Hippocampal oscillatory dynamics in freely behaving rats during exploration of social and non-social stimuli

Hippocampal CA2 supports social memory and encodes information about social experiences. Our previous study showed that CA2 place cells responded specifically to social stimuli (Nat Commun, (Alexander et al. 2016)). In addition, a prior study showed that activation of CA2 induces slow gamma rhythms (~ 25–55 Hz) in the hippocampus (Elife, (Alexander 2018)). Together, these results raise the question of whether slow gamma rhythms coordinate CA2 activity during social information processing. We hypothesized that slow gamma would be associated with transmission of social memories from CA2 to CA1, perhaps to integrate information across regions or promote social memory retrieval. We recorded local field potentials from hippocampal subfields CA1, CA2, and CA3 of 4 rats performing a social exploration task. We analyzed the activity of theta, slow gamma, and fast gamma rhythms, as well as sharp wave-ripples (SWRs), within each subfield. We assessed interactions between subfields during social exploration sessions and during presumed social memory retrieval in post-social exploration sessions. We found that CA2 slow gamma rhythms increased during social interactions but not during non-social exploration. CA2–CA1 theta-show gamma coupling was enhanced during social exploration. Furthermore, CA1 slow gamma rhythms and SWRs were associated with presumed social memory retrieval. In conclusion, these results suggest that CA2–CA1 interactions via slow gamma rhythms occur during social memory encoding, and CA1 slow gamma is associated with retrieval of social experience.