Are there specialized circuits for social cognition and are theyunique to humans?Matthew FS Rushworth1,2, Rogier B Mars1,2 and Jerome Sallet1
Available online at www.sciencedirect.com
Discussions of the neural underpinnings of social cognition
frequently emphasize the distinctiveness of human social
cognition. Here, however, we review the discovery of similar
correlations between neural networks and social networks in
humans and other primates. We suggest that component parts
of these neural networks in dorsal frontal cortex, anterior
cingulate cortex (ACC), and superior temporal sulcus (STS) are
linked to basic social cognitive processes common to several
primate species including monitoring the actions of others,
assigning importance to others, and orienting behavior toward
or away from others. Changes in activity in other brain regions
occur in tandem with changes in social status and may be
related to the different types of behaviors associated with
variation in social status.
Addresses1 Department of Experimental Psychology, University of Oxford, United
Kingdom2 Oxford Centre for Functional Magnetic Resonance Imaging of the Brain
(FMRIB), University of Oxford, United Kingdom
Corresponding author: Rushworth, Matthew FS
Current Opinion in Neurobiology 2013, 23:436–442
This review comes from a themed issue on Social and emotional
neuroscience
Edited by Ralph Adolphs and David Anderson
For a complete overview see the Issue and the Editorial
Available online 2nd January 2013
0959-4388/$ – see front matter, # 2012 Elsevier Ltd. All rights
reserved.
http://dx.doi.org/10.1016/j.conb.2012.11.013
Social networks and primate brainmorphologyHumans have big brains but there is disagreement about
why they do and about the way in which their brains
might be special [1]. Some neuroanatomical features,
such as a granular prefrontal cortex, are shared with other
primates but not with any other mammals and may reflect
the complexity of the foraging decisions faced by many
diurnal primates [2��,3]. However, it is also possible that
large brain size reflects the complexity of primate, and
especially human, social environments [4]. It is even
argued that some neural processes associated with social
cognition are exclusively human [5].
A precondition for the ‘social brain hypothesis’ is that
skill in navigating social networks impacts on individual
Current Opinion in Neurobiology 2013, 23:436–442
fitness and this is indeed the case. Male macaques
father more offspring when they are in dominant
social positions [6]. Furthermore, getting to the top
of the hierarchy is not simply a matter of brute strength
and aggression. Social skills are important too. The
ability to form coalitions is a predictor of dominance
and this in turn is predicted by the ability to form
pair bonds [6]. Some personality traits akin to friendli-
ness also play a role in the structure of a social network
[7].
The original social brain hypothesis was supported by
comparative studies of whole brain or cortex volumes
[3] but there is now evidence that a specific neural
network covaries with complexity of social networks.
There is more gray matter in amygdala, ventromedial
prefrontal cortex, anterior cingulate cortex (ACC), and
the temporal lobe, including the superior temporal
sulcus (STS), in people with larger social networks
[8��,9��,10].
Social networks and brain networks: thedirection of cause and effectIt seems intuitive to think that individual differences in
neuroanatomy determine individual differences in
social networks. However, the alternative hypothesis,
that cause and effect may occur in the converse
direction, should be considered. Sensorimotor gray
matter, white matter, and activity all change as sensor-
imotor skills are learned [11,12,13��] and so the same
may hold in the social domain. Many experimental
sensorimotor learning manipulations take place for only
a limited period of an hour or less per day albeit for
several weeks or a month. By contrast, for many
primates, the social network is experienced almost
constantly.
Sallet et al. [14] took advantage of a research institute’s
attempt to group-house all the macaques in its colony and
obtained MRI scans of 22 macaques living in groups of
between one and seven individuals. Gray matter in STS,
amygdala, and dorsal and anterior prefrontal cortex was
correlated with social network size [14] (Figure 1). In
these studies the macaques could not determine their
own social group sizes. Instead they were housed in a
group because they were being used in the same research
project. In such a setting it seems more parsimonious to
conclude that social network experience has an impact on
neuroanatomy.
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Are there specialized circuits for social cognition and are they unique to humans? Rushworth, Mars and Sallet 437
Figure 1
STS
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(a) Gray matter in macaque mid-STS correlates positively with social network size. The x and y values correspond to coordinates expressed in mm
within the MNI macaque rhesus template place. (b) Resting state functional connectivity in a network that includes this mid-STS region and a cluster in
the anterior cingulate gyrus (in green) is stronger in macaques living in a larger social group. (c) The human posterior temporo-parietal junction area (in
green) has a similar functional connectivity profile as the macaque mid-STS.
Data redrawn from [14,17�,23] with permission.
It has been argued that assignment of individuals to
groups would have had to reflect an individual maca-
que’s prior inclination to sociability [15]. However,
while it seems plausible that a very antisocial individual
might be housed alone, or in a pair with a more docile
individual where it might be more easily managed, it
does not seem plausible that pairs of the most aggres-
sive animals would be housed together (and then the
next most aggressive animals identified and housed in a
trio, and so on). In other words, it seems unlikely that
predisposition to sociability would have a simple
relationship with group size and therefore that it is
unlikely to have driven the results. Moreover, Sallet
and colleagues were able to show that the brain-social
network correlations they found still held even when
the monkeys that were housed singly or in pairs were
excluded from the analysis.
Beyond morphology: relating neural activity tosocial network sizeIt is not just gray matter that is correlated with
social network size but also brain activity measured
with functional MRI (fMRI) [14,16]. Spontaneous
coupling of activity between STS and dorsal prefrontal
cortex and ACC increased with social group size
[14,17�]. Activity in these areas, and interactions be-
tween them, may be occurring more frequently
when animals are in larger social groups because they
have to make and adjust more predictions about what
their cage mates, and groups of their cage mates,
will do. We explain below how some of these brain
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areas may be involved in orienting behavior toward
other individuals and in tracking and predicting their
behavior.
In summary, there is evidence that brain structure and
activity covary with social network size in both humans
and macaques. The covarying brain areas are therefore
likely to mediate skills important for social life. Although
some social skills might be uniquely human, for example
‘Theory of Mind’ — the inferring of another’s beliefs and
intentions [18��], there are likely to be other more basic
social skills that are possessed by a range of primates. The
next sections outline basic social cognitive processes that
might be common to humans and macaques and depend
on at least partially shared neural systems identified in the
social network experiments.
Social skills for life in a complex socialnetwork: the amygdala and the posterior STSA large body of work has underlined the importance of the
amygdala in emotional responsiveness in humans and
macaques [19,20]. If one of its functions is to link stimuli
to innate behaviors and autonomic responses then it is not
surprising that altered social interaction patterns follow
amygdala lesions [21]. In macaques the effects of amyg-
dala lesions are greater when they occur earlier in de-
velopment [22]. By contrast the impact of early lesions in
other brain areas (on other cognitive domains) is less.
It has been debated whether the posterior STS region
linked to social network size [10] is a region especially
Current Opinion in Neurobiology 2013, 23:436–442
438 Social and emotional neuroscience
concerned with social cognition or a region with a more
general role in attentional control [5]. Mars and colleagues
[23] used diffusion weighted imaging (DWI)-based par-
cellation techniques to show that the temporo-parietal
junction (TPJ) area in which the posterior STS is situated
could be divided into two component parts and that each
region was associated with different patterns of coupling
with activity in other brain areas while subjects are at rest.
In other studies such inter-regional differences in resting
state connectivity have been linked in part to underlying
differences in anatomical connections [24]. The activity
coupling patterns of the most posterior part of the STS
suggest that it was connected to the medial frontal and
ACC areas that have also been linked to social cognition
[19,25,26,27��,28] (Figure 1). While most social cognition-
related activity is reported in posterior STS more anterior
TPJ activity was linked to attentional control.
The exact contribution posterior STS makes to social
cognition remains unclear. A theme emerging from
diverse experimental approaches is that it is concerned
with determining the degree to which behavior is
oriented in a social direction. Gray matter in this region
covaried with predisposition to make altruistic choices (as
opposed to selfish choices) and its activity was predictive
of altruistic choices [29��]. Noninvasive stimulation
experiments also emphasize its importance when there
is a conflict between socially and nonsocially oriented
behavior [30��].
A second controversy clouding interpretation of
posterior STS function is how, indeed whether, it is
related to the STS region covarying with social group
size in macaques. The macaque STS region is certainly
responsive to stimuli of social significance such as faces
and bodies [31]. However, it has been argued that the
macaque STS face responsive region is homologous to
the human face selective region in lateral fusiform
gyrus [32]. On the other hand, there is evidence that
the human posterior STS responds to faces and that it
does so in a manner reminiscent of macaque STS [33].
It is possible that the face responsive region in macaque
bears a relationship with both human posterior STS and
fusiform gyrus. Other regions in macaque, such as the
lateral intraparietal area, appear related to a set of areas,
perhaps relatively specialized ones, rather than a single
area in humans [24]. This would suggest that the
human posterior STS and fusiform gyrus once had a
common origin but have become specialized, separated,
and divided by expansion of auditory association and
language areas.
Frontal and anterior cingulate cortex: socialpredictions and interestIn contrast to STS, surprisingly clear relationships can be
established between frontal and cingulate brain regions
linked to social network size in humans and macaques.
Current Opinion in Neurobiology 2013, 23:436–442
The macaque ACC region linked to social network size is
in the gyral areas 24a and 24b dorsal and anterior to the
corpus callosum [14] and a region with probably similar
connections can be identified in humans [34]. Lesions of
ACC, but not other frontal areas, disrupt the pattern of
interest that macaques take in others as a function of
social rank and sex [28,35]. At the same time, some
cognitive processes, such as linking of stimuli to reward
outcomes, that are impaired by lesions to other brain
areas, such as amygdala and orbitofrontal cortex (OFC),
remain intact. Activity in the human gyral ACC tracks the
weight of interest assigned to another social agent but not
that assigned to comparable nonsocial variables [26].
Activity is diminished when less weight is given to some
types of social feedback under oxytocin administration
[36]. Little is known about activity of individual neurons
in this part of ACC in primates. There are, however,
similarities between it and rodent ACC. ACC lesions in
rats disrupt patterns of interest in other rats [37]. Rat ACC
neurons are responsive to impending social challenges
that impact on decision making [38��] and variation in
synaptic inputs in a similar region in mice is related to
dominance [39��]. The ACC’s involvement in social
cognition may, therefore, not be limited to primates
but a feature of many mammals.
Two of the other regions linked to social network size in
the macaque are dorsal prefrontal convexity area 9 and a
region in or near the frontal polar area 10 [14]. In humans,
gray matter in similar regions is correlated with social
network size and individual differences in ability to
engage in Theory of Mind [10]. The resting state activity
in these two regions is coupled with activity in the
temporal pole and amygdala but, unlike most dorsal
prefrontal areas, activity is uncoupled with that through-
out parietal cortex. Such a pattern reflects the known
connectivity of these regions and is similar to the
coupling patterns of dorsomedial prefrontal areas 9 and
10 in humans (Sallet J, Mars RB, Noonan MP, Jbabdi S,
O’Reilly J, Filippini N, Rushworth MF: The organiz-ation of dorsal prefrontal cortex in humans and maca-ques, submitted for publication). In other words, there
are similarities between these macaque brain regions and
human brain regions that have been linked to Theory of
Mind. There has been no other investigation yet to test
whether these brain regions in macaques are concerned
with social cognition. It should, however, be noted that,
despite repeated testing, it has been difficult to demon-
strate they are concerned with the same general aspects
of decision making, cognitive control, and memory as
more lateral prefrontal regions [40,41].
Macaques have failed most of the Theory of Mind tasks
they have been set [42]. But while this means that they
may not track other agents’ beliefs, especially when they
run counter to reality, it does not mean that they do
not track and predict other aspects of the behavior of
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Are there specialized circuits for social cognition and are they unique to humans? Rushworth, Mars and Sallet 439
Figure 2
(a)Partner’s erroneous choicesPartner’s correct choices
Partner’s erroneous choicesPartner’s correct choices
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Current Opinion in Neurobiology
Yoshida et al. [43,44] trained pairs of monkeys to choose between yellow or green buttons. One monkey made the responses and the other watched
and then after two trials the roles of observer and responder were reversed. One of the two buttons was designated as the correct one for several trials
in a row and then the other color button became the correct response. By watching the other monkey’s actions an observer monkey could ascertain
which rule, yellow or green button pressing, was in place and could respond accordingly on the first trial after role reversal. Two errors were identified
in responder monkeys. In type 1 errors the monkey made the wrong response: a response that was inconsistent with all the other previous responses
that had recently been rewarded in that block. In type 2 errors, however, the monkey made a response that was appropriate given the reward
assignment in the recent block but the response was incorrect because a reward contingency switch had been implemented by the experimenter.
Some neurons in the medial frontal cortex in the presupplementary motor area and more anterior dorsomedial prefrontal cortex responded only to
errors made by the partner. The figures show the activity of the neurons in responses to type 2 events on which no reward was delivered. The neurons
are divided into two groups. (a) Population activity for partner-error neurons with significant responses to type 2 no reward (n = 46). (b) Population
activity for partner-error neurons without significant responses to type 2 no reward (n = 51). The displays are aligned at the time of target button
pressing (left) and the onset of reward feedback (right). (c) Spatial distribution of partner-error neurons with or without significant responses to type 2
no reward (left hemispheres). The size of each filled circle is proportional to the number of neurons at each site. Green arrows indicate the
physiologically defined border between the SMA and the pre-SMA. The inset shows the top view of the left frontal lobe (left) and a coronal section
(right) cut through the broken line. CgS, cingulate sulcus. Light colors indicate all of the partner-error neurons and dark colors indicate partner-error
neurons exhibiting significant responses to type 2 no reward.
other monkeys. In fact macaques appear to monitor the
actions that are chosen by another macaque and the
consequences of the actions [43,44]. Moreover they
predict the consequences that will ensue from an action
and on the basis of their observations they select their
own subsequent actions so that they maximize their
chances of obtaining food rewards [43,44]. A class of
neurons in macaque dorsomedial frontal cortex, including
the presupplementary area, responds preferentially to the
actions that another macaque makes rather than their own
actions [43,44] (Figure 2). Many of the same neurons
differentiate between another macaque’s actions that
were unsuccessful, because the circumstances changed,
and actions that were unsuccessful because the other
macaque did not make the best choice given the circum-
stances. The macaques adjusted their own subsequent
actions in different ways after these two types of obser-
vations. There is also activity in human dorsomedial
prefrontal cortex that reflects expectations about what
an observed person will do and errors in such predictions
[45,46].
Brain changes related to social dominanceWe began by discussing how social skills lead to domi-
nant positions in social groups and how this, in turn,
could impact on an individual’s fitness and in the
interim we examined how brain regions that covaried
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with social network size might mediate social skills. It
seems appropriate, therefore, to end by examining the
relationship between the neural correlates of domi-
nance and brain areas linked to social cognition. Using
techniques similar to those exploited in the social
network study by Sallet et al. [14], Noonan and col-
leagues showed that gray matter in, and activity
coupling across, a set of subcortical regions including
the oxytocin sensitive bed nucleus of the stria termi-
nalis/medial septum, hypothalamus, dopaminergic mid-
brain nuclei, and, in the cortex, OFC is correlated with
dominance in macaques. These changes were unrelated
to social network size. However, coupling between
parts of this neural network and the STS and prefrontal
regions previously linked with social network size did
change with dominance. It is possible that individual
differences in the STS–prefrontal network confer some
macaques with greater social skills that in turn lead to
dominance but that the resulting status is linked to the
distributed subcortical–OFC network. In this network
gray matter and activity coupling are only related to
dominance and not social group size. It is certainly the
case that OFC neurons encode the dominance status of
others [47] and aspects of behavior that depend on
relative dominance status [48] (Figure 3) while other
parts of this network are sensitive to oxytocin which
also alters similar behaviors [49��].
Current Opinion in Neurobiology 2013, 23:436–442
440 Social and emotional neuroscience
Figure 3
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Current Opinion in Neurobiology
Macaques have a social rank that is correlated with different patterns of behavior. More dominant animals are more likely to make prosocial choices, in
other words to make choices that allow other individuals access to food rewards [50]. The OFC may be important in such behavior because neurons there
encode both information about social status and how the values of rewards change when other macaques also receive simultaneous rewards. Watson and
colleagues [47] taught macaques to choose between making saccades to two targets to receive a juice reward or to see a stimulus of social interest (a
photograph of another macaque) accompanied by a smaller juice reward. (a) The percentage of recorded neurons with firing rates significantly modulated
by social image category (black bar), fluid amount (gray bar), or their interaction (white bar) for three different monkeys. The number of neurons modulated
by social image is significantly larger than that modulated by fluid or their interaction for all three monkeys. (b) A representative neuron with firing
significantly modulated by social image category (left), but not by fluid reward magnitude (right). (c) Azzi et al. [48] taught macaques to fixate visual cues
that were associated with different amounts of reward. In a nonsocial condition the cues indicated different amounts of juice (top row on left hand side) and
responses from an example neuron are shown that increased its firing rate as the reward size increased. Activity on the right is from the same neuron but in
a social task in which the cues indicated a consistent amount of reward for the experimental macaque (drops of juice for the experimental macaque are
indicated by drop symbol and the letter A) in all three cases but different amounts of reward for a partner macaque, P1. Increasing rewards for the partner
macaque led to a decrease in activity in the neuron that paralleled a behavioral preference for selfish reward for just the experimental macaque. (d)
Normalized spike density curves and mean discharge rate for the neuron population from which the corresponding single-unit examples are drawn. The
thick horizontal bar below the spike density curves indicates the time window used for computing all statistical tests on mean population activity (right). The
asterisks and thin black or blue horizontal lines indicate significant pair-wise comparisons (P < 0.01).
Current Opinion in Neurobiology 2013, 23:436–442 www.sciencedirect.com
Are there specialized circuits for social cognition and are they unique to humans? Rushworth, Mars and Sallet 441
ConclusionsAlthough the unique features of human social cognition
are often emphasized they may depend on more funda-
mental social cognitive processes present in other
primates and sometimes even in other mammals. Some
brain areas linked to social cognition and social status are
important for other aspects of behavior but some appear
relatively specialized for social cognition in both humans
and macaques.
AcknowledgementFunded by the MRC.
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� of special interest
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