Encoding of social state information by neuronal activities in the macaque caudate nucleus

Social animals adjust their behavior according to social relationships and momentary circumstances. Dominant–submissive relationships modulate, but do not completely determine, their competitive behaviors. For example, a submissive monkey's decision to retrieve food depends not only on the presence of dominant partners but also on their observed behavior. Thus, behavioral expression requires a dynamic evaluation of reward outcome and momentary social states. The neural mechanisms underlying this evaluation remain elusive. The caudate nucleus (CN) plays a pivotal role in representing reward expectation and translating it into action selection. To investigate whether their activities encode social state information, we recorded from CN neurons in monkeys while they performed a competitive food-grab task against a dominant competitor. We found two groups of CN neurons: one primarily responded to reward outcome, while the other primarily tracked the monkey's social state. These social state-dependent neurons showed greater activity when the monkeys freely retrieved food without active challenges from the competitor and reduced activity when the monkeys were in a submissive state due to the competitor's active behavior. These results indicate that different neuronal activities in the CN encode social state information and reward-related information, which may contribute to adjusting competitive behavior in dynamic social contexts.

[1]  A. Cooper,et al.  Predictive Reward Signal of Dopamine Neurons , 2011 .

[2]  Atsushi Iriki,et al.  Social state representation in prefrontal cortex , 2009, Social neuroscience.

[3]  Uri T Eden,et al.  A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. , 2005, Journal of neurophysiology.

[4]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. , 1989, Journal of neurophysiology.

[5]  Atsushi Iriki,et al.  Dynamic Social Adaptation of Motion-Related Neurons in Primate Parietal Cortex , 2007, PloS one.

[6]  Colin Camerer,et al.  Neuroeconomics: decision making and the brain , 2008 .

[7]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[8]  R. Adolphs The neurobiology of social cognition , 2001, Current Opinion in Neurobiology.

[9]  Jonathan D. Cohen,et al.  Imaging valuation models in human choice. , 2006, Annual review of neuroscience.

[10]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[11]  E. Keverne,et al.  Are subordinates always stressed? a comparative analysis of rank differences in cortisol levels among primates , 2003, Hormones and Behavior.

[12]  K. Doya,et al.  The computational neurobiology of learning and reward , 2006, Current Opinion in Neurobiology.

[13]  B. Balleine Reward and decision making in corticobasal ganglia networks , 2007 .

[14]  J. O'Doherty,et al.  Model‐Based fMRI and Its Application to Reward Learning and Decision Making , 2007, Annals of the New York Academy of Sciences.

[15]  Jonathan D. Cohen,et al.  Computational roles for dopamine in behavioural control , 2004, Nature.

[16]  S. Quartz,et al.  Getting to Know You: Reputation and Trust in a Two-Person Economic Exchange , 2005, Science.

[17]  W. Cowan,et al.  Annual Review of Neuroscience , 1995 .

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

[19]  Wolfram Schultz,et al.  Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. , 2003, Journal of neurophysiology.

[20]  A. Sanfey Social Decision-Making : Insights from Game Theory and Neuroscience , 2022 .

[21]  O. Hikosaka,et al.  Neural Correlates of Rewarded and Unrewarded Eye Movements in the Primate Caudate Nucleus , 2003, The Journal of Neuroscience.

[22]  R. Adolphs Cognitive neuroscience: Cognitive neuroscience of human social behaviour , 2003, Nature Reviews Neuroscience.

[23]  J. Grafman,et al.  Human fronto–mesolimbic networks guide decisions about charitable donation , 2006, Proceedings of the National Academy of Sciences.

[24]  O. Hikosaka,et al.  A neural correlate of response bias in monkey caudate nucleus , 2002, Nature.

[25]  Daeyeol Lee Game theory and neural basis of social decision making , 2008, Nature Neuroscience.

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

[27]  H. D. Steklis,et al.  Biochemical and hormonal correlates of dominance and social behavior in all‐male groups of squirrel monkeys (Saimiri sciureus) , 1986, American journal of primatology.

[28]  D. D. de Quervain,et al.  The Neural Basis of Altruistic Punishment , 2004, Science.

[29]  M. Delgado,et al.  Reward‐Related Responses in the Human Striatum , 2007, Annals of the New York Academy of Sciences.

[30]  G. Rizzolatti,et al.  A unifying view of the basis of social cognition , 2004, Trends in Cognitive Sciences.

[31]  A. Maslow,et al.  The Role of Dominance in the Social and Sexual Behavior of Infra-Human Primates: II. An Experimental Determination of the Behavior Syndrome of Dominance , 1936 .

[32]  J. Delgado,et al.  Behavioral inhibition induced by pallidal stimulation in monkeys , 1975, Experimental Neurology.

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

[34]  Niels Birbaumer,et al.  Evidence for a different role of the ventral and dorsal medial prefrontal cortex for social reactive aggression: An interactive fMRI study , 2007, NeuroImage.

[35]  C. Frith,et al.  Functional imaging of ‘theory of mind’ , 2003, Trends in Cognitive Sciences.

[36]  T. Rowell,et al.  Hierarchy in the organization of a captive baboon group. , 1966, Animal behaviour.

[37]  Brian Hare,et al.  Baboon Metaphysics: The Evolution of a Social Mind, Dorothy L. Cheney, Robert M. Seyfarth. University of Chicago Press, Chicago (2007), Pp. x+348. Price $27.50 paperback , 2008 .

[38]  O Hikosaka,et al.  Functional properties of monkey caudate neurons. II. Visual and auditory responses. , 1989, Journal of neurophysiology.

[39]  G. Pagnoni,et al.  A Neural Basis for Social Cooperation , 2002, Neuron.

[40]  R. Hoskins,et al.  Neural Responses to Taxation and Voluntary Giving Reveal Motives for Charitable Donations , 2007 .

[41]  M. Nader,et al.  Effect of social status on striatal dopamine D2 receptor binding characteristics in cynomolgus monkeys assessed with positron emission tomography , 1998, Synapse.

[42]  C. Shively,et al.  Social subordination stress, behavior, and central monoaminergic function in female cynomolgus monkeys , 1998, Biological Psychiatry.

[43]  Jason P. Mitchell,et al.  Special issue: Multiple Perspectives on the Psychological and Neural Bases of Social Cognition , 2006, Brain Research.

[44]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. , 1989, Journal of neurophysiology.

[45]  Matthew F S Rushworth,et al.  The Computation of Social Behavior , 2009, Science.

[46]  N. Sadato,et al.  Processing of Social and Monetary Rewards in the Human Striatum , 2008, Neuron.

[47]  Kae Nakamura,et al.  Basal ganglia orient eyes to reward. , 2006, Journal of neurophysiology.

[48]  R. Saxe Uniquely human social cognition , 2006, Current Opinion in Neurobiology.

[49]  T. Rowell The concept of social dominance. , 1974, Behavioral biology.

[50]  Karl J. Friston,et al.  Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning , 2004, Science.

[51]  M. Delgado,et al.  Perceptions of moral character modulate the neural systems of reward during the trust game , 2005, Nature Neuroscience.

[52]  D. Pandya,et al.  Prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys , 1991, The Journal of comparative neurology.

[53]  H. de Vries,et al.  Dominance and its Behavioral Measures in a Captive Group of Bonobos (Pan paniscus) , 2000, International Journal of Primatology.

[54]  O. Hikosaka,et al.  Correlation of primate caudate neural activity and saccade parameters in reward-oriented behavior. , 2003, Journal of neurophysiology.

[55]  J. Chadwick-Jones Developing a social psychology of monkeys and apes , 1998 .

[56]  Jean Decety,et al.  Social context and perceived agency affects empathy for pain: An event-related fMRI investigation , 2009, NeuroImage.

[57]  R. Sapolsky The Influence of Social Hierarchy on Primate Health , 2005, Science.

[58]  P. Goldman-Rakic,et al.  Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  J. Price,et al.  Prefrontal cortical projections to the striatum in macaque monkeys: Evidence for an organization related to prefrontal networks , 2000, The Journal of comparative neurology.

[60]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[61]  Atsushi Iriki,et al.  Social cognition in premotor and parietal cortex , 2008, Social neuroscience.

[62]  M. Nader,et al.  Social dominance in monkeys: dopamine D2 receptors and cocaine self-administration , 2002, Nature Neuroscience.

[63]  A. Maslow The Role of Dominance in the Social and Sexual Behavior of Infra-Human Primates: I. Observations at Vilas Park Zoo , 1936 .

[64]  Tatsuo K Sato,et al.  Correlated Coding of Motivation and Outcome of Decision by Dopamine Neurons , 2003, The Journal of Neuroscience.

[65]  K. Fernow New York , 1896, American Potato Journal.

[66]  O. Hikosaka,et al.  Role of the basal ganglia in the control of purposive saccadic eye movements. , 2000, Physiological reviews.

[67]  A. Sanfey,et al.  Games in Humans and Non-human Primates: Scanners to Single Units , 2009 .

[68]  A. Graybiel,et al.  Representation of Action Sequence Boundaries by Macaque Prefrontal Cortical Neurons , 2003, Science.

[69]  J. Donoghue,et al.  Collective dynamics in human and monkey sensorimotor cortex: predicting single neuron spikes , 2009, Nature Neuroscience.