Mechanisms of Prosocial Behaviors in Nonhuman Primates: Behavioral, Neural, and Neuromodulatory Insights

Date of Award

Spring 1-1-2025

Document Type

Dissertation

Degree Name

Doctor of Philosophy (PhD)

Department

Interdepartmental Neuroscience Program

First Advisor

Chang, Steve

Abstract

Prosocial behaviors are fundamental to primate social life. They rely on complex cognitive and neural mechanisms that allow individuals to integrate social information, anticipate others’ actions, and adapt their behavior to different social contexts. This dissertation investigates behavioral, neural, and neuromodulatory mechanisms underlying prosocial behaviors in primates, using rhesus macaques and common marmosets as model organisms. By employing both highly controlled experimental approaches and more naturalistic paradigms, this work advances our understanding of how prosocial decision-making is regulated at both behavioral and neural levels.The first study presented examines how oxytocin influences live prosocial decision-making in rhesus macaques. By locally infusing oxytocin into the basolateral amygdala (BLA) and simultaneously recording neural activity from the BLA and anterior cingulate cortex (ACC), we show that oxytocin action in the BLA promotes prosocial behaviors in a state-dependent manner. Underlying this behavioral effect is enhanced BLA and ACC responses to prosocial choices and strengthened BLA-ACC communication. These findings provide mechanistic insight into oxytocin’s action in the BLA to modulate social decision-making and inform its potential therapeutic applications. To study social behavior in a more naturalistic setting, we developed a modernized cooperative pulling apparatus for common marmosets, integrating automated behavioral tracking and wireless electrophysiology techniques. This fully automated apparatus allows for precise analysis of social coordination behaviors and strategies while preserving naturalistic elements of social interactions and decision-making. Marmosets successfully learn to cooperate and critically rely upon social gaze-dependent strategies to develop and maintain these interactions. Furthermore, these strategies are flexibly implemented and influenced by social relationship factors, partner identity, and prior interactions, demonstrating that their cooperation is a dynamic decision-making process rather than a reflexive response. To examine the neural basis of these behaviors, we recorded neuronal activity from the dorsomedial prefrontal cortex (dmPFC) in freely moving marmosets performing this task. Neural analyses reveal that dmPFC neurons encode distinct aspects of social coordination, maintaining structured representations for successful cooperation while displaying increased variability and trajectory lengths during unsuccessful interactions. Furthermore, dmPFC differentiates between social coordination, independent reward-seeking, and non-social coordination tasks, signifying its central role in encoding and integrating contextual information to guide social decision-making. By investigating primate social behaviors in live interactions and in varying contexts, this dissertation provides novel insights into the behavioral and neural dynamics driving prosocial behaviors. These findings have broader implications for creating a better understanding of the neural circuits governing typical social behaviors as well as the potential disruptions that may lead to social deficits in neuropsychiatric disorders, thus laying the groundwork for future studies on therapeutic interventions aimed at restoring social functioning.

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