brain with predictions based on trends for
primates in general. Initial evidence that
there is a deviation from predicted allo-
metries comes from an examination of
studies that have used brain structure vol-
umes to construct possible phylogenetic
trees for primate ancestry. Two studies,
using largely similar data but different
methods that control for the effects of brain
size (Douglas a n d Marcellus, 1975;
Bauchot, 1982), have concluded that the
human brain is more similar to either one
of two New World monkeys' brains (woolly
monkeys in one case and capuchin mon-
keys in the other) and one Old World mon-
key's brain (Cercopithecus talapoin), than to
the brains of any other Old World mon-
keys and apes. It is probably not coinci-
dental that those primates most closely
linked with Homo by these studies also rep-
resent relatively encephalized primates.
When a structure by structure allometric
analysis is performed it appears that the
human brain diverges from primate trends
in a number of striking ways. Based on pre-
dictions from primate trends, the cerebral
cortex and cerebellar cortex of the human
brain are disproportionately large relative
to the diencephalon, corpus striaturn, brain
stem and spinal cord (Deacon, 1984,
1988b). This is depicted in Figure 22.
T h e production of neurons that consti-
tute cortical structures takes place well
before any axonal parcellation processes
begin, and therefore, as noted earlier, the
increase in cerebral cortex cannot be spe-
cific to any particular region of cortex. T h e
increase in radial dimensions of the cortical
germinal field and in the number of onto-
genetic columns that will differentiate out
of it must take place in the human brain
prior to neural production within the cor-
tex. T h e size disproportions between the
expanded neocortical target field, the rel-
atively unexpanded population of thala-
mofugal axons, and the relatively unex-
panded efferent subcortical targets of
cortical neurons must significantly bias
parcellation processes in all these areas
during subsequent stages of differentia-
tion. One effect of this is apparent in devia-
tions of relative cortical area dimensions
with respect to predictions based on the
allometry of these structures in other pri-
mates. Some cortical areas appear signifi-
cantly smaller than expected for a primate
brain this size and others significantly
larger. For example, the visual cortex
appears to scale appropriate to the size of
its peripheral input (the retina) and its
principal thalamic nucleus, but does not
occupy the proportion of cortex predicted
for a primate brain of this size. Its periph-
eral sources are constrained by the small
human body size with respect to the large
brain size. As a result they d o not scale to
 thalamocortical parcellation thalamocortical parcellation
process in a brain with typical process in the human brain with
primate cortical nuclear proportions disproportionately enlarged cortex
FIG. 22. Schematic diagram of large-scale human
brain structure disproportions and their effects on
axonal competition processes during human devel-
opment as compared to development in the absence
of these human disproportions. With respect to the
predictions based on other primate brains, human
cortical structures (including the entire cerebral and
cerebellar cortices) are larger than expected with
respect to brainstem, cerebellar, diencephalic and
telencephalic nuclear structures. Since the cell pro-
duction processes which determine the gross size of
these major morphogenetic fields are completed prior
to their parcellation into functional subdivisions it is
predicted that these disproportions will result in biased
displacement processes. T h e typical condition is
depicted by the three brains on the left. Brains A and
B represent the normal developmental stages of cor-
tical axonal parcellation of visual (gray cortex with
gray dashed arrows as afferents), somato-motor (black
with black arrows) and prefrontal (gray with solid gray
arrows) cortical fields in a large primate. T h e human
deviation from this is depicted by the three brains on
the right. Brains C and D represent the human devel-
opmental stages with constraint of visual and somatic
fields by their unexpanded peripheral afferents and
displacement by prefrontal afferents producing a much
enlarged adult prefrontal area.
the level that would otherwise be predicted
on the basis of brain size (a brain this big
would be expected only in a very very large
ape-the "King Kong" null hypothesis of
human brain evolution). T h e competitive
limits for these afferent systems are con-
strained by the size of the peripheral input.
Preliminary data suggest that this is prob-
ably also the case for auditory, somatic and
FIG. 23. A diagram of some of the relative propor-
tions ofcortical fields in the human brain as compared
to predictions based on typical anthropoid primate
trends. T h e percentages represent absolute devia-
tions from the predictions for a primate brain of human
size. Temporal, parietal, and motor area predictions
are based on too few data points to be significant, but
demonstrate a pattern that is consistent with the find-
ings for other areas and with the displacement
hypothesis. T h e depiction of peripheral structures
associated with different cortical areas is intended to
indicate that cortical areas with relatively direct rep-
resentation of peripheral sensory o r motor systems
are constrained by these afferents or efferents in their
competition for cortical representation. Figure taken
from Deacon (1990b).
motor areas as well as for visual areas (Dea-
con, 1984, 1988b; see Fig. 23).
T h e competitive limitation of these pro-
jection systems translates into a competi-
tive advantage for other areas not con-
strained by peripheral afferents, which
must inherit the cortical surface area that
is left unrecruited as a result. T h e pre-
frontal zone appears to be one major ben-
eficiary of this competitive imbalance. It is
estimated to be approximately twice the
size expected for a primate brain of human
proportion (and this translates to six times
the size predicted for a primate of human
FIG. 24. Some predicted connectional consequences of prefrontal enlargement are represented by brain A
(typical primate brain structure allometry) as compared to B (human cortical-nuclear disproportion). Dis-
placement theory suggests that the enlargement of the number of prefrontal efferents competing for midbrain
targets as compared to diencephalic efferents will bias competition in favor of prefrontal projections which
will displace both some diencephalic, limbic and intrinsic midbrain axons from their normal targets. This may
lead to the relative dominance of prefrontal outputs over limbic and diencephalic outputs in control of midbrain
and brainstem vocalization centers and motor circuits. This may be linked to adaptations associated with
language skills and the loss of many stereotypic vocalizations in human evolution.

body size; Deacon, 1 984, 1 988b). Prefron-
tal cortex is not a recipient of peripheral
inputs, but of inputs from other nonspe-
cific and polymodal systems of the mid-
brain and cerebral cortex. It is thus buff-
ered by being synaptically removed from
the cascading effects of peripheral bias that
affect other systems. It is probably not inci-
dental that Broca's area for speech is con-
tained within this enormously expanded
field.
This disproportionate prefrontal corti-
cal surface area is a secondary consequence
of the initial disproportion of the entire
embryonic cortex with respect to its sub-
cortical-peripheral connections. These ini-
tial disproportions biased axonal compe-
tition for cortical representation in favor
of cortical areas whose afferents were not
constrained by peripheral systems. But this
secondary disproportion of prefrontal areas
itself must have other tertiary biasing con-
sequences. Deacon (1990c) notes that effer-
ent projections of this system target limbic
cortical structures and a range of midbrain
structures. We can expect prefrontal pro-
jections to have a significant competitive
advantage over other afferents to these
areas during development (see Fig. 24). T h e
midbrain targets of prefrontal projections
also receive descending limbic cortical and
hypothalamic projections and intrinsic
projections from the central gray and retic-
ular formation. Many of these prefrontal
and limbic cortical targets turn out to play
major roles in vocal call production in pri-
mates. T h e displacement of "normal"
afferents of these areas and replacement
by a larger fraction of prefrontal axons may
have significantly altered their function.
Deacon (1990c) argues t h a t this may
account for the significantly reduced rep-
ertoire of stereotypic call types in humans,
as well as for the recruitment of some of
these systems by cortical areas capable of
supporting complex skilled motor pro-
gramming. T h e disproportions among
cortical areas and the relative reduction of
thalamocortical as opposed to corticocorti-
cal axons undoubtedly also played a role
in altering cortical functions, some of which
are related to the human language capac-
ity.
Human brain evolution cannot be con-
ceived in the terms of a conservative-pro-
gressive scheme of mammalian brain evo-
lution. Our brains are not at the pinnacle
of any evolutionary trend. Rather the
human brain is an unusual divergent case.
T h e extreme disproportion of human brain
size with respect t o the human body size
with respect to other primates and mam-
mals is only a surface manifestation of a
complex allometric reorganization within
the brain, and is unlikely itself to be the
crucial trait under selection in human evo-
lution. It is not just the increase in cortical
complexity nor the increased relative size
of the whole brain but the correlated reor-
ganization of underlying neural circuitry
that is probably most significant to human
uniqueness (see also Holloway, 1979).
Because the data that we possess con-
cerning the human brain are still neces-
sarily limited to morphological informa-
tion and notably do not include detailed
connectional data (due to the invasive
nature of present tracer techniques) direct
verification of these hypothetical reorgani-
zations will have to wait. However, our
understanding of the processes that must
underly development of a brain with the
allometric characteristics of the human
brain can be further augmented by con-
tinuing investigations of the relationships
between allometric and developmental
processes shared by all mammals. T h e
details of human brain evolution are still
largely obscure. T h e hypotheses presented
here are based on a massively incomplete
set of data. And yet the basic underlying
logic of allometric change and axonal dis-
placement processes during development
has provided an important new window
through which to view these data and an
indispensable guide to the gathering of
subsequent information about human brain
structures and human development.
Conclusions
Understanding the evolutionary ances-
try of the brain's organization is not merely
an academic exercise. It is crucial to the
study of its basic functional processes as
well. Few if any brain structures initially
evolved their present form precisely for
the purposes they now serve, and many
current brain systems may be the result of
lucky syntheses of previously separated cir-
cuits o r else the result of fortuitous degen-
erative events. Because the brain was not
predesigned for its current adaptations the
strategies employed in its operation will not
likely yield to a purely functional physio-
logical analysis. More importantly, a n
understanding of the predispositions and
constraints inherited from past adaptations
and developmental strategies can lead us
beyond a merely superficial understanding
of function to appreciate some of the
deeper fundamental organizing principles
shared by all features of the brain.
Neither the study of mammalian brain
evolution nor even the study of human
brain evolution is limited to merely theo-
retical exploration. We currently have
access to experimental tools that are ade-
quate to the task of analyzing the neural
developmental processes that underly, can-
alize and constrain brain evolution, and are
capable of gathering the sorts of compar-
ative anatomical evidence that can eluci-
date the variety of ways these processes
have been expressed in evolution. This is
an invaluable complement to other areas
of the neurosciences that are rapidly build-
ing a database of comparative physiologi-
cal and behavioral information. O u r fail-
ure to immediately grasp the significance
of these data for brain evolution has largely
been the fault of the unrecognized influ-
ence of some very old notions about evo-
lution, the nature of mental processes;.and
the place of humans in some cognitive scala
naturae.
T h e displacement hypothesis has led me
to propose four highly speculative. expla-
nations of some major problems in mam-
malian brain evolution. But displacement
theory does not depend on the correctness
of these particular interpretations. In fact,
it provides means to falsify them if they re
incorrect. T h e theory clearly requires t a t
patterns of brain evolution be ex p lained in
terms of the biasing of competitive devel-
opmental mechanisms a n d suggests
numerous possible candidates for' biasing
influences that are likely involved: includ-
ing (in order of likely importance) allo-
metric relationships, cell death, hetero-
chronous changes in maturational events
and changes in molecular affinities between
cells and axons. T h e correlate's of displace-
ment processes that are postulated t o
account for an evolutionary change must
be physically exhibited by the develop-
mental processes that construct living
brains. If they are not observed then a dis-
placement explanation must be rejected o r
modified. T h e examples presented in this
paper have been chosen not as test cases
for the theory, but rather as exemplars of
the range of possible displacement effects
and their consequences. Whatever the ulti-
mate applicability of these individual
accounts, the general approach should at
least serve to focus attention on a number
of previously unappreciated correlations
between biasing influences in neural devel-
opment and phylogenetic differences in
adult brain structure. T o the extent that
these biases are altered in brains of differ-
ent sizes or can be manipulated by exper-
imental modification of neural population
size or developmental timing, it should be
possible to develop explicit experimental
models of many evolutionary changes in
brain structure. T h e ultimate test of a gen-
eral theory is not just whether or not it can
account for the data that are already
known, but also how useful it is in leading
to new experimental approaches and new
insights concerning the underlying hidden
logic of the systems we wish to understand.
ACKNOWLEDGEMENTS
I would like to thank Joseph Marcus for
his comments and editorial assistance in
preparing this manuscript.
REFERENCES
Abbie, A. A. 1940. Cortical lamination in the Mono-
tremata. J. Comp. Neurol. 72:428-467.
Alberch, P. 1982. Developmental constraints in evo-
lutionary processes. In T. Bonner (ed.), Evolution
and development, pp. 313-332. Springer-Verlag,
Berlin.
Alexander, G. E. and P. L. Strick. 1986. Parallel
organization of functionally segregated circuits
linking basal ganglia and cortex. Ann. Rev. Neu-
rosci. 9:357-38 1 .
Alley, K. E. 1974. Morphogenesis of the trigeminal
mesencephalic nucleus in the hamster: Cytogene-
sis and neurone death. J. Exp. Morph. 31:99-
121.
Allman, J. M. 1982. Reconstructing the evolution of
the brain in primates through the use of com-
parative neurophysiological data. In E. Arm-
strong and D. Falk (eds.), Primate brain evolution,
pp. 13-28. Plenum Press, New York.
Allman, J. M. 1990. Evolution of neocortex. Cerebral
cortex, Vol. 8, Evolution and comparative anatomy of
cerebral cortex. Plenum Press, New York. (In press)
Ariëns Kappers, C. U., C. G. Huber, and E. C. Crosby.
1936. The comparative anatomy of the nervous system
of vertebrates including man, Vol. III. MacMillan,
New York.
Armstrong, E. 1979. A quantitative comparison of
the hominoid thalamus. I: Specific sensory relay
nuclei. Am. J. Phys. Anthrop. 51:365-382.
Armstrong, E. 1983. Relative brain size and metab-
olism in mammals. Science 220: 1302-1 304.
Armstrong, E. 1985. Allometric considerations of
the adult mammalian brain, with special emphasis
on primates. In W. Jungers (ed.), Size and scaling
in primate biology, pp. 115-146. Plenum Press,
New York.
Atchley, W. R. 1984. T h e effect of selection on brain
and body size association in rats. Genet. Res. 43:
289-298.
Baldwin, J. M. 1985. Mental development in the child
and the race. Macmillan, New York.
Barbus, H. 1986. Pattern in the laminar origin of
corticocortical connections. J. Comp. Neurol. 252:
41 5-422.
Barbus, H. and D. N. Pandya. 1982. Cytoarchitec-
ture and intrinsic connections of the prefrontal
cortex of the rhesus monkey. Soc. Neurosci. Abstr.
8:933.
Barbus, H. and D. N . Pandya. 1987. Architecture
and frontal cortical connections of the premotor
cortex (area 6) in the rhesus monkey. J . Comp.
Neurol. 256:211-228.
Bauchot, R. 1982. Brain organization and taxonomic
relationships in Insectivora and Primates. In E.
Armstrong and D. Falk (eds.), Primate brain evo-
lution, pp. 163-175. Plenum Press, New York.
Bauchot, R., J. M. Ridet, and M. L. Bauchot. 1979.
Encephalization and evolutionary level in aquatic
vertebrates. Vie Milieu Biol. Mar. Oceanogr. 197:
253-266.
Bishop, G. H. 1959. T h e relation between nerve fiber
size and sensory modality: Phylogenetic impli-
cations of the afferent innervation of cortex. J.
Nerv. Ment. Dis. 128:84-114.
Bohringer, R. C. and M. J. Rowe. 1977. T h e orga-
nization of the sensory and motor areas of cere-
bral cortex in the platypus (Ornithorhynchus ana-
tinus). J . Comp. Neurol. 174:1-14.
Bonin, G. von. 1937. Brain-weight and body-weight
in mammals. J. Gen. Psych. 16:379-389.
Bonin, G. von and P. Bailey. 1961. Patterns of cere-
bral isocortex. Primatologia 11/2, Lief. 10:1-42.
Brodmann, K. 1909. Vergleichende Lokalisationslehre
der Grosshirnrinde in ihren prinzipien dargestellt auf
Grand der Zellenbaus. A. Barth, Leipzig.
Brown, J. W. 1977. Mind, brain, and consciousness.
Academic Press, New York.
Brown, J. W. 1988. The life of the mind. Erlbaum,
Hillsdale, New Jersey.
Bullier, J., H. Kennedy, and W. Salinger. 1984.
Branching and laminar origin of projections
between visual cortical areas in the cat. J. Comp.
Neurol. 228:329-341.
Calford, M. B., M. L. Graydon, M. F. Huerta, J. H.
Kass, and J. D. Pettigrew. 1985. A variant of the
mammalian somatotopic map in a bat. Nature
3 13:477-480.
Campbell, A. 1905. Histological studies on the localiza-
tion of cerebral function. Cambridge University
Press, Cambridge.
Campbell, C. B. G. 1982. Some questions and prob-
lems related to homology. In E. Armstrong and
 D. Falk (eds.), Primate brain evolution, pp. 1-1 1.
Plenum Press, New York.
Campbell, C. B. G. 1988. Primate survivors and neo-
cortical evolution. Behav. Brain Sci. 11:90-91.
Campbell, C. B. G. and W. Hodos. 1970. T h e con-
cept of homology and the evolution of the ner-
vous system. Brain Behav. Evol. 3:353-367.
Campos, G. B. and W. I. Welker. 1976. Comparisons
between brains of a large and small hystrico-
morph rodent: Capybara, Hydrochoerus and guinea
pig, Cavia (neocortical projection regions and
measurements of brain subdivisions). Brain Behav.
Evol. 13:243-306.
Cartmill, M. 1972. Arboreal adaptations and the ori-
gin of the order Primates. In R. H. Tuttle (ed.),
The functional and evolutionary biology of primates,
pp. 97-122. Aldine-Atherton, Chicago.
Cartmill, M. 1974. Rethinking primate origins. Sci-
ence 184:433-436.
Caviness, V. S., Jr. and D. O. Frost. 1980. Tangential
organization of thalamic projections to the neo-
cortex in the mouse. J. Comp. Neurol. 194:335-
368.
Chomsky, N. 1972. Language and mind. Harcourt
Brace Javonovich, New York.
Count, E. W. 1947. Brain and body weight in man:
Their antecedents in growth and evolution. Ann.
N.Y. Acad. Sci. 46:993-1122.
Cowan, W. M. 1973. Neuronal death as a regulative
mechanism in the control of cell number in the
nervous system. I n M. Rockstein (ed.), Develop-
ment and aging i n the nervous system, pp. 119-141.
Academic Press, New York.
Cowan, W. M., J. W. Fawcett, D. D. M. O'Leary, and
B. B. Stanfield. 1984. Regressive events in neu-
rogenesis. Science 255: 1258-1265.
Cranach, M. von. 1976. Methods of inference from ani-
mal to human behavior. Aldine, Chicago.
Crosby, E. C. 19 17. T h e forebrain of Alligator mis-
sissippiensis. J. Comp. Neurol. 27:325-403.
Dart, R. 1934. T h e dual structure of the neopallium:
Its history and significance. J. Anat. 69:3-19.
Deacon, T. W. 1984. Connections of the inferior
periarcuate area in the brain of Macaca fascicu-
laris. An experimental and comparative investi-
gation of language circuitry and its evolution.
Ph.D. Diss., Harvard University, Cambridge,
Massachusetts.
Deacon, T. W. 1985. "Counter-current flow" of cor-
tico-cortical information processing through the
laminar segregation of reciprocal connections.
Soc. Neurosci. Abstr. 1 1:203.1
Deacon, T. W. 1988a. Cortical and midbrain con-
nections of the intermediodorsal nucleus in the
rat. Soc. Neurosci. Abstr. 14:328.1.
Deacon. T. W. 1988b. Human brain evolution: II.
Embryology and brain allometry. I n H. Jerison
and I. Jerison (eds.), Intelligence and evolutionary
biology, pp. 383-41 5. Springer-Verlag, Berlin.
Deacon, T. W. 1989. Holism and associationism in
neuropsychology: An anatomical synthesis. In E.
Perecman (ed.), Integrating theory and practice in
clinical neuropsychology, pp. 1-47. Erlbaum, Hills-
dale, New Jersey.
Deacon, T. W. 1990a. Fallacies of progression in
theories of brains size evolution. Int. J. Primatol.
11: 193-236.
Deacon, T. W. 1990b. Problems of ontogeny and
phylogeny in brain size evolution. lnt. J. Prima-
tol. 11:237-282.
Deacon, T. W. 1990c. T h e neural circuitry under-
lying primate calls and human language. Human
Evol. (In press)
Deacon, T. W., A. Sokoloff, and D. Wecht. 1987.
Circular organization of connections linking mid-
brain areas, sections of the mediodorsal thala-
mus, and prefrontal areas in the rat. Soc. Neu-
rosci. Abstr. 13:304.9.
Deacon, T. W., D.-W. Wang, and A. Carpenter.
1989. Similarities and differences in the laminar
organization of corticocortical connections in rat
as compared t o monkey. Soc. Neurosci. Abstr.
15:114.10.
Diamond, I. T. 1979. T h e subdivisions of the neo-
cortex: A proposal to revise the traditional view
of sensory, motor and association areas. I n J.
Sprague and A. Epstein (eds.), Progress i n psycho-
biology and physiological psychology, Vol. 8. Aca-
demic Press, New York.
Diamond, I. T. 1982. T h e functional significance of
architectonic divisions of the cortex, Lashley's
criticism of the traditional view. I n J. Orbach
(ed.), Neuropsychology after Lashley, pp. 101-1 35.
Erlbaum, Hillsdale, New Jersey.
Diamond, I. T . , D. Fitzpatrick, and J. M. Sprague.
1985. T h e extrastriate visual cortex. A historical
approach to the relation between the "visuo-sen-
sory" and "visuo-psychic" areas. In A. Peters and
E. G. Jones (eds.), Cerebral cortex, Vol. 4; Associ-
ation and auditory cortices, pp. 63-87. Plenum Press,
New York.
Diamond, I. T. and W. C. Hall. 1969. Evolution of
neocortex. Science 164:251-262.
Dom, R., G. F. Martin, B. L. Fisher, A. M. Fisher,
and J. K. Harting. 197 1. T h e motor cortex and
corticospinal tract of the armadillo (Dasypus no-
vemcincus). J. Neurol. Sci. 14:225-236.
Donoghue, J. P., K. L. Kerman, and F. F. Ebner.
1979. Evidence for two organizational plans
within the somatic sensory-motor cortex. of the
rat. J. Comp. Neurol. 183:647-664.
Douglas, R. J. and D. Marcellus. 1975. T h e ascent
of man: Deductions based on a multivariate anal-
ysis of the brain. Brain Behav. Evol. 11:179-2 13.
Dubois, E. 1913. O n the relation between quantity
of brain and the size of the body in vertebrates.
Verh. Kon. Akad. Wetenschappen Amsterdam
16:647.
Ebbesson, S. O. 1980. T h e parcellation theory and
its relation t o interspecific variability in brain
organization, evolutionary a n d o n t o g e n e t i c
development, and neuronal plasticity. Cell Tissue
Res. 2 13: 179-2 12.
Ebbesson, S. O. 1984. Evolution and ontogeny of
neural circuits. Behav. Brain Sci. 7:32 1-366.
Edelman, G. M. 1987. Neural Darwinism. Basic Books,
New York.
Elliot-Smith, G. 1910. Some problems related to the
 evolution of the brain. Lancet 1:1-6, 147-153,
22 1-227.
Elliot-Smith, G. 1919. A preliminary note o n the
morphology of the corpus striatum and the origin
of the neopallium. J. Anat. 53:271-291.
Falk, D. 1980. A reanalysis of the South African
australopithecine natural endocast. Am. J. Phys.
Anthrop. 53:525-539.
Falk, D. 1983. Cerebral cortices of East African early
hominids. Science 221: 1072- 1074.
Falk, D. 1989. Ape-like endocast of "Ape-man"
Taung. Am. J. Phys. Anthrop. 80:335-339.
Fasolo, A. and G. Malacarne. 1988. Comparing the
structure, of brains: Implications for behavioral
homologies. In H. Jerison and I. Jerison (ed.),
Intelligence and evolutionary biology, pp. 119-142.
Springer-Verlag, Berlin.
Filimonof, I. N. 1949. Comparative anatomy of the cere-
bral cortex of mammals. paleocortex, a rchicortex, and
intermediate cortex. [Trans. by V. Dukhoff, 1965].
Joint Pub. Res. Service, Office of Sci. Inf. Dept.
of Interior, Washington, D.C.
Filler; A. 1986. Axial character seriation in mam-
mals. An historical exploration of the origin,
development, use and current collapse of the
homology paradigm. Ph.D. Diss., Harvard Uni-
versity, Cambridge, Massachusetts.
Finlay, B. L. and M. Slattery. 1983. Local differences
in early cell death in neocortex predict adult local
specializations. Science 2 19:1349-1 351.
Finlay, B.L., K. C. Wikler, and D. R. Sengelaub.
1987. Regressive events in brain development
and scenarios for vertebrate brain evolution. Brain
Behav. Evol. 30: 102-1 17.
Flechsig, P. 1900. Über Projections und Associations
Zentren des menschlichen Gehirns. [On projec-
tion and association centers of the human brain.]
Neurologie Zentralblatt 19.
Flechsig, P. 190 1 . Developmental (myelogenetic)
localization of the cerebral cortex in the human
subject. Lancet 2:1027-1029.
Friedman, D. P., L. G. Bachevalier, L. G. Unger-
lieder, and M. Mishkin. 1987. Widespread tha-
lamic projections to layer I of primate cortex.
Soc. Neurosci. Abstr. 13:73.17.
Frost, D. and V. Caviness, Jr. 1980. Radial organi-
zation of thalamocortical projections. J. Comp.
Neurol. 194:369-394.
Frost, D. O. and C. Metin. 1985. Induction of func-
tional retinal projections to the somatosensory
system. Nature 3 17: 162.
Fuller, J. L. 1979. Fuller BWS lines: History and
results. I n M. E. Hahn, C. Jensen, and B. C. Dudek
(eds.), Development and evolution of brain size, pp.
190-204. Academic Press, New York.
Galaburda, A. M. and D. N. Pandya. 1983. T h e
intrinsic architectonic and connectional organi-
zation of the superior temporal region of the
rhesus monkeys. J. Comp. Neurol. 22 1:169-184.
Gardner, H. 1983. Frames of mind: The theory of mul-
tiple intelligences. Basic Books, New York.
Garey, L. J. and G. Leuba. 1986. A quantitative study
of neuronal and glial numerical density in the
visual cortex of the bottlenose dolphin: Evidence
for a specialized subarea and changes with age.
J. Comp. Neurol. 247:491-496.
Gaskin, D. E. 1982. The ecology of whales and dolphins.
Heineman, New York.
Geschwind, N. 1964. Development of brain and evo-
lution of language. Georgetown Univ. Monogr.
Ser. Language Linguistics 17: 155-170.
Ghiselin, M. T. 1976. T h e nomenclature of corre-
spondence: A new look at "homology" and "anal-
ogy." In R. B. Masterton, W. M. Hodos, and H.
Jerison (eds.), Evolution, brain and behavior: Per-
sistent problems, pp. 129-142. Erlbaum, New York.
Glezer, I. I., M. S. Jacobs, and P. J. Morgane. 1988.
Implications of the "initial brain" concept for
brain evolution in Cetacea. Behav. Brain Sci. 1 1 :
75-116.
Goldowitz, D. 1987. Cell partitioning and mixing in
the formation of the CNS: Analysis of the cortical
somatosensory barrels in chimeric mice. Devel.
Brain Res. 35:1-9.
Gould, S. J. 1966. Allometry and size in ontogeny
and phylogeny. Biol. Rev. Camb. Phil. Soc. 41:
587-640.
Gould, S. J. 1975. Allometry in primates with empha-
sis of scaling and the evolution of the brain. Contr.
Primatol. 5:244-292.
Gould, S. J. 1977. Ontogeny and phylogeny. Harvard
University Press, Cambridge, Massachusetts.
Gould, S. J. 1981. The mismeasure of man. George J.
McLeod Limited, Toronto.
Gregory, W. K. 1935. Replication in evolution. Q.
Rev. Biol. 10:272-290.
Guillery, R. W. 1974. Visual pathways in albinos. Sci.
Amer. 230:44-54.
Haight, J. R. and L. Neylon. 1978. T h e organization
of neocortical projections from the ventropos-
terior thalamic complex in the marsupial brush-
tailed opossum, Trichosurus vulpecula, a horserad-
ish peroxidase study. J. Anat. 126:459-485.
Haight, J. R. and L. Neylon. 1979. T h e organization
of neocortical projections from the ventrolateral
thalamic nucleus in the brush-tailed possum,
Trichosurus vulpecula, and the problem of motor
and somatic sensory convergence within the
mammalian brain. J. Anat. 129:673-694.
Haug, H. 1987. Brain sizes, surfaces, and neuronal
sizes of the cortex cerebri: A stereological inves-
tigation of man and his variability and a com-
parison with some mammals (primates, whales,
marsupials, insectivores, and one elephant). Am.
J. Anat. 180:126-1 42.
Herkenham, M. 1980. Laminar organization of tha-
lamic projections to the rat neocortex. Science
207:532-534.
Herman, L. M. (ed.) 1980. Cetacean behavior: Mech-
anisms and functions. Wiley, New York.
Herrick, C. J. 1920. A sketch of the origin of the
cerebral hemispheres. J. Comp. Neurol. 32:429-
454.
Hodos. W. 1988. Comparative neuroanatomy and
the evolution of intelligence. I n H. Jerison and
I. Jerison (eds.), Intelligence and evolutionary biol-
ogy pp. 93-108. Springer-Verlag, Berlin.
Holloway, R. L. 1979. Brain size, allometry, and
reorganization: Toward a synthesis. In M. Hahn,
C. Jensen, and B. Dudek (eds.), Development and
evolution of brain size, pp. 59-88. Academic Press,
New York.
Holloway, R. L. 1981. Revisiting the South African
Taung australopithecine endocast: T h e position
of the lunate sulcus as determined bv the ste-
reoplotting technique. Am. J. Phys. Anthrop. 56:
43-58.
Holloway, R. L. 1984. T h e Taung endocast and the
lunate sulcus: A rejection of the hypothesis of its
anterior position. Am. J. Phys. Anthro. 1984:
285-287.
Holloway, R. L. 1985. T h e past, present, and future
significance of the lunate sulcus in early hominid
evolution. In P. V. Tobias (ed.), Hominid evolution:
Past, present and future, pp. 47-62. Alan R. Liss,
New York.
Holloway, R. L. 1988. Some additional morpholog-
ical and metrical observation on Pan brain casts
and their relevance to the Taung endocast. Am.
J. Phys. Anthro. 77:27-33.
Hopf, A. 1965. Volumetrische Untersuchunger sur
vergleichenden Anatomie des Thalamus. J. Hir-
forsch. 8:25-38.
Jacobs, M. S., A. M. Galaburda, W. L. McFarland,
and P. J. Morgane. 1984. T h e insular formation
of the dolphin brain. Quantitative cytoarchitec-
tonic studies of the insular component of the lim-
bic lobe. J. Comp. Neurol. 225:396-432.
Jacobs, M. S., W. L. McFarland, and P. J. Morgane.
1979. T h e anatomy of the brain of the bottlenose
dolphin (Tursiops truncatus). Rhinic lobe (rhinen-
cephalon): I. T h e archicortex. Brain Res. Bull.
4(Suppl. 1):1-108.
Jacobs, M. S., P. J. Morgane, and W. L. McFarland.
197 1. T h e anatomy of the brain of the bottlenose
dolphin (Tursiops truncatus). Rhinic lobe (rhinen-
cephalon): I. T h e paleocortex. J. Comp. Neurol.
141:205-272.
Jacobson, J. 1978. Developmental neurobiology, 2nd ed.
Holt, Rhinehart, and Winston, New York.
Jarvis, M. J. and G. Ettlinger. 1977. Cross-modal
recognition in chimpanzees and monkeys. Neu-
ropsychologia 15:499-506.
Jerison, H. J. 1973. Evolution of the brain and intelli-
gence. Academic Press, New York.
Jouandet, M., M. Tramo, D. Herron, A. Hermann,
W. Loftus, J. Bazell, and M. Gazzaniga. 1989.
Brainprints: Computer-generated two-dimen-
sional maps of the human cerebral cortex in vivo.
J. Cog. Neurosci. 1:88-117.
Johnson, J. I. 1988. Whose brain is initial-like? Behav.
Brain Sci. 1 1:96.
Johnston, J. B. 1906. The nervous system of vertebrates.
P. Blackiston's Son and Co., Philadelphia.
Jones, E. G., J. D. Coulter, and S. H. C. Hendry. 1978.
Intracortical connectivity of architectonic fields
in the somatic sensory, motor and parietal cortex
of monkeys. J. Comp. Neurol. 18 1:291-348.
Kaas, J. H. 1987. T h e organization and evolution of
neocortex. In S. P. Wise (ed.), Higher brain func-
tions. Recent explorations of the brain's emergent prop-
erties, pp. 347-378. John Wiley & Sons, New York.
Kaas, J. H. 1989. Why does the brain have so many
visual areas? J. Cog. Neurosci. 1:12 1-135.
Kaas, J . H. and R. W. Guillery. 1973. T h e transfer
of abnormal visual field representations from the
dorsal lateral geniculate nucleus to the visual cor-
tex in Siamese cats. Brain Res. 59:61-95.
Kaas, J. H., W. C. Hall, and I. T. Diamond. 1970.
Cortical visual areas I and II in the hedgehog:
Relation between evoked potential maps and
architectonic divisions. J. Neurophys. 33:595-
615.
Kaas, J. H. and M. F. Huerta.1988. Subcortical visual
system of primates. In H. D. Steklis (ed.), Com-
parative primate biology, Vol. 4: Neurosciences, pp.
327-391. Alan R. Liss, New York.
Karten, H. J. 1969. T h e organization of the avian
telencephalon and some speculations o n the phy-
logeny of the amniote telencephalon. Ann. N.Y.
Acad. Sci. 167: 164-179.
Karten, H. J. and T. Shimuzu. 1989. T h e origins of
neocortex: Connections and lamination as dis-
tinct events in evolution. J. Cog. Neurosci. 1:29 1-
30 1.
Kaplan, S. R. and G. E. Goslow. 1989. Neuromus-
cular organization of the pectoralis (pars thora-
cicus) of the pigeon (Columba livia): Implications
for motor control. Anat. Rec. 224:426-430.
Katz, M. 1982. Ontogenetic mechanisms: T h e mid-
dle ground of evolution. In T. Bonner (ed.), Evo-
lution and development, pp. 207-2 12. Springer-
Verlag, Berlin.
Kirsch, J. A. W., A. I. Johnson, and R. C. Switzer.
1983. Phylogeny through brain traits: The mam-
malian family tree. Brain Behav. Evol. 22:70-74.
Kruska, D. 1987. How fast can total brain size change
in mammals? J. Hirnforsch. 28:59-70.
Kuljis, R. O. and P. Rakic. 1988. Segregation of neu-
ropeptide Y-containing neurons outside cyto-
chrome oxidase puffs in the monkey develops in
the absence of visual input. Soc. Neurosci. Abstr.
14:243.5.
Le Gros Clark, W. E. 197 1. Antecedents of man. Edin-
burgh University Press, Edinburgh.
Le Gros Clark, W. and D. Northfield. 1939. The
cortical projection of the pulvinar in the macaque
monkey. Brain 60: 126-1 42.
Lende, R. A. 1963. Cerebral cortex: A sensorymotor
amalgam in the Marsupialia. Science 141:730-
732. . ,
Lende, R. A. 1969. A comparative appoach to neo-
cortex: Localization in monotremes, marsupials
and insectivores. Ann. N.Y. Acad. Sci. 167:262-
275.
Lieberman, P. 1984. The biology and evolution of lan-
guage. Harvard University Press, Cambridge,
Massachusetts.
Livingstone, R. and D. Huebel. 1988. Segregation
of form, color, movement, and depth: Anatomy,
physiology, and preception. Science 240:740-749.
Luria, A. R. 1980. Higher cotical functions in man
2nd ed. (English trans.). Basic Books, New York.
MacLean, P. D. 1970. T h e triune brain, emotion and
scientific basis. In F. O. Schmitt (ed.), The neu-
rosciences: Second study program. Rockefeller Uni-
versity Press, New York.
MacLean, P. D. 1973. A triune concept of the brain
and behavior. In T. J. Boag and D. Campbell
(eds.), A triune concept of the brain and behavior.
University of Toronto Press, Toronto.
MacPhail, E. 1982. Brain and intelligence in vertebrates.
Clarendon Press, Oxford.
Magalhães-Castro, B. and P. E. S. Saraiva. 1971. Sen-
sory and motor representation in the cerebral
cortex of the marsupial Didelphis azarae azarae.
Brain Res. 34:291-299.
Marin-Padilla, M. 1978. Dual origin of the mam-
malian neocortex and evolution of the cortical
plate. Anat. Embryol. 152: 109-156.
Martin, R. D. 1973. Comparative anatomy and pri-
mate systematics. Symp. Zool. Soc. London 33:
301-337.
Martin, R. D. 1981. Relative brain size and basal
metabolic rate in terrestrial vertebrates. Nature
293:57-60.
Martin, R. D. 1983. Human brain evolution in an
ecological context. Fifty-second James Arthur
Lecture on the evolution of the human brain.
Am. Mus. Nat. Hist., New York.
Maunsell, J. H. R. and D. C. Van Essen. 1983. T h e
connections of the middle temporal visual area
(MT) and their relationship to a cortical hier-
archy in the macaque monkey. J. Neurosci. 3:
2563-2586.
Meculam, M.-M., G. W. Van Hoesen, D. N. Pandya,
and N. Geschwind. 1977. Limbic and sensory
connections of the inferior parietal lobule (area
PG) in the rhesus monkey: A study with a new
method for horseradish peroxidase histochem-
istry. Brain Res. 136:393-414.
Mishkin, M. and T. Appenzeller. 1987. The anatomy
of memory. Sci. Amer. 256:80-89.
Morgane, P. J., I. I. Glezer, and M. S. Jacobs. 1990.
Comparative and evolutionary anatomy of visual
cortex of the dolphin. In E. G. Jones and A. Peters
(eds.), Cerebral cortex, Vol. 8. Evolution and com-
parative anatomy of cerebral cortex. Plenum Press,
New York. (In press)
Morgane, P. J. and M. S. Jacobs. 1972. Comparative
anatomy of the cetacean nervous system. In R. J.
Harrison (eds.), Functional anatomy of marine mam-
mals, pp. 117-244. Academic Press, London.
Morgane, P. J., M. S. Jacobs, and A. Galaburda. 1985.
Conservative features of neocortical evolution in
dolphin brain. Brain Behav. Evol. 26:176-184.
Morgane, P. J., M. S. Jacobs, and A. Galaburda.
1986a. Evolutionary aspects of cortical organi-
zation in the dolphin brain. In R. J. Harrison and
M. Bryden (eds.), Research on dolphins, pp. 71-98.
Oxford University Press, Oxford.
Morgane, P. J., M. S. Jacobs, and A. Galaburda.
1986b. Evolutionary morphology of the dolphin
brain. In R. Schusterman, F. Wood, and J. Thomas
(eds.), Dolphin cognition and behavior: A comparative
approach, pp. 5-29. Erlbaum, Hillsdale, New Jer-
sey.
Morgane, P. J., W. L. McFarland, and M. S. Jacobs.
1982. T h e limbic lobe of the dolphin brain: A
quantitative cytoarchitectonic study. J. Hirn-
forsch. 23:465-552.
Nauta, W. J. H. and H. J. Karten. 1970. A general
profile of the vertebrate brain with sidelights on
the ancestry of the cerebral cortex. In F. O.
Schmidt (ed.), The neurosciences: Second study pro-
gram. Rockefeller Press, New York.
Northcutt, R. G. 1981. Evolution of the telenceph-
alon in nonmammals. Ann. Rev. Neurosci. 4:301-
350.
Northcutt, R. G. 1984. Evolution of the vertebrate
central nervous system: Patterns and processes.
Amer. Zool. 24:70 1-7 16.
O'Leary, D. D. M. 1989. Do cortical areas emerge
from a protocortex? Trends Neurosci. 12:400-
406.
O'Leary, D. D. M. and B. B. Stanfield. 1989. Selec-
tive elimination of axons extended by developing
cortical neurons is dependent o n regional locale
experiments utilizing fetal cortical transplants. J.
Neurosci. 9:2230-2246.
Optican, L. M. and B. J. Richmond. 1987. Temporal
encoding of two-dimensional patterns by single
units in primate inferior temporal cortex. III.
Information theoretic analysis. J. Neurophysiol.
57:162-178.
Pandya, D. and E. Yeterian. 1985. Architecture and
connections of cortical association areas. In A.
Peters and E. G. Jones (eds.), Cerebral cortex, Vol.
4, Association and auditory cortices, pp. 3-61. Ple-
num Press, New York.
Passingham, R. E. 1975. Changes in the size and
organisation of the brain in man and his ances-
tors. Brain Behav. Evol. 11:73-90.
Passingham, R. E. 198 1. Broca's area and the origins
of human vocal skill. Phil. Trans. R. Soc. London,
B 292: 167-175.
Primrose, D. and P. Strick. 1985. T h e organization
of interconnections between the premotor areas
of the primate frontal lobe and the arm area of
primary motor cortex. Soc. Neurosci. Abstr. 11:
127.4.
Purves, D. 1988. Body and brain: A trophic theory of
neural connections. Harvard University Press,
Cambridge, Massachusetts.
Purves, D. and J. W. Lichtman. 1980. Elimination
of synapses in the developing nervous system.
Science 2 10: 153-157.
Purves, D. and J. W. Lichtman. 1985. Principles of
neural development. Sinauer, New York.
Rakic, P. 1988. Specification of cerebral cortical areas.
Science 24 1: 170-1 76.
Rausell, E. and C. Avendano. 1985. Thalamocortical
neurons projecting to superficial and to deep lay-
ers in parietal, frontal and prefrontal regions in
the cat. Brain Res. 347:159-165.
Reynolds, P. C. 1976. Language and skilled activity.
In S. R. Harnad, H. D. Steklis, and J. Lancaster
(eds.), Origins and evolution of language and speech.
Ann. N.Y. Acad. Sci. 280:1-914.
Riska, B., W. R. Atchley, and J. J. Rutledge. 1984.
A genetic analysis of targeted growth in mice.
Genetics 107:79-101.
Rockel, A.J., R. W. Hiorns, and T. P. S. Powell. 1980.
T h e basic uniformity in structure of the neocor-
tex. Brain 103:221.
Rockland, K. and D. N. Pandya. 1979. Laminar
 origins and terminations of connections of the
occipital lobe in the rhesus monkey. Brain Res.
179:3-20.
Roderick, T. H., R. E. Wimer, and C. C. Wimer.
1976. Genetic manipulation of neuroanatomical
traits. I n L. Petrinovich and J. L. McGaugh (eds.),
Knowing, thinking nnd believing, pp. 143-178. Ple-
num Press, New York.
Rose, J. and C. Woolsey. 1949. Organization of the
mammalian thalamus and its relation to the cere-
bral cortex. Electroenceph. Clin. Neurophysiol.
1:391-404.
Royce, G. J., G. F. Martin, and R. N. Dom. 1975.
Functional organization and cortical architecture
in the nine-banded armadillo (Dasjpus novemcinc-
tus). J . Comp. Neurol. 164:495-522.
Russell, E. S. 19 16. Form and function. John Murray,
London.
Sacher, G. A. 1970. Allometric and factorial analysis
of brain structure in insectivores and primates.
I n C. R. Novack and W. Montagna (eds.), The
primate brain: Advances in primatology, pp. 245-
287. Appleton Century Crofts, New York.
Sacher, G. A. and E. F. Staffeldt. 1974. Relation of
gestation time to brainweight for placental mam-
mals: Implications for the theory of vertebrate
growth. Am. Nat. 108:593-615.
Sanides, F. 1969. Comparative architectonics of the
neocortex of mammals and their evolutionary
interpretation. Ann. N.Y. Acad. Sci. 167:404-
423.
Sanides, F. 1970. Functional architecture of motor
and sensory cortices in primates in the light of a
new concept of neocortex evolution. I n C. Noback
and W. Montagna (eds.), The primate brain:
Advances in primatology, pp. 137-208. Appleton
Century Crofts, New York.
Sanides, F. 1972. Representation in the cerebral cor-
tex and its areal lamination patterns. I n G. F.
Bourne (ed.), Structure and function of nervous tis-
sue, Vol. 5, pp. 329-453. Academic Press, New
York.
Sanides, F. 1975. Comparative neurology of the tem-
poral lobe in primates including man with ref-
erence to speech. Brain Lang. 2:396-419.
Saraiva, P. E. S. and B. Magalh„es-Castro. 1975. Sen-
sory and motor representation in the cerebral
cortex of the three-toed sloth {Bradypus tridacty-
lus). Brain Res. 90: 181-1 93.
Sarnat, H. B. and M. G. Netsky. 1981. Evolution of
the nervous system. Oxford University Press, New
York.
Seltzer, B. and D. N. Pandya. 1980. Converging visual
and somatic sensory cortical input to the intra-
parietal sulcus of the rhesus monkey. Brain Res.
192:339-351.
Semsa, M., V. Casagrande, and J. Kaas. 1984. Cor-
tical connections of area 17 in tree shrews. J.
Comp. Neurol. 230:337-35 1.
Sherrington, C. 1906. The integrativeaction of the ner-
vous system. Yale University Press, New Haven.
Smith-Gill, S. J. 1983. Developmental plasticity:
Developmental conversion versus phenotypic
modulation. Amer. Zool. 23:47-55.
Snell, 0. 1891. Das Gewicht des Gehirns und des
Hirnmantels der Saugetiere in Beziehung zu
deren geistigen Fahigkeiten. Sitz. Ges. Morph.
Physiol. (Munchen) 7:90-94.
Sohal, G. S. 1976. An experimental study of cell
death in the developing trochlear nucleus. Exp.
Neurol. 5 1 :684-698.
Sokoloff, A., T. W. Deacon, and G. E. Goslow. 1989.
Musculotopic innervation of the primary flight
muscles, the pectoralis (pars thoracicus) and
supracoracoideus, of the pigeon (Columba livia):
A HRP study. Anat. Rec. 225:35-40.
Spencer, H. 1980. Principles of psychology, 2nd ed.
Longman Press, London.
Stanfield, B. B. and D. D. M. O'Leary. 1985. Fetal
occipital cortical neurons transplanted to the ros-
tral cortex can extend and maintain a pyramidal
tract axon. Nature 3 13: 135-137.
Stephan, H. 1969. Quantitative investigations o n
visual structures in primate brains. I n Proceed-
ings of the Second International Congress on Pri-
mates 3:34-42. Karger, Basel.
Stephan, H., H. Frahm, and G. von Baron. 1981.
New and revised data on volumes of brain struc-
tures in insectivores and primates. Folia Prima-
tologica 35: 1-29.
Sur, M., P. E. Garraghty, and A. W. Roe. 1988.
Experimentally induced visual projections into
auditory thalamus and cortex. Science 242: 1437-
1441.
Thompson, D. 1917. O n growth and form. Cambridge
University Press, Cambridge.
Tigges, J., W. Spatz, and M. Tigges. 1973. Recip-
rocal point-to-point connections between para-
striate and striate cortex in the squirrel monkey
(Saimiri). J. Comp. Neurol. 148:481-490.
Tigges, J., M. Tigges, and A. Perachio. 1977. Com-
plementary laminar terminations of afferents to
area 17 originating in area 18 and in the lateral
geniculate nucleus in the squirrel monkey. J.
Comp. Neurol. 176:87-100.
'Tobias, P. V. 198 1 . T h e emergence of man in Africa
and beyond. Philos. Trans. R. Soc. London B,
Biol. Sci. 292:43-56.
Tower, D. B. 1954. Structural and functional orga-
nization of the mammalian cerebral cortex. T h e
correlation of neuron density with brain size.
Cortical density in the finwhale with a note on
the cortical neurone density in the Indian ele-
phant. J. Comp. Neurol. 101:19-53.
Ulinski, P. S. 1983. Dorsal ventricular ridge. Wiley,
New York.
Ulinski, P. S. 1986. Neurobiology of the therapsid-
mammal transition. In N. Hottén, P. D. Mac-
Lean, J. J. Roth, and E. Roth (eds.), The ecology
and biology of mammal-like reptiles, pp. 149-17 1.
Smithsonian Institution Press, Washington, D.C.
Valverde, F. and L. López-Mascaraque. 198 1. Neo-
cortical endeavor: Basic neuronal organization in
the cortex of the hedgehog. Eleventh international
congress of anatomy, glial and neuronal cell biology.
Alan R. Liss, New York.
Van Valen, L. 1982. Homology and causes. J. Morph.
173:305-312.
Walsh, C. and C. L. Cepko. 1988. Clonally related
cortical cells show several migration patterns. Sci-
ence 141:1342-1345.
Walsh, T. M. and F. F. Ebner. 1970. T h e cytoar-
chitecture of somatic sensory-motor cortex in the
opossum (Didelphis marsupialis virginiana), a Golgi
study. J. Anat. 107:1-18.
Warren, S. and M. Carlson. 1986. Topography of
primary somatic sensory cortex (SI) in Old World
primates, Cercopithecus and Myopithecus. Soc. Neu-
rosci. Abstr. 12:386.1.
Wilczynski, W. 1984. Central neural systems sub-
serving a homoplasous periphery. Amer. Zool.
24:755-763.
Wiley, E. O. 1981. Phylogenetics. Wiley, New York.
View publication stats
Woolsey, T. A. and J.R. Wann. 1976. Areal changes
in mouse cortical barrels following vibrissal dam-
age at different postnatal ages. J. Comp. Neurol.
170:53-66.
Würsig, B. 1989. Cetaceans. Science 244:1550-1557.
Yakovlev, P. I. and A.-R. Lecours. 1967. The myelo-
genetic cycles of regional maturation of the brain.
In A. Minkowski (eds.), Regional development of the
brain in early life. A symposium. F. A. Davis Co.,
Philadelphia.
Zilles, K. and G. Rehkämper. 1988. T h e initial brain
concept: A work in progress. Behav. Brain Sci.
11:105-106.