available online at · complexity of the foraging decisions faced by many diurnal large primates...

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

([email protected])

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


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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mid STS

Current Opinion in Neurobiology

(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


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


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.


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



Figure 2

(a)Partner’s erroneous choicesPartner’s correct choices

Partner’s erroneous choicesPartner’s correct choices

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1 mm 1 mmMidline MidlineButton press Reward feedback Reward feedbackButton press

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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


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��].



Figure 3

(a)

(c)

(d)

(b)

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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


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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http://www.cell.com/current-biology/abstract/S0960-9822%2811%2901455-2#Comments

http://www.cell.com/current-biology/abstract/S0960-9822%2811%2901455-2#Comments


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Rats were given a choice between foraging in different parts of a maze.When the one of the choices entailed competitive foraging in competitionwith another rat then ACC neuron activity was enhanced. Control experi-ments demonstrated that the activity change was not simply due toaltered expecations about either reward or effort in isolation. Suchcompetitive foraging decisions are likely to be common in group livinganimals.

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Inhaled oxytocin causes macaques to make more prosocialchoices when there is no cost to themselves. Macaques were given achoice between an option that led to reward for both themselves andanother macaque or an option that just led to reward for themselves.Oxytocin increased the frequency of the first type of choice. The effectwas specific to a situation in which the prosocial choice entailed no costs.When the choice was between a reward for just themselves and a rewardfor just the other macaque then oxytocin increased the first type ofbehavior.

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