Humans are exceedingly social animals, but the neural underpinnings of social cognition
and behavior are not well understood. Studies in humans and other primates have pointed
to several structures that play a key role in guiding social behaviors: the amygdala,
ventromedial frontal cortices, and right somatosensory-related cortex, among others. These
structures appear to mediate between perceptual representations
of socially relevant stimuli, such as the sight of conspecifics, and retrieval of knowledge
(or elicitation of behaviors) that such stimuli can trigger. Current debates concern the
extent to which social cognition draws upon processing specialized for social information,
and the relative contributions made to social cognition by innate and acquired knowledge.
Social cognition refers to the processes that subserve behav- ior in response to conspecifics
(other individuals of the same species), and, in particular, to those higher cognitive
processes subserving the extremely diverse and flexible social behaviors that are seen in
primates. Its evolution arose out of a complex and dynamic interplay between two
opposing factors: on the one hand, groups can provide better security from predators,
better mate choice, and more reliable food; on the other hand, mates and food are available
also to competitors from within the group. An evolutionary approach to social cogni- tion
therefore predicts mechanisms for cooperativity, altruism, and other aspects of prosocial
behavior, as well as mechanisms for coercion, deception and manipulation of conspecifics.
The former are exemplified in the smallest groups, in the bond between mother and infant;
the latter in the largest groups by the creation of complex dominance hierarchies.
It is clear that primates are exceedingly adept at negotiating the social environment. This
ability is most striking in the most social primate, Homo sapiens, suggesting the hypothesis
that our exceptional cognitive skills may be traced back to evolution in an environment in
which there was a premium on social skills. In support of this idea, there is a correlation
between mean group size among various primate species and their neocortex volume
(specifically, the ratio of neo- cortex volume to the rest of the brain1). Such a correlation
has been found also for several other mammals that all feature a complex social structure
(e.g. bats, carnivores and toothed whales) – the larger the social groups, the larger the
brains (relative to body size). Although it has been proposed that brain size correlates with
a number of other factors, including dietary foraging strategy, tool use and longevity2,3, it
might be that large brain size is at least a partial consequence of the fact that primates have
a complex ecological niche with re- spect to social structure (including its effect on food
and mate availability). This hypothesis, variously dubbed the ‘Machiavellian Intelligence
Hypothesis’4 or the ‘Social Brain
Hypothesis’1, depending on what theorists take to be its most salient features, suggests that
the complexity of primate social structure, together with certain of its unique features, such
as cooperativity and deception, led to an advantage for larger brains.
Aside from sheer brain volume, one would of course like to know more about the specific
neural systems that sub- serve various aspects of social cognition. A seminal review5
argued for the importance of the following set of structures: amygdala, temporal cortex,
anterior cingulate cortex, and orbitofrontal cortex6. The neurobiological underpinnings of
social cognition in humans, the topic of this review, are being investigated using various
methods, including lesion studies and functional imaging, and can be situated in the
context of what we know about social cognition from anthropological, comparative and
developmental studies.
An overview of the neurobiology of social cognition in primates Non-human primates Two
sets of findings, one at a macroscopic level, the other at a microscopic level, first
suggested that the primate brain might contain neural systems specialized for processing
socially relevant information. In the 1930s, Kluver and Bucy made large bilateral lesions
in monkey brains, encompassing amygdala, temporal neocortex, and surrounding
structures7. The animals subsequently appeared able to perceive and respond to objects in
their environment, but they behaved inappropriately with respect to the emotional
significance that objects would normally signal. This included a com- pulsive examination
of objects, especially with the mouth, hypersexual behavior, unusual tameness, and a
complete lack of awareness of the emotional significance of stimuli (‘psychic blindness’;
e.g. handling of snakes). Selective neurotoxic lesions of the monkey amygdala result in
more subtle impairments; however they do still appear to impair disproportionately
those behaviors normally elicited by social cues8–10. Although the amygdala is a
heterogeneous collection of nuclei that par- ticipate in several different functional
systems11, at least some of its components thus appear to contribute disproportionately to
social behavior.
The other set of findings that first sparked interest in the neural basis of social cognition
pertains to the level of single neurons. Neurophysiological studies in non-human primates
have shown that single neurons in the monkey inferotemporal cortex respond relatively
selectively to the sight of faces12. Moreover, specific neurons modulate their response
prefer- entially with specific information about faces, such as their identity, social status or
emotional expression13–15. There are also neurons whose responses are modulated by
viewing complex scenes of social interaction16,17, as well as by specific features of faces
that can signal social information, such as gaze direction18. A neural code in which the
responses of individual neurons are tuned relatively selectively to highly specific feature
conjunctions may permit a neuronal ensemble to distinguish among complex, similar
members of a large class of stimuli, such as the faces of conspecifics. Current
information-theoretical approaches are providing more detail on how such socially
relevant information might be encoded in a neuronal population19.
Humans
Human social cognition has received extensive attention from cognitive, developmental
and social psychologists. Some important current issues that might be informed by
findings from cognitive neuroscience concern how social cognitive abilities develop in
infants, and to what extent genetic factors might influence such abilities. Clearly, the
emotional and social development of humans is extraordinarily complex, involving a
multi-factorial interplay between genes, parental behavior, and the influence of culture.
There have been two major sets of studies that first argued for neural systems critical to
social cognition in humans: social impairments following damage to the frontal lobe, and,
more recently, social impairments in subjects with autism. The observation that the frontal
lobes can contribute relatively specifically to behavior in the social domain was first made
on the basis of a rather horrible accident: the injury of the rail- road worker Phineas
Gage20. Gage received a large bilateral lesion of his frontal lobe, including the
ventromedial prefrontal cortex, from an accidental explosion that shot a metal rod through
his head (see Fig. 1 for neuroanatomical structures highlighted in this review). Whereas
Gage had been a diligent, reliable, polite and socially adept person before his accident, he
subsequently became uncaring, profane, and socially in- appropriate in his conduct. This
change in his personality remained a mystery until it could be interpreted in the light of
similar patients in modern times: like Gage, other subjects with bilateral damage to the
ventromedial frontal lobes show a severely impaired ability to function in society, despite
an entirely normal profile on standard neuropsychological meas- ures, such as IQ,
language, perception and memory. Recent theoretical explanations propose that the
ventromedial frontal cortices play an important role in associating emotional experi- ence
with decision making in complex situations, especially perhaps situations in the social
domain (see below).
Box 1. Social cognition, modularity and innateness
Focal brain damage can result in impaired processing that is limited to highly specific
categories. For instance, patients have been reported who are specifically unable to
recognize, or to name, tools, animals, people, or a variety of other selective categories.
There is thus very strong evidence that categories are, in some sense, mapped in the brain
(but in a way that differs from as- pects of objects that are a direct consequence of
topography at the sensory epithelium). While initially surprising, the finding is in fact
predicted from the assumption of a few, very simple, local rules that specify how brains
represent stimuli (Ref. a). In essence, local rules for organizing neural tissue as a function
of activity suffice to generate topographic representations of abstract stimulus categories.
The categories that are abstracted emerge naturally out of the covariances of our
interactions with certain classes of stimuli in the environment. Thus, we typically inter- act
with members of the class of animals in a similar way; that is, the similarity is greater
among animals than it is to how we typically interact with members of the class of tools, or
members of the class of people. Similarity in sensorimotor interaction can thus translate
into functional and anatomical similarity in the brain (Refs b,c).
The above view suggests a strong component of experience and learning in such
self-organized topographic maps. A different explanation comes from the view that there
are innately speci- fied modules in the brain for processing specific categories of
knowledge. The evidence for this latter view is strongest from domains such as language,
and it is the view that has historically been associated with the notion of ‘modularity’ (Ref.
