Brain-wide electrical dynamics encode an appetitive socioemotional state

Many cortical and subcortical regions contribute to complex social behavior; nevertheless, the network level architecture whereby the brain integrates this information to encode appetitive socioemotional behavior remains unknown. Here we measure electrical activity from eight brain regions as mice engage in a social preference assay. We then use machine learning to discover an explainable brain network that encodes the extent to which mice chose to engage another mouse. This socioemotional network is organized by theta oscillations leading from prelimbic cortex and amygdala that converge on ventral tegmental area, and network activity is synchronized with brain-wide cellular firing. The network generalizes, on a mouse-by-mouse basis, to encode socioemotional behaviors in healthy animals, but fails to encode an appetitive socioemotional state in a ‘high confidence’ genetic mouse model of autism. Thus, our findings reveal the architecture whereby the brain integrates spatially distributed activity across timescales to encode an appetitive socioemotional brain state in health and disease.