Adaptations for social cognition in the primate brain

Studies of the factors affecting reproductive success in group-living monkeys have traditionally focused on competitive traits, like the acquisition of high dominance rank. Recent research, however, indicates that the ability to form cooperative social bonds has an equally strong effect on fitness. Two implications follow. First, strong social bonds make individuals' fitness interdependent and the ‘free-rider’ problem disappears. Second, individuals must make adaptive choices that balance competition and cooperation—often with the same partners. The proximate mechanisms underlying these behaviours are only just beginning to be understood. Recent results from cognitive and systems neuroscience provide us some evidence that many social and non-social decisions are mediated ultimately by abstract, domain-general neural mechanisms. However, other populations of neurons in the orbitofrontal cortex, striatum, amygdala and parietal cortex specifically encode the type, importance and value of social information. Whether these specialized populations of neurons arise by selection or through developmental plasticity in response to the challenges of social life remains unknown. Many brain areas are homologous and show similar patterns of activity in human and non-human primates. In both groups, cortical activity is modulated by hormones like oxytocin and by the action of certain genes that may affect individual differences in behaviour. Taken together, results suggest that differences in cooperation between the two groups are a matter of degree rather than constituting a fundamental, qualitative distinction.

[1]  Benjamin Y Hayden,et al.  Economic principles motivating social attention in humans , 2007, Proceedings of the Royal Society B: Biological Sciences.

[2]  A. Kling,et al.  Amygdalectomy and social behavior in the caged stump-tailed macaque (Macaca speciosa). , 1971, Folia primatologica; international journal of primatology.

[3]  Kevin E. Langergraber,et al.  Food sharing is linked to urinary oxytocin levels and bonding in related and unrelated wild chimpanzees , 2014, Proceedings of the Royal Society B: Biological Sciences.

[4]  O. Schülke,et al.  Coalition formation among Barbary macaque males: the influence of scramble competition , 2010, Animal Behaviour.

[5]  R. Stoop Neuromodulation by Oxytocin and Vasopressin , 2012, Neuron.

[6]  Barbara Taborsky,et al.  Social competence: an evolutionary approach. , 2012, Trends in ecology & evolution.

[7]  P. Whitten,et al.  The effect of new alpha males on female stress in free-ranging baboons , 2005, Animal Behaviour.

[8]  R. Seyfarth,et al.  The evolutionary origins of friendship. , 2012, Annual review of psychology.

[9]  Carol Carter Porges Neuroendocrine perspectives on social attachment and love , 1998 .

[10]  D. Amaral,et al.  Amygdalectomy and responsiveness to novelty in rhesus monkeys (Macaca mulatta): generality and individual consistency of effects. , 2006, Emotion.

[11]  M. Chance,et al.  Social behaviour and primate evolution. , 1988 .

[12]  Zuoxin Wang,et al.  Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles , 2003, Neuroscience.

[13]  Stephen V. Shepherd,et al.  Following Gaze: Gaze-Following Behavior as a Window into Social Cognition , 2010, Front. Integr. Neurosci..

[14]  M. Shadlen,et al.  Neurology: An awakening , 2007, Nature.

[15]  R. Wittig,et al.  Focused grooming networks and stress alleviation in wild female baboons , 2008, Hormones and Behavior.

[16]  Anna S. Mitchell,et al.  A Neural Circuit Covarying with Social Hierarchy in Macaques , 2014, PLoS biology.

[17]  J. Silk,et al.  The benefits of social capital: close social bonds among female baboons enhance offspring survival , 2009, Proceedings of the Royal Society B: Biological Sciences.

[18]  Michael L. Platt,et al.  Social Signals in Primate Orbitofrontal Cortex , 2012, Current Biology.

[19]  Robin I. M. Dunbar,et al.  Orbital prefrontal cortex volume predicts social network size: an imaging study of individual differences in humans , 2012, Proceedings of the Royal Society B: Biological Sciences.

[20]  P. Whitten,et al.  Behavioural and hormonal responses to predation in female chacma baboons (Papio hamadryas ursinus) , 2006, Proceedings of the Royal Society B: Biological Sciences.

[21]  K. Nakamura,et al.  The human amygdala plays an important role in gaze monitoring. A PET study. , 1999, Brain : a journal of neurology.

[22]  C. Zink,et al.  Know Your Place: Neural Processing of Social Hierarchy in Humans , 2008, Neuron.

[23]  P. Whitten,et al.  Female hierarchy instability, male immigration and infanticide increase glucocorticoid levels in female chacma baboons , 2006, Animal Behaviour.

[24]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[25]  F. Warneken The Development of Altruistic Behavior: Helping in Children and Chimpanzees , 2013 .

[26]  Fitness benefits of coalitionary aggression in male chimpanzees , 2013, Behavioral Ecology and Sociobiology.

[27]  L. Young,et al.  The neuroanatomical distribution of oxytocin receptor binding and mRNA in the male rhesus macaque (Macaca mulatta) , 2014, Psychoneuroendocrinology.

[28]  A. Sirigu,et al.  Switching brain serotonin with oxytocin , 2014, Proceedings of the National Academy of Sciences.

[29]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[30]  Kevin E. Langergraber,et al.  Urinary oxytocin and social bonding in related and unrelated wild chimpanzees , 2013, Proceedings of the Royal Society B: Biological Sciences.

[31]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[32]  Bennett L. Leventhal,et al.  Association of the oxytocin receptor gene (OXTR) in Caucasian children and adolescents with autism , 2007, Neuroscience Letters.

[33]  S. Semple,et al.  Social capital and physiological stress levels in free-ranging adult female rhesus macaques , 2011, Physiology & Behavior.

[34]  J. Horvath,et al.  Genetic influences on social attention in free-ranging rhesus macaques , 2015, Animal Behaviour.

[35]  Robert M. Seyfarth,et al.  Strong and Consistent Social Bonds Enhance the Longevity of Female Baboons , 2010, Current Biology.

[36]  K. Zuberbühler,et al.  Why mutual helping in most natural systems is neither conflict-free nor based on maximal conflict , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[37]  Lawrence H Snyder,et al.  Reward-Based Decision Signals in Parietal Cortex Are Partially Embodied , 2015, The Journal of Neuroscience.

[38]  B. Hayden,et al.  Distinct Value Signals in Anterior and Posterior Ventromedial Prefrontal Cortex , 2010, The Journal of Neuroscience.

[39]  U. Fischbacher,et al.  Oxytocin Shapes the Neural Circuitry of Trust and Trust Adaptation in Humans , 2008, Neuron.

[40]  Jeanne Altmann,et al.  Social Bonds of Female Baboons Enhance Infant Survival , 2003, Science.

[41]  K. J. Parker,et al.  Plasma oxytocin concentrations and OXTR polymorphisms predict social impairments in children with and without autism spectrum disorder , 2014, Proceedings of the National Academy of Sciences.

[42]  J. Silk,et al.  Evolutionary foundations of human prosocial sentiments , 2011, Proceedings of the National Academy of Sciences.

[43]  A. A. Wijers,et al.  Anxiety, cortisol, and attachment predict plasma oxytocin. , 2007, Psychophysiology.

[44]  M. Tomasello,et al.  The Developmental and Evolutionary Origins of Human Helping and Sharing , 2015 .

[45]  Steve W. C. Chang,et al.  Inhaled oxytocin amplifies both vicarious reinforcement and self reinforcement in rhesus macaques (Macaca mulatta) , 2012, Proceedings of the National Academy of Sciences.

[46]  R. B. Ebitz,et al.  Oxytocin blunts social vigilance in the rhesus macaque , 2013, Proceedings of the National Academy of Sciences.

[47]  D. Amaral,et al.  The Development of Social Behavior Following Neonatal Amygdala Lesions in Rhesus Monkeys , 2004, Journal of Cognitive Neuroscience.

[48]  J. Silk,et al.  Stability of partner choice among female baboons , 2012, Animal Behaviour.

[49]  R. Wittig,et al.  Kin-mediated reconciliation substitutes for direct reconciliation in female baboons , 2007, Proceedings of the Royal Society B: Biological Sciences.

[50]  R Saxe,et al.  People thinking about thinking people The role of the temporo-parietal junction in “theory of mind” , 2003, NeuroImage.

[51]  J. Silk,et al.  Evidence for intrasexual selection in wild female baboons , 2012, Animal Behaviour.

[52]  M. Sanchez,et al.  The impact of early adverse care on HPA axis development: Nonhuman primate models , 2006, Hormones and Behavior.

[53]  R. Seyfarth,et al.  Chapter 1 Stress and Coping Mechanisms in Female Primates , 2009 .

[54]  F. Champagne Early environments, glucocorticoid receptors, and behavioral epigenetics. , 2013, Behavioral neuroscience.

[55]  J. Silk,et al.  Social bonds in female baboons: the interaction between personality, kinship and rank , 2014, Animal Behaviour.

[56]  R. Adolphs,et al.  The social brain: neural basis of social knowledge. , 2009, Annual review of psychology.

[57]  M. Chance,et al.  Attention Structure as the Basis of Primate Rank Orders , 1967 .

[58]  J. Silk The Strategic Dynamics of Cooperation in Primate Groups , 2007 .

[59]  R. Seyfarth,et al.  Stress and Coping Mechanisms in Female Primates , 2009 .

[60]  J. Altmann,et al.  Social environment influences the relationship between genotype and gene expression in wild baboons , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[61]  Bradford C. Dickerson,et al.  Amygdala Volume and Social Network Size in Humans , 2010, Nature Neuroscience.

[62]  Katherine A. Cronin,et al.  Variation in oxytocin is related to variation in affiliative behavior in monogamous, pairbonded tamarins , 2010, Hormones and Behavior.

[63]  N. Bolger,et al.  Social effects of oxytocin in humans: context and person matter , 2011, Trends in Cognitive Sciences.

[64]  M. Platt,et al.  Neural Correlates of Social Target Value in Macaque Parietal Cortex , 2008, Current Biology.

[65]  U. Fischbacher,et al.  Oxytocin increases trust in humans , 2005, Nature.

[66]  P. Brown,et al.  Modulation by dopamine of human basal ganglia involvement in feedback control of movement , 2007, Current Biology.

[67]  L. Young,et al.  Neuroanatomical distribution of oxytocin and vasopressin 1a receptors in the socially monogamous coppery titi monkey (Callicebus cupreus) , 2014, Neuroscience.

[68]  Michael L. Platt,et al.  Social Information Signaling by Neurons in Primate Striatum , 2013, Current Biology.

[69]  Steve W. C. Chang,et al.  Vicarious Reinforcement in Rhesus Macaques (Macaca Mulatta) , 2011, Front. Neurosci..

[70]  Michael L. Platt,et al.  Genetic origins of social networks in rhesus macaques , 2013, Scientific Reports.

[71]  Stephen V. Shepherd,et al.  Reversible inactivation of pSTS suppresses social gaze following in the macaque (Macaca mulatta). , 2014, Social cognitive and affective neuroscience.

[72]  Dino J. Levy,et al.  The root of all value: a neural common currency for choice , 2012, Current Opinion in Neurobiology.

[73]  D. Ariely,et al.  Beautiful Faces Have Variable Reward Value fMRI and Behavioral Evidence , 2001, Neuron.

[74]  R. Seyfarth,et al.  O brother, where art thou? The varying influence of older siblings in rank acquisition by female baboons , 2009, Behavioral Ecology and Sociobiology.

[75]  T. Insel,et al.  Neuroendocrine bases of monogamy , 1998, Trends in Neurosciences.

[76]  M. Bortolini,et al.  Evolutionary pattern in the OXT-OXTR system in primates: Coevolution and positive selection footprints , 2014, Proceedings of the National Academy of Sciences.

[77]  Steve W. C. Chang,et al.  Annals of the New York Academy of Sciences the Neuroethology of Friendship , 2022 .

[78]  John A Updegraff,et al.  Biobehavioral responses to stress in females: tend-and-befriend, not fight-or-flight. , 2000, Psychological review.

[79]  C. Feinstein,et al.  Plasma oxytocin levels in autistic children , 1998, Biological Psychiatry.

[80]  J. Silk,et al.  Factors Affecting Reproduction and Mortality Among Baboons in the Okavango Delta, Botswana , 2004, International Journal of Primatology.

[81]  Christophe Boesch,et al.  Long-term reciprocation of grooming in wild West African chimpanzees , 2009, Proceedings of the Royal Society B: Biological Sciences.

[82]  D. Amaral,et al.  Role of the Primate Amygdala in Fear-Potentiated Startle: Effects of Chronic Lesions in the Rhesus Monkey , 2007, The Journal of Neuroscience.

[83]  M. Behrmann,et al.  Congenital prosopagnosia: face-blind from birth , 2005, Trends in Cognitive Sciences.

[84]  M. Weinstock The long-term behavioural consequences of prenatal stress , 2008, Neuroscience & Biobehavioral Reviews.

[85]  Y. Gilad,et al.  Social environmental effects on gene regulation , 2013, Cellular and Molecular Life Sciences.

[86]  Penelope A. Lewis,et al.  Ventromedial prefrontal volume predicts understanding of others and social network size , 2011, NeuroImage.

[87]  J. Silk,et al.  Variation in personality and fitness in wild female baboons , 2012, Proceedings of the National Academy of Sciences.

[88]  D. Cheney Extent and limits of cooperation in animals , 2011, Proceedings of the National Academy of Sciences.

[89]  Jing Liu,et al.  Positive Association of the Oxytocin Receptor Gene (OXTR) with Autism in the Chinese Han Population , 2005, Biological Psychiatry.

[90]  B. Chapais Rank Maintenance in Female Japanese Macaques: Experimental Evidence for Social Dependency , 1988 .

[91]  M. Platt,et al.  Personality Traits in Rhesus Macaques (Macaca mulatta) Are Heritable but Do Not Predict Reproductive Output , 2013, International Journal of Primatology.

[92]  C. Frith The social brain? , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[93]  R. Seyfarth,et al.  How Monkeys See the World: Inside the Mind of Another Species , 1990 .

[94]  C. Padoa-Schioppa,et al.  Contributions of Orbitofrontal and Lateral Prefrontal Cortices to Economic Choice and the Good-to-Action Transformation , 2014, Neuron.

[95]  Jerome Sallet,et al.  Are there specialized circuits for social cognition and are they unique to humans? , 2013, Current Opinion in Neurobiology.

[96]  J L Andersson,et al.  Social Network Size Affects Neural Circuits in Macaques , 2011, Science.

[97]  T. Bergman,et al.  Concessions of an alpha male? Cooperative defence and shared reproduction in multi-male primate groups , 2012, Proceedings of the Royal Society B: Biological Sciences.

[98]  Michael L. Platt,et al.  Neuroethology of primate social behavior , 2013, Proceedings of the National Academy of Sciences.

[99]  J. Mitani,et al.  Male chimpanzees form enduring and equitable social bonds , 2009, Animal Behaviour.

[100]  J. Bernardo MATERNAL EFFECTS IN ANIMAL ECOLOGY , 1996 .

[101]  Klaus Zuberbühler,et al.  Triadic social interactions operate across time: a field experiment with wild chimpanzees , 2014, Proceedings of the Royal Society B: Biological Sciences.

[102]  G. Fishell,et al.  Oxytocin enhancement of CA1 spike transmission by modulation of fast-spiking interneurons , 2013, Nature.

[103]  John M. Pearson,et al.  Decision Making: The Neuroethological Turn , 2014, Neuron.

[104]  R. Seyfarth,et al.  Social cognition , 2015, Animal Behaviour.

[105]  E. Hollander,et al.  The neuroscience of affiliation: Forging links between basic and clinical research on neuropeptides and social behavior , 2006, Hormones and Behavior.

[106]  Amygdala: Eyes Wide Open , 2014, Current Biology.

[107]  M. Heistermann,et al.  Low female stress hormone levels are predicted by same- or opposite-sex sociality depending on season in wild Assamese macaques , 2014, Psychoneuroendocrinology.

[108]  L. Young,et al.  The neurobiology of pair bonding , 2004, Nature Neuroscience.

[109]  J. Altmann,et al.  Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons , 2014, Proceedings of the Royal Society B: Biological Sciences.

[110]  Margaret Wilson,et al.  Six views of embodied cognition , 2002, Psychonomic bulletin & review.

[111]  Katalin M. Gothard,et al.  Neurons in the Monkey Amygdala Detect Eye Contact during Naturalistic Social Interactions , 2014, Current Biology.

[112]  S. Schanberg,et al.  Visual Receptive Fields of Neurons in Inferotemporal Cortex of the Monkey , 2005 .

[113]  Robert O Deaner,et al.  Mirroring of attention by neurons in macaque parietal cortex , 2009, Proceedings of the National Academy of Sciences.

[114]  R. Seyfarth,et al.  Who, me? Can baboons infer the target of vocalizations? , 2006, Animal Behaviour.

[115]  John M. Pearson,et al.  Neuroethology of decision-making , 2012, Current Opinion in Neurobiology.

[116]  D. Kumaran,et al.  The Emergence and Representation of Knowledge about Social and Nonsocial Hierarchies , 2012, Neuron.

[117]  J. Altmann,et al.  Persistence of maternal effects in baboons: Mother's dominance rank at son's conception predicts stress hormone levels in subadult males , 2008, Hormones and Behavior.

[118]  Rui F. Oliveira,et al.  Cooperation in animals: toward a game theory within the framework of social competence , 2015, Current Opinion in Behavioral Sciences.

[119]  Angela Sirigu,et al.  Promoting social behavior with oxytocin in high-functioning autism spectrum disorders , 2010, Proceedings of the National Academy of Sciences.

[120]  R. Seyfarth,et al.  Affiliation, empathy, and the origins of theory of mind , 2013, Proceedings of the National Academy of Sciences.

[121]  D. B. Bender,et al.  Visual properties of neurons in inferotemporal cortex of the Macaque. , 1972, Journal of neurophysiology.

[122]  B. Bahrami,et al.  Online social network size is reflected in human brain structure , 2011, Proceedings of the Royal Society B: Biological Sciences.

[123]  L. Vigilant,et al.  Social Bonds Enhance Reproductive Success in Male Macaques , 2010, Current Biology.

[124]  Michael L. Platt,et al.  Serotonin Transporter Genotype Modulates Social Reward and Punishment in Rhesus Macaques , 2009, PloS one.

[125]  E. Bullmore,et al.  Social intelligence in the normal and autistic brain: an fMRI study , 1999, The European journal of neuroscience.

[126]  Michael L. Platt,et al.  Monkeys Pay Per View: Adaptive Valuation of Social Images by Rhesus Macaques , 2005, Current Biology.

[127]  M. Tomasello,et al.  Understanding and sharing intentions: The origins of cultural cognition , 2005, Behavioral and Brain Sciences.

[128]  R. Collins The awakening. , 1996, Nursing standard (Royal College of Nursing (Great Britain) : 1987).

[129]  Visual preferences for sex and status in female rhesus macaques , 2012, Animal Cognition.

[130]  Michael L. Platt,et al.  Social Attention and the Brain , 2009, Current Biology.

[131]  Jason P. Mitchell,et al.  Response of Dorsomedial Prefrontal Cortex Predicts Altruistic Behavior , 2012, The Journal of Neuroscience.

[132]  Shaul Shalvi,et al.  References and Notes Supporting Online Material Materials and Methods Som Text Figs. S1 to S16 References the Neuropeptide Oxytocin Regulates Parochial Altruism in Intergroup Conflict among Humans , 2022 .

[133]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[134]  James P. Curley,et al.  Epigenetic mechanisms mediating the long-term effects of maternal care on development , 2009, Neuroscience & Biobehavioral Reviews.

[135]  J. C. Meadows The anatomical basis of prosopagnosia , 1974, Journal of neurology, neurosurgery, and psychiatry.

[136]  L. O’Connell,et al.  Evolution of a Vertebrate Social Decision-Making Network , 2012, Science.

[137]  K. Nakayama,et al.  Developmental Prosopagnosia: a Window to Content-specific Face Processing This Review Comes from a Themed Issue on Cognitive Neuroscience Edited Developmental Prosopagnosia and Inferences to Functional Organization Investigating the Architecture of Face Processing through Developmental Prosopagnosia , 2022 .