NEURONAL-LEVEL UNDERPINNINGS OF INTERBRAIN SYNCHRONIZATION DURING SOCIAL INTERACTIONS

A fundamental challenge in social neuroscience is understanding how two brains achieve neural coordination underlying social interactions. While hyperscanning studies revealed interbrain synchronization during social interactions, critical gaps remain: human-studies employed aggregate neural measures obscuring the cellular-level mechanisms underlying social coordination; while animal-studies examined free unconstrained social interactions or passive observation that limit interpretation. Critically, it remains unknown how interbrain individual neuron synchrony relates to social interactions, and specifically to opponent modeling. Here we address this gap through simultaneous single-neuron recordings from the dorsal anterior cingulate cortex of monkeys engaged in an iterated Prisoner’s Dilemma.

We conducted multi-level analyses from individual neurons to population dynamics. First, average firing rates between brains exhibited prominent zero-lag and secondary non-zero cross-correlation peaks, revealing real-time synchronization during interactions framed by task structure. Second, pairwise across-brain neuronal correlation significantly exceeded random shuffling and shuffling that preserved shared decision visual feedback, indicating synchronization reflects richer social cognitive context rather than individual encoding of sensory input or shared outcome. Third, multivariate data analysis combining principal component and canonical correlation analysis, uniquely enabled by single-neuron resolution and task structure, identified time-resolved population modes connecting interbrain synchronization with single-trial behavioral context.

These findings demonstrate context-dependent interbrain synchronization that emerges from specific patterns of single-neuron coupling, scaling to coordinated population dynamics. By achieving single-neuron resolution during social decision-making, this work lays a foundation for understanding how neural circuits in separate brains achieve the coordination underlying social cognition, establishing a framework for understanding the cellular basis of social decision making.