Oxytocin in the Amygdala Sustains Prosocial Behavior via State-Dependent Amygdala–Prefrontal Modulation

Abstract

Prosocial behaviors are crucial for maintaining primates' complex social relationships. As central regions involved in social decision-making, the basolateral amygdala (BLA) processes social salience and value, while the gyrus of the anterior cingulate cortex (ACCg) integrates social information to guide decision-making. Oxytocin, a key modulator of social behavior, can influence both prosocial behavior and neural activity in these regions, but the precise mechanisms remain unclear. We investigated oxytocin's effects on prosocial behavior and neural activity by infusing oxytocin or saline into the BLA (Oxt-BLA, Sal-BLA) and examining the effects of Oxt-BLA on prosocial decisions, BLA and ACCg neural activity, and the coordination between the two regions in male rhesus macaques. We found that Oxt-BLA's behavioral effects were state-dependent: during high prosocial states, it sustained prosocial choices and task engagement, counteracting the natural decline seen in the control condition. However, during low prosocial states, Oxt-BLA had minimal behavioral effects. At the neural level, Oxt-BLA enhanced BLA and ACCg activity for prosocial choices only during high prosocial states. Importantly, Oxt-BLA maintained stable BLA–ACCg coordination during high prosocial states, preventing the decline in communication observed in control conditions. These findings demonstrate that oxytocin's ability to sustain prosocial behavior depends on social motivational state. These results support that oxytocin processing in the BLA acts as a state-dependent neuromodulator that enhances BLA and ACCg neural responses and maintains BLA–ACCg communication to guide prosocial decisions.