Hippocampal contextualization of social rewards in mice
Joana Mendes Duarte, Robin Nguyen, Marios Kyprou, Kaizhen Li, Anastasija Milentijevic, Carlo Cerquetella, Thomas Forro, Stéphane Ciocchi
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 neuronal representations and circuits underlying contextual memories of socially rewarding stimuli are poorly understood. Here, using in vivo electrophysiological recordings, in vivo one-photon calcium imaging, and optogenetics during a social reward contextual conditioning paradigm in male mice, we show that vH neurons discriminate between contexts with neutral or acquired social reward value. The formation of context-discriminating vH neurons following learning was contingent upon the presence of unconditioned stimuli. Moreover, vH neurons showed distinct contextual representations during the retrieval of social reward compared to fear 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. The neuronal mechanisms serving contextual memories of socially rewarding stimuli are unclear. Here the authors demonstrate that neurons in the ventral hippocampus of male mice discriminate between neutral and socially rewarding contexts, a process dependent on input from the locus coeruleus.