The Golden Rule transcends time and culture. Social reciprocity, as implied by the Golden Rule, is a crucial component of normal social interactions. Individuals with psychiatric disorders marked by social deficits often fail to reciprocate normally with others. Although various types of reciprocity have been observed in humans and non-humans, the underlying neural mechanisms remain unknown. An animal model of complex social cognition that could be explored with single-unit recording and pharmacological manipulations of specific groups of neurons will help uncover the neural mechanisms underlying social reciprocity. Here we propose to develop a new social game in interacting dyads of rhesus monkeys. We have previously shown that rhesus monkeys prefer to donate juice rewards to other monkeys when the alternative is to reward neither monkey, but prefer to reward just themselves when the alternative is to share the rewards with others. In the new social game proposed here, the reward-donating (prosocial) and reward-withholding (antisocial) preferences displayed by one monkey could be subsequently reciprocated by the other monkey in a turn-taking fashion. This game will be used to investigate how neurons in the primate prefrontal cortex are involved in the computation of reciprocity during social interactions. We will record neuronal spiking activity from a brain structure in the medial prefrontal cortex called the anterio cingulate gyrus (ACCg), as it contains neurons that signal both the rewards received by oneself and another individual. In particular, we will investigate whether, how, and at what points in time the reciprocity-induced changes in social preferences are reflected in the activity of ACCg neurons. We hypothesize that ACCg activity associated with rewards received by self and others is gain modulated by the reciprocity level across two interacting monkeys. Furthermore, we will examine how the activity in one monkey's brain is dynamically modulated with respect to the neuronal activity in the other's brain during these reciprocal reward exchanges. We hypothesize that the reward outcome signaling by the ACCg is central to reciprocity, endorsing the notion that ACCg belongs to the core circuits mediating normal social behaviors.

Public Health Relevance

Individuals with psychiatric disorders marked by social deficits often fail to reciprocate normally in social situations. However, neural mechanisms underlying reciprocity remain unknown. We will develop a turn-taking dictator game in rhesus monkeys, in which we can study prosocial and antisocial reciprocity. We will examine neuronal signatures of reciprocity in the anterior cingulate cortex (ACC), a brain region implicated in signaling the rewards received by oneself and other individuals. We hypothesize that the reward signaling by the ACC neurons is central to reciprocity, endorsing the notion that ACC belongs to the core circuits mediating normal social behaviors that are compromised in numerous psychiatric disorders.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Exploratory/Developmental Grants (R21)
Project #
1R21MH107853-01A1
Application #
9035065
Study Section
Biobehavioral Regulation, Learning and Ethology Study Section (BRLE)
Program Officer
Simmons, Janine M
Project Start
2015-09-25
Project End
2017-07-31
Budget Start
2015-09-25
Budget End
2016-07-31
Support Year
1
Fiscal Year
2015
Total Cost
$244,825
Indirect Cost
$69,825
Name
Yale University
Department
Psychology
Type
Schools of Arts and Sciences
DUNS #
043207562
City
New Haven
State
CT
Country
United States
Zip Code
06510
Piva, Matthew; Chang, Steve W C (2018) An integrated framework for the role of oxytocin in multistage social decision-making. Am J Primatol 80:e22735
Chang, Steve W C (2017) An Emerging Field of Primate Social Neurophysiology: Current Developments. eNeuro 4:
Apps, Matthew A J; Rushworth, Matthew F S; Chang, Steve W C (2016) The Anterior Cingulate Gyrus and Social Cognition: Tracking the Motivation of Others. Neuron 90:692-707
Dal Monte, Olga; Piva, Matthew; Morris, Jason A et al. (2016) Live interaction distinctively shapes social gaze dynamics in rhesus macaques. J Neurophysiol 116:1626-1643