Triune Brain Concept: A Comparative Evolutionary Perspective 1185
Triune Brain Concept: A Comparative Evolutionary Perspective
A B Butler, George Mason University, Fairfax, VA, USA
ã 2009 Elsevier Ltd. All rights reserved.
Introduction
In 1990, Paul MacLean published his book on The
Triune Brain in Evolution: Role in Paleocerebral
Functions, based on years of neuroethological and
neurobiological studies in his laboratory and copious
other sources. His ideas about viewing the brains of
extant mammals, including humans, as comprising
three main formations that were gained sequentially
over a long evolutionary history, have been enthusi-
astically accepted by a number of scientists, particu-
larly those interested in neuropsychiatry and related
areas but, in stark contrast, strongly rejected by most
scientists in the field of comparative, evolutionary
neurobiology. While scientific disputes are not un-
heard of, the level of disagreement over the triune
brain concept does distinguish it from many other
current hypotheses. In discussing the triune brain
concept, it is thus both necessary and of some interest
to consider not only the concept itself but also the
evolutionary, comparative point of view that takes
issue with it.
Two reviews of MacLean’s book, one by Anton
Reiner, and the other by Boyd Campbell, written the
same year as its publication, were critical on a num-
ber of points. Subsequently, in both editions of Com-
parative Vertebrate Neuroanatomy: Evolution and
Adaptation (Butler and Hodos), those criticisms
were supported. More recently, others have mounted
defenses of the triune brain concept; Jaak Panksepp
particularly addressed conflicts engendered by the
work of Joseph LeDoux on the amygdala and its
relationship to emotion, and Gerald Cory replied to
the reviews by Reiner and Campbell, as well as to the
comments on the triune brain concept in the first
edition of the Butler and Hodos textbook (as also
maintained in the second edition).
As someone thus already involved in the continuing
dispute, I will endeavor to be as objective and dispas-
sionate as possible in presenting MacLean’s triune
brain concept and also the objections to it raised by
comparative neuroscientists, recognizing that my
own background and knowledge of brain evolution
unavoidably influence and inform my perspective.
Also, since Cory characterized Reiner’s criticisms as
‘destructive’ rather than ‘constructive,’ in that Reiner
did not offer a ‘replacement generalization,’ I will do
so here. It is my hope that the alternative concepts
presented here, an objective-terminology model for
amniote brain evolution and an evolutionarily accu-
rate model of mammalian brain evolution, will clarify
the reasons why most comparative neurobiologists
view the triune brain concept as they do. These alter-
native models allow for neuroanatomical hypotheses
that encompass the recently discovered, exceptionally
high-level cognitive abilities of birds without detract-
ing from the similarly high-level cognitive abilities of
mammals and especially humans.
From an evolutionary, systematic viewpoint, birds
are actually reptiles, derived from the thecodont radi-
ation that also gave rise to crocodiles. Since the brains
of birds are, in many respect, enlarged and elaborated
versions of other reptilian brains, all of which lack the
particular cytoarchitectural arrangements that are the
hallmark of the mammalian neocortex, the triune
brain model does not account for their remarkable
cognitive abilities that far exceed the more basic,
species-specific behaviors involved in reproduction
of the species and in maintaining homeostasis that
MacLean accounts for in his model. While it was
never the intent of the triune brain model to account
for high-level cognition in birds, the fact that a brain
with very different cytoarchitecture can generate such
abilities definitively demonstrates that neocortex –
the ‘neomammalian’ telencephalic component of the
triune brain model – is not uniquely requisite to this
function. It also definitively demonstrates that birds,
as legitimate representatives of the reptilian lineage,
have far more to their telencephalons than merely
basal ganglia and far more to their behavioral cap-
abilities than just ‘species-typical stereotyped behav-
iors,’ on which the triune brain model is focused.
The various high-level cognitive abilities of birds
were not known when MacLean developed his model.
The objections that comparative neurobiologists
had to the model were, however, based on the then-
current data set of known sensory pathways and other
connections of forebrain structures in birds and rep-
tiles, as well as those in mammals. These objections
are validated by the new findings on avian cognitive
abilities. We will thus now review the basic premises
of the triune brain model and the objections raised by
the comparative, evolutionary community, two of the
most salient and important of which focus on (1) the
issue of pallial evolution across all amniotes rather
than just within the mammalian lineage and (2) the as-
signment of involvement of various particular neural
structures in the generation of a number of behaviors.
Of great importance for those whose research is
focused on human behaviors – including social,
psychological, and economic as well as pathological
conditions such as those of the basal ganglia – is that
1186 Triune Brain Concept: A Comparative Evolutionary Perspective
the ‘replacement generalizations’ (see later), the
objective-terminology model for amniotes and the
evolutionarily-accurate model for mammals, do not
contradict or undermine any of their findings or
theoretical base. These models simply rectify the con-
ceptual approach with the full range of comparative
evolutionary data on brain evolution. In his foreword
to the 2002 book, The Evolutionary Neuroethology
of Paul MacLean, Jaak Panksepp noted that emotions
cannot be understood simply as ‘‘channel functions’’
at the level of single cells but must rather be appre-
ciated as ‘‘global ‘state-functions’ reliant on complex
organic organization of broadly operating brain sys-
tems,’’ for which the triune brain concept, including
the limbic system concept, is valuable. Since both
single cellular activity and global brain systems are
active and ultimately produce emotional feelings (and
other aspects of higher order consciousness), both
need to be acknowledged and dealt with in any heu-
ristic device. The revised concepts offered in the fol-
lowing discussions are compatible at both levels.
What they both lack is the romantic cache of a ‘rep-
tilian’ image, darkly lurking under the surface, within
the deep ‘core’ of a mammal – an image unfortunately
better suited to a Victorian novel than to a scientific
hypothesis.
The Triune Brain Hypothesis
As presented by MacLean in his 1990 book, the tri-
une brain of mammals comprises three formations – a
Neomammalian
eomammalian
Pal ic syste
b m)
(lim
Reptilian
Figure 1 The triune brain model as presented by PD MacLean
in his 1990 book. Reproduced from MacLean PD (1990) The
Triune Brain in Evolution: Role in Paleocerebral Functions, p. 9.
New York: Plenum, with kind permission from Springer Science
and Business Media.
‘Reptilian,’ or ‘R-complex’ formation, a ‘Paleomam-
malian’ formation, or limbic system, and a ‘Neomam-
malian’ formation (Figure 1). These three formations
are shown with equivalent color coding for ease of
comparison across Figures 1–4. In the figure caption
of the original figure in his book (his figure 2-1),
MacLean states that ‘‘the human forebrain expands
along the lines of three basic formations that anato-
mically and biochemically reflect an ancestral rela-
tionship, respectively, to reptiles, early mammals, and
late mammals.’’ The ‘reptilian’ formation includes the
basal ganglia within the telencephalon and a number
of brain stem structures. The ‘paleomammalian’ for-
mation is the limbic system, and the ‘neomammalian’
formation is the mammalian neocortex and its asso-
ciated brain stem structures. MacLean focuses on the
limbic system as ‘‘the common denominator in the
brains of all mammals’’ (p. 16). He states that it
consists of ‘‘three main subdivisions . . . [with] the
third subdivision, for which there appears to be no
rudimentary counterpart in reptiles, . . . implicated in
parental care, audiovocal communication, and play
behavior’’ (p. 17). By implication, MacLean recog-
nizes that the other two limbic divisions may have
counterparts in the reptilian brain, but clearly
excludes the third division. The ‘neomammalian’
Neoreptilian
oreptilian
Pale
(l im bic system)
Mammalian
Figure 2 ‘Reversal test’ of the triune brain concept. Here, the
brain stem and basal ganglia are labeled as the ‘Mammalian’ for-
mation, the limbic system as the ‘Paleoreptilian’ formation, and the
expanded nonlimbic pallial areas as the ‘Neoreptilian’ formation.
This set of labels depicts amniote brain evolution from a sauropsid
chauvinist viewpoint; it is just as evolutionarily inaccurate as the
mammalian chauvinist triune brain model. The reversal test thus
demonstrates the fallacy of the latter. Redrawn and modified from
MacLean PD (1990) The Triune Brain in Evolution: Role in Paleo-
cerebral Functions. New York: Plenum.
 Triune Brain Concept: A Comparative Evolutionary Perspective 1187

Mammals Reptiles and birds

Nonlimbic pallium Nonlimbic pallium

ic system Limbic system

Limb

Basal Basal
ganglia ganglia

Figure 3 The objective-terminology model, a ‘replacement generalization’ for the triune brain concept for both mammals (left), and
reptiles and birds (sauropsids; right). This model employs labels that are objective and based on actual brain structures. As in MacLean’s
original drawing, the formations are labeled only at the level of the telencephalon as basal ganglia, limbic system, and nonlimbic pallium,
respectively. These labels comfortably and accurately accommodate evolutionary histories of both the sauropsidian and the mammalian
lineages. It should be noted that in this model, the mammalian prefrontal cortex is included in the nonlimbic pallium even though it is
sometimes thought of as a limbic component. The model easily could be modified, depending upon one’s preference, to include prefrontal
cortex as a limbic component in mammals, with a comparable adjustment in sauropsids – particularly birds – to similarly include their
pallial areas that are possibly homologous to prefrontal cortex and involved in comparable aspects of higher cognitive processing, such as
the nidopallium caudolaterale and/or the dorsolateral corticoid area. Redrawn and modified from MacLean PD (1990) The Triune Brain in
Evolution: Role in Paleocerebral Functions. New York: Plenum.

formation is the ‘‘neocortex and the thalamic struc-
tures with which it is primarily connected’’ (p. 17).
MacLean states that ‘‘In its evolution the neocortex,
together with its brainstem and neocerebellar connec-
tions, has afforded a progressive capacity for problem
solving, learning, and memory of details . . . [and has
the] capacity to generate verbal communication [in
humans]’’ (p. 17).
In a later chapter (pp. 43ff), MacLean acknowl-
edges that a large part of the reptilian (and avian)
telencephalon, the dorsal ventricular ridge (DVR), is
a pallial formation rather than a component of the
basal ganglia within the subpallium. He also acknow-
ledges that ‘‘In recent years several authors seem to
have been persuaded that the DVR is the equivalent
of the mammalian neocortex’’ (p. 45), citing the work
of Walle Nauta and Harvey Karten on this issue.
MacLean felt that ‘‘The question of whether or not
some other mammalian structure might be the coun-
terpart of the DVR is better deferred until embryo-
logical findings have been reviewed’’ (p. 45). In this
pronouncement, he was highly prescient, since it is
currently a matter of substantial debate, based to
some extent on recent embryological and gene
expression data, as to whether the DVR, particularly
its anterior part, the anterior dorsal ventricular ridge
(ADVR), is homologous to the mammalian neocortex
(i.e., at the level of various specific cell populations
within both structures, as Karten originally postu-
lated) or to the thalamo-recipient basolateral division
of the amygdala.
The better part of MacLean’s book covers neuro-
ethological and experimental behavioral observations
from his extensive work on various reptiles and squir-
rel monkeys. Since the observations of reptilian behav-
iors, and investigations into the contribution of the
basal ganglia toward these behaviors, are of para-
mount importance as the foundation of the triune
concept, this part of MacLean’s research program
will be focused on here. Much of this research was
carried out by Neil Greenberg and his co-workers in
MacLean’s Poolesville (Maryland) research facility.
Greenberg and MacLean, from extensive observations
of the behaviors of Anolis lizards in laboratory vivaria,
as well as observations on other species drawn from
the literature, categorized them into daily routines and
subroutines and component behaviors associated with
territorial and reproductive issues, including establish-
ment of homesite and homerange, patrolling territory,
ritualistic defense displays, intraspecific fighting, use of
1188 Triune Brain Concept: A Comparative Evolutionary Perspective

H H

N Ci

Ctx Ctx

C
IC ADVR ADVR
P
S
G

S S

CI
LFB LFB

A St-P St-P

Figure 4 Comparison of drawings of the left hemisphere through the telencephalon of the squirrel monkey (left), and the right
hemisphere through the telencephalon of the tegu lizard (center and right), showing the basal ganglia (tan), the limbic pallium (green),
and the nonlimbic pallium (blue). The two versions of the tegu hemisphere represent the two current hypotheses as to whether the ADVR
is a nonlimbic (center) or limbic (right) component. Regardless of the homology of the latter structure, note that most of the telencephalic
areas are pallial rather than subpallial (the basal ganglia) in both mammals and lizards. In birds, the pallial regions are even more
expanded and elaborated than in lizards. Not all structures are present in both the mammal and the tegu hemispheres at the levels shown.
A, amygdala; ADVR, anterior dorsal ventricular ridge; C, caudate nucleus; Ci, cingulate gyrus; Cl, claustrum; Ctx, cortex; G, globus
pallidus; H, hippocampal formation; IC, internal capsule; LFB, lateral forebrain bundle; N, neocortex; P, putamen; S, septum; St-P,
striatopallidum.

defecation posts, foraging, hunting, homing, hoarding,
social group formation, establishment of social hierar-
chy, greeting, grooming, courtship displays, mating
and breeding, flocking, and migration.
As discussed by Neil Greenberg in his 1988 paper,
they regarded the ‘‘highly stereotyped, species-typical
behavioral patterns, particularly social displays, [as]
the most robust data to illuminate neural corollaries
of complex behavioral functions.’’ Since MacLean
had previously found that the dorsal striatum ‘‘is
necessary for the performance of a species-typical
display in the [squirrel] monkey . . . an investigation
of the paleostriatum [i.e., dorsal striatum] of a lizard
predicated on a close understanding of the units of
behavior spontaneously emitted in naturalistic set-
tings’’ was undertaken. As summarized by MacLean
in his 1990 book, Greenberg had previously identified
major stereotyped behaviors in the blue spiny lizard
Sceloporus cyanogenys – signature (‘assertive’),
challenge (‘territorial’), courtship, and submissive
(‘appeasement,’ ‘assentive’). Similarly, Anolis lizards,
under the seminatural vivarium conditions of the
laboratory, exhibit social displays that include asser-
tion (a ‘general arousal’), challenge (addressed to a
conspecific male), and courtship (addressed to a con-
specific female).
Of these behaviors, only the challenge display was
disrupted by lesions that involved the output pathway
(the lateral forebrain bundle region) of the striatum.
The species-typical stereotyped behaviors of assertion
and courtship were not disrupted by such lesions.
Other studies have not contributed any additional
definitive indication of striatal involvement in these
sorts of functions. While both lesion and stimulation
studies are subject to problems of interpretation, the
lack of evidence that the basal ganglia generate most
of the behaviors observed in reptiles should preclude
designating this part of the brain as singularly crucial
to them. The broad generalization of assigning most
aspects of reptilian behavior to the ‘R-complex’ in
the triune brain model simply is not justified by the
experimental data. Other parts of the reptilian brain,
particularly the pallium, may well be contributing
substantially, in concert with the basal ganglia, to a
number of these behaviors, just as in mammals the
neocortex and the basal ganglia interact in concert to
generate cognitive and affective as well as stereotypical
motor behaviors.
 Triune Brain Concept: A Comparative Evolutionary Perspective 1189
Origins of the Triune Brain Hypothesis and
the Comparative Neuroanatomical
Perspective
Paul MacLean’s life and career recently have been
reviewed by Kelly Lambert. Having received his med-
ical degree at Yale University School of Medicine and
exposure to the field of psychiatry during a World
War II assignment to New Zealand and a brief stint in
private practice, MacLean had worked in the labora-
tory of Stanley Cobb at Massachusetts General Hospi-
tal and subsequently held a position in the Department
of Physiology at Yale Medical School. During this
period he developed an interest in the work of James
Papez, who was at Cornell, and was able to meet with
him to discuss Papez’s work in comparative neuroanat-
omy and the circuitry of the limbic lobe in mammals.
In a paper published in 1952, MacLean coined the
term ‘limbic system’ to refer to the set of structures that
include the limbic lobe of Broca plus the related brain
stem structures. While this term has been criticized in
some circles, as Panksepp has discussed, it has been
widely accepted by comparative neuroanatomists,
since the main components of this system – such as the
hippocampus and its related cortical areas, the septal
nuclei, hypothalamus, amygdala, and ventral striato-
pallidal components – are widely distributed across
vertebrates. This issue will thus not be discussed further
here, since from the comparative viewpoint, the limbic
system concept per se is not a point of contention.
In 1957, MacLean joined a newly founded lab
section at the National Institutes of Health (NIH),
which subsequently was named the Section on Limbic
Integration and Behavior, and in 1971 moved to new
NIH laboratory quarters near Poolesville, Maryland,
where he was able to expand his studies to include
reptile behaviors and to begin his efforts to under-
stand the possible contributions of the basal ganglia
to these behaviors. During the several years on either
side of that point in time, two major breakthroughs in
comparative neuroanatomy were occurring, one in
regard to the telencephalic pallium of birds and rep-
tiles and the other in regard to similar parts of the
brain in sharks.
In sharks, Sven Ebbesson and his colleagues had
found that (1) olfactory projections are confined to a
small region of the lateral pallium, rather than being
widely distributed across it, (2) two major ascending
pathways, one via the midbrain roof and thalamus and
one directly via the thalamus, to nonlimbic parts of the
pallium are present, and (3) the integrity of the pallium
is necessary for the sharks to discriminate visual pat-
terns. This new information contradicted the then gen-
erally accepted idea that the forebrains of all fishes
were dominated by olfactory information – mere
‘smell brains’ – and that the other sensory systems
had ‘invaded’ the forebrains of terrestrial vertebrates
during their evolutionary transition. In regard to the
telencephalic pallium of birds, Harvey Karten and
his colleagues had confirmed that a large structure
in the telencephalon, the DVR (now also referred to
in birds as nidopallium and mesopallium) is indeed
pallial rather than subpallial and also is in receipt of
several ascending sensory pathways – as known at
that time, a visual and an auditory pathway, and,
as later identified, a somatosensory pathway. These
sensory pathways are in addition to the then-known
visual pathway to the more caudal part of the avian
equivalent of the cortex in reptiles, called the Wulst
or hyperpallium, and a subsequently discovered
somatosensory pathway to its more rostral part that
also gives rise to a pyramidal tract-like efferent
motor pathway.
By the mid-1970s, these findings in sharks and
birds were published and were augmented by findings
of similar ascending sensory pathways in a variety of
reptiles. In 1978, MacLean held a conference at his
Poolesville laboratory, to which a number of us were
invited and at which many of these findings were
presented and subsequently published in the resulting
book, edited by Neil Greenberg and Paul MacLean,
Behavior and Neurology of Lizards. A survey of the
comparative findings on telencephalic evolution
across vertebrates was subsequently published in
another volume edited by Sven Ebbesson in 1980,
from a conference held in Caracas, Venezuela, Com-
parative Neurology of the Telencephalon, and from
the mid-1960s to the present, a massive body of
publications on this subject has appeared in the pri-
mary literature and other symposium volumes.
In his own summary of his triune brain hypothesis,
MacLean acknowledged current findings about
brain evolution within amniotes, particularly within
the sauropsid radiation of reptiles and birds, but
then set them aside in favor of his ‘triune model’ of
brain evolution within the mammalian line. In the
caption for his famous figure of the mammalian
triune brain (his figure 2-1), he states that the three
formations within the brain – the parts of which
are labeled at the rostral end of the brain as the
‘Reptilian’ formation (or ‘R-complex’), the ‘Paleo-
mammalian’ formation (limbic system), and the
‘Neomammalian’ formation (neocortex and its related
thalamic structures) – ‘‘reflect an ancestral relation-
ship, respectively, to reptiles, early mammals, and
late mammals.’’ The latter statement is contradictory
to all data collected and analyzed by comparative stud-
ies over the past four decades, as already discussed.
A ‘reptilian’ formation – that is, the basal ganglia – is
1190 Triune Brain Concept: A Comparative Evolutionary Perspective
common to early and late reptiles, early and late birds,
and early and late mammals. A ‘paleomammalian’ for-
mation, or limbic system, is also common to all of these
taxa. While neocortex is indeed a unique feature of
mammals, an expanded nonlimbic pallium, part of
which comprises the neocortex in mammals, is likewise
common to all of these taxa, and this crowning compo-
nent of the telencephalon is particularly elaborate and is
involved in sensory processing and associative functions
that reach very high cognitive levels in both mammals
and birds.
MacLean notes in his discussion of anatomical and
functional comparisons (in chapter 2 of his 1990
book) that a large formation, the DVR is present in
sauropsid brains and is clearly pallial. However, he
regards it as having been independently evolved and
as not being of significant interest in regard to the
evolutionary origins of mammalian neocortex. In this
view, he is partly correct and partly wrong. As dis-
cussed by Anton Reiner, early amniotes most likely
had neither neocortex nor a DVR, but rather had a
small ‘‘proto-DVR’’ region in the lateral aspect of the
pallium and a modest region of cortex medial to it. In
the mammalian lineage, which precedes the reptilian
lineage in the fossil record by 10 My, the more medial
region became expansively elaborated to form part
(or possibly all) of the neocortex, and the lateral
region likewise became elaborated to form either
part of the neocortex and/or the pallial, thalamo-
recipient (basolateral) part of the amygdala. In the
sauropsid line, the lateral region became elaborated
and expanded to form the definitive DVR, and the
medial region formed the rudimentary cortex; within
the avian lineage, the medial region expanded
substantially to form the Wulst, while the DVR
expanded further to reach its apogee.
The triune brain hypothesis, by essentially dismiss-
ing interest in pallial elaboration within the sauropsid
line, errs by instead promoting the scientifically
contradicted but still widespread popular view of a
scala naturae, a linear ranking of animal taxa, with
fish near the bottom, reptiles not much higher, non-
human mammals higher and ranked in sequence
(such as rat-to-cat-to-monkey), and with humans at
the top. The summary figure of the triune brain, now
widely published and commonly referred to in some
of the psychiatric literature, implies that the core
structures of basal ganglia and the more caudal
parts of the brain stem represent the ‘reptilian brain’
that is still present in mammals, including humans. It
specifically states that the gain of a limbic system
occurred in early mammals. It specifically implies
that a large, expanded nonlimbic pallium is unique
to mammals.
Applying a ‘reversal test’ is often a fruitful way to
assess particular situations or statements. We can
apply this test to the triune brain hypothesis to assess
whether it is a reasonable view of brain evolution.
Figure 2 shows the view of brain evolution, as seen
from the sauropsid point of view. The labeling in this
figure is equally incorrect, from the established body
of data on brain evolution, as that of MacLean’s
canonical figure. It identifies the core of the brain as
the ‘Mammalian’ formation, the limbic system as the
‘Paleoreptilian’ formation, and the nonlimbic pallium
as the ‘Neoreptilian’ formation. As we have noted, in
birds the ‘Neoreptilian’ formation, comprising the
Wulst and DVR, is particularly expanded, and the
recent findings of highly sophisticated cognition of
which at least some birds are capable compel viewing
it as a worthy rival of neocortex in terms of its neural
processing abilities. To ignore the sauropsid line and
to assign some mammalian behaviors as ‘reptilian’ is
to ignore a virtual goldmine of information on how
neurons process and assess information and how
thoughts and emotions are generated and dealt with.
In trying to understand human behaviors, the latter
course is as foolish as if one were to ignore all mam-
malian, including human, research and study only
reptiles and birds. Taking the complete picture into
account, based on the actual evolutionary events and
particularly including the intriguing differences in
cytoarchitecture of the pallial formations in saurop-
sids versus mammals, is the course most likely to yield
a correct understanding of pallial function, including
the generation of complex human behaviors.
In assessing the triune brain model, one wonders
why MacLean did not simply label its components by
their correct terms, as shown in Figure 3. In this figure
the core of the brain (at the telencephalic level) is
labeled ‘basal ganglia.’ The limbic system is so
labeled, and the overlying nonlimbic pallium is like-
wise labeled as itself. These labels are objective; they
have no scala naturae baggage attached to them. All
mammals and all reptiles and birds have a core region
(in simplistic terms) that includes the basal ganglia
within the telencephalon. All mammals and all rep-
tiles and birds have a limbic system. All mammals and
all reptiles and birds have an expanded nonlimbic
pallium. For that matter, fish and amphibians also
have components of the basal ganglia, limbic system,
and nonlimbic pallial regions. None of these neural
systems is unique even to amniotes, let alone to mam-
mals. This objective-terminology model is a highly
reasonable ‘replacement generalization’ for the triune
brain model. It is anatomically accurate, simple, and
straightforward, and does not conflict with any phylo-
genetic data. It is wholly applicable to all of the
 Triune Brain Concept: A Comparative Evolutionary Perspective 1191

clinical and related findings to which the triune brain
model has previously been applied.
Another view of the anatomical comparison is
shown in Figure 4. In this figure, a drawing of a trans-
verse hemisection through the telencephalon of a
squirrel monkey, the species of primate that Paul
MacLean studied so extensively, is shown on the
left, and two similar drawings of a transverse hemi-
section through the telencephalon of a tegu lizard
(with features essentially the same as that of Anolis
and other lizards of this DVR type) is shown on
the right. The two drawings of the lizard telen-
cephalon represent the two extremes in the current
debate about homology of the ADVR: whether it is
nonlimbic pallium, as indicated by its blue shading in
the first (center) drawing, or whether it is amygdala
and thus a limbic component, as indicated by its green
shading in the second drawing. Either way, it is clear
that the reptilian telencephalon is largely constituted
by pallial territory, just as are mammalian and avian
brains, and that the structures designated as the
‘R-complex’ by MacLean (the basal ganglia, shaded
in tan) comprise only a minor fraction of the telence-
phalic tissue.
For those in the clinically related fields who still
wish, however, to retain the triune brain concept (or at
least some version of it that may be more in line with
the data accumulated to date), a view that focuses

Early mammals:
Possible addition of thalamocingulate component
to limbic system with neocortical cytoarchitecture
of cingulate gyrus; expanded primary sensory-recipient
and motor pallial areas plus addition of more
association pallial areas, including prefrontal cortex,
all with neocortical cytoarchitecture:
‘Stem Mammalian Formation’
Therian mammals:
Additional association neocortical
Common amniote ancestor:
areas, particularly in the occipital,
Basal ganglia, major limbic system
temporal, and parietal lobes; expansion
components, primary sensory-recipient
of the prefrontal cortex; and gain of
and motor pallial areas, and a few
the corpus callosum:
association pallial areas:
‘Therian Formation’
‘Common Amniote Formation’
or ‘A-complex’

Figure 5 The evolutionarily accurate model of brain evolution within the mammalian (synapsid, i.e., with one temporal fenestra in the
skull) radiation, which separated from ancestral lineage of anapsid (lacking any bony fenestrae) amniotes 10 My before the sauropsid
(diapsid, i.e., with two temporal fenestrae) line of ancestral reptiles appears in the fossil record. In this model, the neural components
present in the common, anapsid ancestor (‘Common Amniote Formation,’ or ‘A-complex’) include major limbic system components,
primary sensory-recipient and motor pallial areas, and a few association pallial areas, in addition to the basal ganglia. Early mammals and
therian (marsupial and placental) mammals then gained additional structures and/or modifications to existing structures, as shown for the
‘Stem Mammalian Formation’ and ‘Therian Formation,’ respectively. Redrawn and modified from MacLean PD (1990) The Triune Brain in
Evolution: Role in Paleocerebral Functions. New York: Plenum.
1192 Triune Brain Concept: A Comparative Evolutionary Perspective
solely on the mammalian lineage but is evolutionarily
accurate is shown in Figure 5. This is offered here as
an alternative ‘replacement generalization.’ It suffers
from being more cumbersome in terms of the detail
put into the labels for the three sets of brain structures,
which even so are only a generalization. It is not
shaded in colors as was done for the other figures,
since the comparison is no longer one-to-one. The
‘common amniote formation’ (or ‘A-complex,’ for
those who wish to use such a term), shown in light
gray, includes much more than the basal ganglia, and
so its color shading would necessarily have to include
all three colors used before – tan, green, and blue. Both
the intermediately positioned area shown in white,
designated here as the ‘Stem Mammalian Formation,’
and the outer area shown in darker gray, the ‘Therian
Formation,’ would have to include both green and
blue. While this model does not thus correspond easily
to the original triune brain model or to the objective-
terminology model, it nonetheless reflects in some-
what more detail the particular evolutionary course
that was taken along the mammalian lineage.
When MacLean developed his triune brain model,
the extensive and very high-level cognitive abilities of
birds, as alluded to several times previously, were not
appreciated. One of the most crucial and difficult
questions to answer in all of neurobiology is how
such complex cognitive abilities and the probably
correlated high levels of consciousness are generated
by neuronal assemblies. The foundation of behavioral
data amassed by MacLean as well as the numerous
other studies in the literature can contribute to
answering this question when assessed in an evolu-
tionarily accurate perspective. For example, in dis-
cussing the ‘paleomammalian formation,’ as noted
earlier, MacLean specifically cited the third division
of the limbic system, that is, its thalamocingulate com-
ponent, as being ‘‘implicated in parental care, audio-
vocal communication, and play behavior.’’ While it
is true that only a few reptiles (mostly crocodiles)
exhibit even the most rudimentary of these behaviors,
birds exhibit all three to an extensive degree. In his
1981 book Animal Play Behavior, Robert Fagan
documents and discusses many examples of play
behavior in birds; the literature that documents the
complexity of song learning and production in song-
birds is extensive; and the maternal care exhibited by
most species of birds is widely known.
In discussing the ‘neomammalian formation,’
MacLean cites its roles in ‘‘problem solving, learning,
and memory of details . . . [and its] capacity to gener-
ate verbal communication.’’ As reviewed by Butler
and Cotterill, the recent spate of studies on avian
cognitive abilities has established that various species
of birds also can problem-solve, learn, and remember
to an extensive degree, and even generate verbal com-
munication. In fact, they exhibit numerous cognitive
behaviors of a very high level. They (1) use transitive
inference, the use of logical and successive compar-
isons (a process attributed to the working memory
functions of prefrontal cortex in humans and some
other mammals) to determine social hierarchies,
(2) exhibit a phenomenon called coherence, or multi-
stability, of ambiguous figures, previously considered
unique to primates and also involving working mem-
ory, in which one interpretation of a visual stimulus
(such as a Necker cube) is perceived for a set of trials,
followed by a set of the alternate interpretation,
rather than just randomly switching back and forth,
(3) form conceptual categories, such as distinguishing
cubist paintings from impressionist ones, (4) exhibit
object constancy to a high level, as delineated by
Piaget, (5) manufacture tools for use in food
gathering, another ability previously thought unique
to primates, (6) culturally transmit the design features
of such tools to conspecifics, (7) communicate with
humans using the English language to an extensive
degree, (8) understand numerical concepts up to
about the number 7 and also exhibit a zerolike
concept – a particularly challenging feat, (9) exhibit
theory of mind in terms of anticipating and taking
steps to prevent thievery from food caches by conspe-
cifics and practicing deceptive behaviors to outwit a
dominant rival, and (10) exhibit the capacity to remem-
ber past events and their relative lengths of time.
These high-level cognitive abilities are all supported,
in concert with the thalamus and other structures, by
the ADVR and Wulst in birds – the pallial regions of the
telencephalon that are homologous to major pallial
regions in mammals and to the major pallial regions
of reptilian brains as well. One of the strengths of the
comparative method is its focus on identifying both
the similarities and differences between brains and the
correlated functions that they support. The objective-
terminology model of amniote brain evolution offered
here (Figure 3) facilitates such comparisons and can
contribute to illuminating how different cytoarchitec-
tures, including our own, support the generation of
high-level cognition and consciousness by neuronal
assemblies.
See also: Basal Ganglia: Evolution; Brain Development:
The Generation of Large Brains; Brain Evolution:
Developmental Constraints and Relative Developmental
Growth; Brain Evolution: The Radiator Theory; Brain
Fossils: Endocasts; Broca’s Area: Evolution; Cerebellum:
Evolution and Comparative Anatomy; Comparative
Neurobiology: History; Neuroanatomy Methods in
Humans and Animals.
 Triune Brain Concept: A Comparative Evolutionary Perspective 1193
Further Reading
Butler AB (1994) The evolution of the dorsal pallium in the telen-
cephalon of amniotes: Cladistic analysis and a new hypothesis.
Brain Research Reviews 19: 66–101.
Butler AB and Cotterill RMJ (2006) Mammalian and avian neuro-
anatomy and the question of consciousness in birds. Biological
Bulletin 211: 106–127.
Butler AB and Hodos W (2005) Comparative Vertebrate Neuroanat-
omy: Evolution and Adaptation, 2nd edn. Hoboken, NJ: Wiley.
Campbell CBG (1992) Book review (MacLean: The Triune Brain in
Evolution). American Scientist 80: 497–498.
Clayton NS, Bussey TJ, and Dickinson A (2003) Can animals recall
the past and plan for the future? Nature Reviews Neuroscience
4: 685–691.
Cory GA Jr. (2002) Reappraising MacLean’s triune brain concept.
In: Cory GA Jr. and Gardner R Jr. (eds.) The Evolutionary Neuro-
ethology of Paul MacLean, pp. 9–27. Westport, CT: Praeger.
Cory GA Jr. and Gardner R Jr. (eds.) (2002) The Evolutionary
Neuroethology of Paul MacLean. Westport, CT: Praeger.
Ebbesson SOE (1980) Comparative Neurology of the Telencepha-
lon. New York: Plenum.
Fagan R (1981) Animal Play Behavior. New York: Oxford Univer-
sity Press.
Greenberg N (2002) Adaptive functions of the corpus striatum: The
past and future of the R-complex. In: Cory GA Jr. and Gardner
R Jr. (eds.) The Evolutionary Neuroethology of Paul MacLean,
pp. 45–81. Westport, CT: Praeger.
Greenberg N, Font E, and Switzer R (1988) The reptilian striatum
revisited. In: Schwerdtfeger WK and Smeets WJ (eds.) The
Forebrain in Reptiles: Current Concepts of Structure and
Function, pp. 162–177. Basel: Karger.
Greenberg N and MacLean P (eds.) (1978) Behavior and Neurology
of Lizards. Rockville, MD: National Institute of Mental Health.
Lambert KG (2003) The life and career of Paul MacLean:
A journey toward neurobiological and social harmony. Physio-
logy & Behavior 79: 343–349.
MacLean PD (1990) The Triune Brain in Evolution: Role in Paleo-
cerebral Functions. New York: Plenum.
Panksepp J (2002) Foreword: The MacLean legacy and some mod-
ern trends in emotion research. In: Cory GA Jr. and Gardner R
Jr. (eds.) The Evolutionary Neuroethology of Paul MacLean,
pp. ix–xxvii. Westport, CT: Praeger.
Pepperberg IM (1999) The Alex Studies: Cognitive and Communi-
cative Abilities of Gray Parrots. Cambridge, MA: Harvard
University Press.
Reiner A (1990) An explanation of behavior [review of The Triune
Brain in Evolution: Role in Paleocerebral Functions, by Paul
D. MacLean, 1990]. Science 250: 303–305.
Reiner A (2000) A hypothesis as to the organization of cerebral
cortex in the common amniote ancestor of modern reptiles and
mammals. In: Bock GR and Cardew G (eds.) Evolutionary
Developmental Biology of the Cerebral Cortex. Novartis Foun-
dation Symposium 228, pp. 83–102. Chichester, UK: John
Wiley & Sons.
Reiner A, Yamamoto K, and Karten HJ (2005) Organization and
evolution of the avian forebrain. The Anatomical Record Part A
287A: 1080–1102.
Weir AAS, Chappell J, and Kacelnik A (2002) Shaping of hooks in
New Caledonian crows. Science 297: 981.