Hippocampal contextualization of social rewards

Abstract Acquiring and exploiting memories of rewarding experiences is critical for survival. The spatial environment in which a rewarding stimulus is encountered regulates memory retrieval. The ventral hippocampus (vH) has been implicated in contextual memories involving rewarding stimuli such as food, social cues or drugs. Yet, the spatial representations and circuits underlying contextual memories of socially rewarding stimuli are poorly understood. Here, using in vivo electrophysiological recordings during a social reward contextual conditioning paradigm in mice, we showed that vH neurons discriminate between contexts with neutral or acquired social reward value and exhibit a preferential remapping of their place fields to the context previously paired with social reward cues. The formation of context-discriminating vH neurons following learning was contingent upon the presence of salient reinforcers. Moreover, vH neurons showed different contextual representations during retrieval of social reward and fear contextual memories, suggesting different vH circuits underlie positively and negatively valenced contextual memories. Finally, optogenetic inhibition of locus coeruleus (LC) projections in the vH selectively disrupted social reward contextual memory by impairing vH contextual representations. Collectively, our findings reveal that the vH integrates contextual and social reward information, with memory encoding of these representations supported by input from the LC.