Social Decision-Making and the Brain: A Comparative Perspective

doi:10.1016/j.tics.2017.01.007

Trends in Cognitive Sciences

Volume 21, Issue 4, April 2017, Pages 265-276

https://doi.org/10.1016/j.tics.2017.01.007 Get rights and content

Trends

Evidence converging from several animal models of social interactions offers an unprecedented view of the brain areas and networks involved in social cognition.

Experimental manipulation of social brain networks in human and nonhuman animals offers new causal insights that go beyond mere correlation between brain and social behavior.

Neuropeptides, such as oxytocin, offer great promise as modulators of social behavior in humans. However, experts ask for cautious interpretation of the literature in humans and request more research in nonhuman primates.

Behavioral and neurobiological investigations of social behavior across species are beginning to reveal more continuity between humans and other animals than ever before imagined.

The capacity and motivation to be social is a key component of the human adaptive behavioral repertoire. Recent research has identified social behaviors remarkably similar to our own in other animals, including empathy, consolation, cooperation, and strategic deception. Moreover, neurobiological studies in humans, nonhuman primates, and rodents have identified shared brain structures (the so-called ‘social brain’) apparently specialized to mediate such functions. Neuromodulators may regulate social interactions by ‘tuning’ the social brain, with important implications for treating social impairments. Here, we survey recent findings in social neuroscience from a comparative perspective, and conclude that the very social behaviors that make us human emerge from mechanisms shared widely with other animals, as well as some that appear to be unique to humans and other primates.

Section snippets

The Human ‘Social Brain’

Consider the following common scenario (Figure 1): you step into a busy outdoor market on a Saturday afternoon to purchase some fresh fruit from a local farmer. You are looking for a particular vendor with whom you have done business before, and whom you know is open to concede some discounts if you buy a lot of fruit. Upon arrival, you notice that the vendor is in a bad mood and that his fruits are not particularly appealing. You vacillate between bargaining with him for a lower price and

Deep Homology in the Social Brain

Choosing with whom to compete, with whom to mate, and with whom to cooperate are critical decisions for many animals that strongly impact survival and reproductive success 19, 20. Selective pressure on neural circuits supporting social behavior may generate similar solutions based on either convergence in the absence of shared ancestry [21] or elaboration of traits shared by common descent [22]. Homology is defined as shared ancestry in traits between different species. Deep homology extends

Primate Specializations in Social Behavior and Cognition

Despite growing evidence for deep homologies in biology and social behavior across vertebrates, many of our most complex, flexible, visually guided, and strategic social behaviors appear to be restricted to other primates [54]. For most primates, social bonds are crucial, shaping the reproductive success of males [55], females [56], and offspring [57]. Variation in social skills among human primates 58, 59 and nonhuman primates 60, 61 is directly related to observable variation in brain

Translational Applications

Ultimately, furthering our basic understanding of the social brain will provide new targets and opportunities to treat humans with social impairments. Research across several species of mammals has identified a highly conserved social modulator in the neuropeptide OT, provoking a recent surge of excitement about its therapeutic potential (Figure 3) [88]. Numerous studies have found that intranasal administration of OT (IN-OT) enhanced a range of complex social cognitive processes in both

Concluding Remarks

Social neuroscience is still in its infancy (see Outstanding Questions). Despite this early stage, groundwork has been laid for a basic framework in which different brain areas and circuits contribute selectively to the perception, recognition, selection, and recall of socially relevant information. Insights from research conducted in various species, including humans, has highlighted significant convergence in the neuroanatomy and neurophysiology of these brain circuits, as well as in the

Acknowledgments

This work was supported by a grant from the Simons Foundation (SFARI 304935, to M.L.P.) and the National Institutes of Health (R21 MH106772, R01 NS088674, U19 MH108206, R37 MH109728, R01 MH108627 and R01 MH095894). We would also like to thank Valentine Dubois for producing the artwork in Figure 1.

Glossary

Blood-oxygen-level dependent (BOLD) imaging: a non-invasive functional neuroimaging method that maps the flow of deoxygenated hemoglobin molecules in small blood vessels across the brain. This hemodynamic response is associated with single neuron spiking and dendritic potentials averaged over large volumes of tissue (voxels), each containing hundreds of thousands of cells often with different physiological properties.
Dictator game: an economic game in which one participant, called the dictator, is

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Trends in Cognitive Sciences

ReviewSocial Decision-Making and the Brain: A Comparative Perspective

Trends

Section snippets

The Human ‘Social Brain’

Deep Homology in the Social Brain

Primate Specializations in Social Behavior and Cognition

Translational Applications

Concluding Remarks

Acknowledgments

Glossary

Neuroimage

Current Opinion in Neurobiology

Neuron

Neuron

Neuron

Neuron

Current Opinion in Behavioral Sciences

Trends Ecol. Evol. (Amst.)

Neuron

Behav. Brain Res.

Trends Neurosci.

Trends Neurosci.

Anim Behav

Cell

Biol. Psychiatry

Biol. Psychiatry

Biol. Psychiatry

Biol. Psychiatry

Neuron

Curr Biol

Curr Biol

Curr Biol

Neuroimage

Current Biology

Current Opinion in Neurobiology

Current Biology

Curr Biol

Anim Behav

Trends Cogn. Sci. (Regul. Ed.)

Cell

Neuron

Trends Cogn. Sci. (Regul. Ed.)

Psychoneuroendocrinology

Biol. Psychiatry

Hormones and Behavior

Brain Res

Biol. Psychiatry

The computation of social behavior

Science

A cortical region consisting entirely of face-selective cells

Science

Neural mechanisms of belief inference during cooperative games

J Neurosci

Neural correlates of depth of strategic reasoning in medial prefrontal cortex

Proceedings of the National Academy of Sciences

A distinct role of the temporal-parietal junction in predicting socially guided decisions

Science

A neural mechanism of strategic social choice under sanction-induced norm compliance

eNeuro

The neurobiology of rewards and values in social decision making

Nat Rev Neurosci

A common mechanism underlying food choice and social decisions

PLoS Comput Biol

Normalization is a general neural mechanism for context-dependent decision making

Proceedings of the National Academy of Sciences

Social and monetary reward learning engage overlapping neural substrates

Social Cognitive and Affective Neuroscience

Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry

Nature

All that glitters is not reward signal

Nature Neuroscience

On optimal decision-making in brains and social insect colonies

J R Soc Interface

Review
Social Decision-Making and the Brain: A Comparative Perspective