Emotion reconfigures neuronal coordination across brains to control social choice

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Abstract

Responding to others’ emotional states is essential for social behavior, yet the neural mechanisms by which brains dynamically coordinate across individuals in different emotional states is unknown. Here, we show that emotions reorganize brain-to-brain coupling through distinct, cell-type-specific mechanisms that directly guide social choice. Simultaneous calcium imaging in three interacting mice revealed that anterior cingulate cortex (ACC) pyramidal neurons are inter-brain correlated during neutral interactions, but this coupling is disrupted when one partner is stressed. In contrast, stress recruits inter-brain coupling of ACC somatostatin (SOM) neurons. Behaviorally controlled, cell-type-specific optogenetic manipulations demonstrated that preventing SOM inter-brain coupling abolished emotion discrimination, whereas artificially inducing or inverting SOM or pyramidal coupling bidirectionally reshaped social preference in an emotion-dependent manner. Notably, a new closed-loop paradigm in which real-time activity from one mouse drove cell-type-specific stimulation in another promoted social preference only when targeting SOM neurons in stress conditions. Extending these findings to humans, we show that stress similarly disrupts frontal gamma-band inter-brain coupling during live social interaction, indicating conserved emotion-sensitive principles across species. Together, these findings establish a mechanistic framework in which emotion-dependent, cell-type-specific brain-to-brain dynamics causally shape socio-emotional behavior.

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