Dynamic and stable hippocampal representations of social identity and reward expectation support associative social memory in male mice

Recognizing an individual and retrieving and updating the value information assigned to the individual are fundamental abilities for establishing social relationships. To understand the neural mechanisms underlying the association between social identity and reward value, we developed Go-NoGo social discrimination paradigms that required male subject mice to distinguish between familiar mice based on their individually unique characteristics and associate them with reward availability. We found that mice could discriminate individual conspecifics through a brief nose-to-nose investigation, and this ability depended on the dorsal hippocampus. Two-photon calcium imaging revealed that dorsal CA1 hippocampal neurons represented reward expectation during social, but not non-social tasks, and these activities were maintained over days regardless of the identity of the associated mouse. Furthermore, a dynamically changing subset of hippocampal CA1 neurons discriminated between individual mice with high accuracy. Our findings suggest that the neuronal activities in CA1 provide possible neural substrates for associative social memory.