The Journal of Socio-Economics 35 (2006) 626–633

The evolutionary neuroscience of human reciprocal

sociality: A basic outline for economists
Daniel R. Wilson
Departments of Psychiatry and Anthropology, Creighton University, 3528 Dodge Street, Omaha, NE 68114, USA

Abstract
MacLean’s tri-level concept of the human brain is the foundational concept for a comprehensive under-
standing of human sociality from the standpoint of physiology and medicine. This conceptual platform
is basic to any proper contextualization of evolutionary psychiatry, as MacLean essentially describes two
opposing archetypal neuromental circuitries upon which our sociality is based. It is important that the
social sciences, notably economics, achieve more comprehensive, reliable and valid progress. Integration
of evolutionary behavioral neuroscience is especially pertinent as deficiencies of the received model – a
hyper-rational, self-interested homo economicus – are increasingly evident.
In particular, the MacLeanian model is re-emerging as the principal basis for an evolutionary psychology
with meaningful attention to both genes and brains. This evolutionary psychology is, in turn, the most natu-
ralistic and accurate formulation for reciprocity and exchange behavior of social species, notably humans. As
such, evolutionary neuroscience is of direct and increasing pertinence to economics generally and especially
socioeconomics. This paper is meant to cogently summarize key elements to foster greater cross-inquiries
between evolutionary neuroscience and economics.
© 2006 Elsevier Inc. All rights reserved.

JEL classification: C710; C720; A120; Z130

Keywords: Evolution; Neuroscience; Economics; Psychiatry; Genetics; Brain

1. Introduction

Economics is in need of a more valid model of human behavior. Deficiencies of the received
model – the hyper-rational, self-interested, utilitarian homo economicus first indicated by Smith
(1776) posited by Lowe (1935) – are increasingly evident. While superb for much classical
economic applications, it misses many naturalistic and significantly instinctive or emotive aspects
that facilitate the algorithms of decision-making as initially described by Darwin (1859).

E-mail address: wilson@creighton.edu.

1053-5357/$ – see front matter © 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.socec.2005.12.020
 D.R. Wilson / The Journal of Socio-Economics 35 (2006) 626–633 627

Fortunately, MacLean’s tri-level conceptual platform of the human brain is the foundational
concept for a comprehensive understanding of human sociality from the standpoint of physiology
and medicine (MacLean, 1949, 1985, 1990; Wilson, 2002). This evolutionary neuropsychology
is, in turn, the most naturalistic and accurate formulation in the science of attachment, reciprocity
and exchange behavior of social species, notably humans (Bowlby, 1969, 1973, 1980). Yet without
a formulation ala’ MacLean, the data raining in from evolutionary neuroscience drowns out most
any effort to understand the complex heuristic of global state mechanisms that underlie human
social exchange and reciprocity behavior.
Indeed, even a school-boy or school-girl survey of the human brain is daunting for its nigh
unchartable ranges – a billion years of evolution, hundreds of neuromodulators, thousands of
genes and millions-to-billions of neurons, and trillions of synapses. Though in some respects
seemingly simple, comprised as it is of a modal 1400 g of 78% water, 10% fat, 8% protein, even
basic brain anatomy and physiology is quite complex and ever more so up the scala natura.
Serial assemblages are plainly evident in hierarchical fashion as well as the species-specific body
mass indices. Human brain is perhaps the most complex and among the most robust indices of
species-specific neuronal counts and brain-mass in relation to body size. For example, the fruit
fly has some 100,000 neurons, monkey nearly 10 billion, and human on the order of 100 billion.
In all, the modal human brain has 1.5 M km of nerve fibers even though non-axonal glial cells
considerably out-number neurons. Beyond this fundamental and complex anatomy, there is a new
appreciation for the vast arena of developmental plasticity, again rising with the taxonomic scale.
Adult humans have 1/2 the neurons compared to a 2-year old and lose some 10 k daily through
the span of adult life (Panksepp, 1998, 2003).
Yet, cognition and wisdom gather well into the life-span despite (and in some ways perhaps
due to) this on-going neural pruning. That this counter-intuitive accrual of wisdom from experi-
ence can occur at all in the face of apparent neural decline is remarkable enough; but it is now
further confirmed that neural stem cells enable regeneration and remodeling throughout the life-
cycle of most species, including humans. So too, evidence abounds that human brain adjusts to
environmental stress via gain or loss of cells and synapses, including direct evidence that stress
– with its cascades of biomodulators – reduces key cell populations that can be restored, at least
with the early resolution of stress. Given the vast scale, the complex phylogentic assemblages and
the here-to-fore unthinkable ontogentic dynamism of brain, it is simply impossible to coherently
integrate the data without a model such as MacLean’s (Wilson, 1998; Panksepp, 1998; Mayr,
1988).
Meanwhile, the social sciences have begun a long-deferred embrace of relevant natural sciences
– all as explicitly predicted by Wilson in his magisterial sociobiology (Wilson, 1975). Adam Smith
(1776) distinguished the human species by the “. . . propensity to truck, barter, and exchange. . .”,
which Lowe (1935) dubbed “Homo Economicus”. With this, the evolutionary neurosciences have
a priority place due to the comprehensive validity, reliability and vigor with which they infuse
efforts to fully understand behavior, especially social behavior and most especially reciprocal
exchange of highly social species. Thereby, evolutionary neuroscience is of direct and increasing
pertinence to economics generally, especially socioeconomics.

2. ‘Tug and pull’ in the triune brain

MacLean’s neuroethological conceptualization essentially describes three main levels of

archetypal neuromental circuitries upon which our sociality is based. It further is compatible
with two opposing algorithms – one for self-maintenance (agonic competition) and the other for
628 D.R. Wilson / The Journal of Socio-Economics 35 (2006) 626–633

care-giving (or hedonic affection) – operating with rather more refinement as three main assem-
blages arose in succession (Price, 1988; Gilbert, 1992; Gilbert et al., 1995). This evolutionary
neuroethological model is currently the only synthesis that renders the vastly larger and pro-
foundly complex body of neuroscientific data as a valid and workable schematic (Cory, 1999,
2003; Cory and Garnder, 2002; Wilson, 2002). That this schematic describes a coherent, global
state mechanism is increasingly important for much social science if the latter is to achieve reliable
and valid theoretical or practical progress – much less subsume and reconcile the huge influx of
pertinent neurobiological and evolutionary facts underlying behavior.
The first of these three circuitries MacLean dubbed the Reptilian complex (‘R-complex’). The
R-complex is constituted of the brain stem and midbrain (along with a very small and primitive
part of forebrain). These anatomical structures and behavioral functions evolved with early cold-
blooded vertebrates and became fully instantiated in the essentially asocial, self-maintaining
circuitry of the reptilian line ancestral to humans.
The second of these circuitries MacLean dubbed the ‘Paleomammalian complex’ (or, as an
alternative, often retaining a slightly modified extant term, the ‘limbic system’). The paleomam-
malian limbic system comprises a more recently elaborated assemblage anatomically bordering
the earlier R-complex. MacLean’s limbic system is a refinement of the ‘Lobe Limbique’ of Broca,
who so named it as it was at the edge (or limbus) of the old brain (Broca, 1878; Pribram, 1958;
Harlow and Harlow, 1965). The earliest aspects of limbic system evolution trace to the transitional
emerging from the reptilian line 300 million years ago.
The paleomammalian complex became fully instantiated with the more comprehensive and
complete mammalian neural structures and behavioral functions that evolved with remarkable
rapidity some 120 million years ago. Within only 10 million years or so were laid down
the exceptionally complex neuroendocrine anatomical physiology that facilitates all classical
mammalian behavior ranging from internal fetal development, parturition, nursing of infants,
parent–infant bonding, and continuous interactive, reciprocal ‘warm-blooded’ social life (not to
mention innovations such as hair and thermo-regulation as well as diverse far more detailed
somatic endocrinology).
Interestingly, the earliest feature of the limbic system is the thalamocingulate gyrus that first
evolved to enable ancient mammalian mothers to identify the distress cries of their off-spring
(Clutton-Brock, 1991; Wilson, 2002). Later if equally critical adaptations of the paleomammalian
complex allows for the emergence of play – reciprocal and convivial social interaction – among
mammals as a more general social extension of kinship bonding. Thus, the parent–infant bond
that blends self-preservation genetic kinship circuitry with affectional circuitry in a reciprocal
social relationship is, in fact, the foundation for extended social reciprocity (‘eusociality’ and
altruism) that underpins human social life (Piaget, 1971; Wilson, 1975; Plutchik, 1984; Zajonc,
1980; Panksepp, 1998; Carter and Keverne, 2002; Gardner and Wilson, 2003).
Both the archetypal reptilian and early mammalian circuits are necessary to human sociality.
The second was not possible without the first and certainly much interactivity has evolved. Mam-
malian social circuitry rests upon a basis of self-maintaining circuitry in a manner that reflects
Maslow’s ‘Hierarchy of Needs’ with safety first (Maslow, 1971). Moreover, to be favored in Dar-
winian selection and passed in the genome, their interplay must keep within survival limits. Indeed,
even before more recent advances in neuroscience and evolution, ethologists such as Harlow and
Harlow (1965), Chance (1967) and Bowlby (1969, 1980) earlier posited such eusociality as a
central element in their concepts of affectional systems and attachment, respectively.
MacLean identified a third level of circuitry the ‘Neomammalian complex’. This neomam-
malian complex is anatomically and behaviorally synonymous with the limbic cortex as it extends
 D.R. Wilson / The Journal of Socio-Economics 35 (2006) 626–633 629

Table 1
Neuromentalities: three main layers of brain and behavior
Taxonomic level Brain structure Phylogeny

Chordates Spinal cord >500 million years ago

Reptilians Midbrain ∼240 million years ago
Mammalians Paleolimbic cortex ∼120 million years ago
Primatohominoids Neolimbic and neocortex <40 million years ago
Hominids Domain-specific neocortex <1 million years ago

the capabilities of the two older circuits more deeply canalized in evolution. That is, the cortical
elements of the limbic system allow increasingly sophisticated and frequently conscious analysis
of a rational-emotive type. Moreover, the limbic cortex emotive rationality mediates essentially
opposing behavioral options.
Such analytic medications are often enriched via domain-specific input from higher cortical
centers, e.g., primary, secondary and tertiary association neocortex that are the basis for language,
numeracy, abstract reasoning (and other talents such as musicality and sensory synesthesia). The
considerable interaction between the limbic system and neocortex is a factor that has greatly
extended reciprocally interactive social life, including self-consciousness, romance, charisma,
Machiavellian intellect and much else (Gilbert et al., 1995; Cosmides and Tooby, 1992).
Between the most primitive vegetative neural apparatus in pre-chordates and the most recent
and abstract domain-specific modules of neocortex, there are three major phylogenetic levels
wherein brain and mind modulate social behavior. These three levels mediate proximal aspects
of social rank competition that, ultimately, allocate resources consistent with Darwinian fitness
(Darwin, 1859). The later, more advanced of these neuromental assemblages are less ‘hardwired’
and thus can better adjust phenotypy in the face of environmental challenges individuals experience
in the course of ontogenic development (Wilson, 1998).
Put differently, instinctive reactions are typical of earlier, more primitive levels whereas expe-
rienced awareness can literally become embodied higher in the mammalian line. Likewise, social
relations moved up from a base level of self-referential egoistic gratification to the higher levels
of more affiliative exchange behavior. The three major levels are summarized in Table 1.

3. Game theoretic models of the triune brain

From the foregoing survey of relevant evolutionary aspects of social psychology and behavioral
neurology, it is clear that several key assemblages of brain structures and mental processes direct
proximal aspects of social behavior toward the ultimate enhancement of differential reproductive
success. Game theoretical mathematics is useful to further explore the two opposing archetypal
neuromental circuits upon which our sociality is based. Game theory offers formal mathematical
operations that demonstrate how both these assemblages and their bimodal global state behavioral
circuits became stabilized in evolution (Borel, 1953a,b,c; Hamilton, 1963; Hamilton and Cairns,
1963; Parker, 1984; Price, 1988; Maynard Smith, 1982; Gilbert, 1992).
Game theory thus renders global state behavioral algorithms as two fundamental repertoires
or modes of interaction, i.e., ‘Hawk’ (bellicose), and ‘Dove’ (obeisant). Agonic and Hedonic are
alternative terms used commonly in behavioral science and clinical research. Terminology apart,
what is critical is how these two archetypal modes mediate extremes of social power (manic
630 D.R. Wilson / The Journal of Socio-Economics 35 (2006) 626–633

dominance versus depressive submission, etc.). Dovish Hedonia produces de-escalation and risk
of loss or social subordination whereas Hawkish Agonia produces escalation aiming at gain or
social domination.
Moreover, the past 50,000,000 years of social brain evolution in primates (and other highly
social species) has even more elaborately optimized behavior in kin bands. This has been via strong
selection of social skills including complex, abstract intellect and linguistic communication among
small, egalitarian, foraging bands of close kin whose relationships endured across life-cycle and,
thereby, assured that personal traits converge closely with social esteem (Wilson, 1998).
Again, this balance, this ‘tug and pull’ between competition and cooperation was build upon
retained reptilian and paleomammalian structures. All this optimized social brain behavior relies
on an expanded limbic system and neocortex with many new subtypes of neurohormones and
other modulators (notably neurotransmitters such as dopamine, serotonin, gamma amino butyric
acid, and other new varieties arborized within the higher neuromental assemblages, see Wilson,
1998). Although ‘young’ in evolutionary terms, these more recent primatohominoid advances
in brain and behavior, in human terms their earliest manifestations are still quite ancient. They
began to differentiate from paleomammalian ancestral types even before India was geologically
attached to Asia, that is remarkably enough, before the rise of the Himalayas.
All this changed in the past 15,000 years – a geologic ‘blink of the eye’ – amid radical
‘demographic transitions’ of the Holocene. Chief among these changes are effects of mass urban
society, migration, agriculture and technology, complex economies and (EEA) habitat destruction.
In consequence, human phenotypes are now ‘reactive’ as adaptations evolved in past phylogeny
are increasingly ‘mismatch’ to new environmental factors (Wilson, 1998). Although germane to
future and more in-depth study of the evolutionary neuroscientific foundations of economics,
analysis of mismatch is an important area of evolutionary psychology but beyond the focus of
this paper (see Bailey, 1987 for a full explication).
Game theoretical models demonstrate subtle but significant differences in how the two opposing
archetypal neuromental modes of behavior operate at each phylogenetic level. This is of direct
importance to social sciences and economics in that human behavior is not solely the product of
rational thought in the highest centers of the brain. Much decision-making still springs from older
mammalian and reptilian neuromental circuits and behavioral algorithms.
Game theory models R-complex in terms of ‘Ritualized Agonistic Behavior’ (RAB), as is
appropriate for basic algorithms of ‘fight or flight’, evolved some 250 million years ago (Lorenz,
1981; Price, 1988; Maynard Smith, 1982). Strong, strident animals maintain territory or other
resources to influence weaker, cowering rivals. This is via displays that are entirely instinctual as
driven by the non-conscious interactions of the autonomic (automatic) nervous systems of two
rivals. These instinctive behaviors are mediated by circuits enervated by the earliest and most
basic vertebro-reptilian types of neurotransmitter receptors (e.g., dopamine 1; serotonin 1; see
Wilson, 2002). The tug and pull in specific individuals alters the balance of such neurotransmitters
in patterns that predictably predispose to a higher or lower status in the pecking order.
Game theory models the paleomammalian level in terms of ‘Resource Holding Potential’
(RHP), as is appropriate for more subtle algorithms of ‘dominance or submission’ evolved some
120 million years ago (Parker, 1984; Price, 1988; Maynard Smith, 1982). Here, confidently opti-
mistic animals acquire influence over meek counterparts via emotionally charged displays driven
by sub-conscious interactions of the paleolimbic systems of the dyad. These emotive behaviors
are mediated by circuits enervated by new mammalian subtypes of neurotransmitter receptors.
The tug and pull in specific individuals affects the balance of neurotransmitters in patterns that
predictably predispose to higher or lower ranges of mood and affect (Wilson, 2002).
 D.R. Wilson / The Journal of Socio-Economics 35 (2006) 626–633 631

Table 2
Summary: dual mode evolutionary epidemiology
Hawk, attractive Dove, avoidant

Neomammalian (“Logistikon”)
Cortex (SAHP)
Sociotropic − cognitive/SAHP Optimistic, charming Pessimistic, ashamed
Cognition > affect Manic/sociopathic Depressed/obsessed
S2 > S1 ∼ D3,4 > D1 S2, D3,4 and NE High S2 Low D3,4 and NE?

Hawk, dominant Dove, submissive

Paleomammalian (“Thimoeides”)
Limbic (RHP)
Acquisative − emotive/RHP Confident, likely to win Unsure, likely to lose
Affect > cognition Aggressive/sadistic Morbid/masochism
S1 > S2, D2,3,4 > D1, +EPS S1, D3,4 and NE High S1, D3,4 and NE Low

Hawk, fighting Dove, fleeing

Reptilian (“Epithimetikon”)
Midbrain (RAB)
Territorial − instinctive/RAB Strident, strong Cowering, weak
Instinct > affect > cognition Violent, solipsistic Fright, abulia
S1  S2  D1  D2,3,4 D1 and NE High S? D1 and NE Low S?

S: serotonin, with subtypes; D: dopamine, with subtypes; NE: norepinephrine; EPS: extrapyramidal symptoms.

Game theory models the Primatohumanoid level in terms of ‘Social Attention Holding Poten-
tial’ (SAHP), as is appropriate for overtly affiliative algorithms of ‘attraction or avoidance’ evolved
over the past 60 million years (Gilbert, 1992; Maynard Smith, 1982). Here, affably charismatic
persons win the esteem of others in whom they inspire confidence. This is via displays that
are social and intellectual as driven by conscious interactions of the limbic and neocortices of
familiars. These rationally creative behaviors are mediated by circuits enervated by the newest
neomammalian, primate and hominoid subtypes of neurotransmitter receptors (e.g., humans have
more than 16 subtypes of receptors for serotonin laid out in highly specific circuits). Here, the
tug and pull in specific individuals alters the balance of such neurotransmitters in patterns that
predictably predispose to higher or lower ranges of sociability, charm and influence (Wilson,
2002).
MacLean’s conceptualization is of a piece with Plato, who also identified a tri-partite system
of archetypal mentation (Hamilton, 1963; Wilson, 1998). Plato’s hierarchy moved from the basest
animal instincts of the Epithimetikon, on to the affiliative yet emotive Thimoeides of more advanced
animals, crowned (in humans alone) by the rational Logistikon (Table 2). Plato, in his metaphor
of the driver, noted that humans struggled with incomplete success to derive behavior from the
Logistikon without undue influence from lower, more emotive and/or reflexive circuits. These
latter circuits may be reined in but are not wholly constrained.

4. Summary

General economics and, in particular, socioeconomics are well-situated to benefit from a con-
certed reconciliation to and integration of knowledge and models accumulating in evolutionary
632 D.R. Wilson / The Journal of Socio-Economics 35 (2006) 626–633

behavioral neuroscience. Opportunities for fertile cross-inquiry between the evolutionary neu-
rosciences and social economics are propitious and active investigations at this extraordinary
interface are long-past due. An early priority may be for economic theory and practice to sys-
tematically invoke the rapidly accumulating evidence from evolutionary neuroscience that makes
clear human social reciprocity results from global state interactions of two essentially opposing
neuromental circuitries, and that these circuitries are the legacy of three different periods of and
neuromental levels in evolution.
This paper is intended to encourage and facilitate such inter-disciplinary work by offering a
heuristic model for the otherwise overwhelming quantity of primary data from the neurobehavioral
and evolutionary sciences, particularly the naturalistic and significantly instinctive or emotive
aspects that facilitate the algorithms of decision-making. To invoke Darwin in his closing of Origin,
from evolution ‘. . . much light will be cast on man. . .’, notably herein human socioeconomic
behavior.

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