Hippocampal CA2 sharp-wave ripples reactivate and promote social memory

The consolidation of spatial memory depends on the reactivation (‘replay’) of hippocampal place cells that were active during recent behaviour. Such reactivation is observed during sharp-wave ripples (SWRs)—synchronous oscillatory electrical events that occur during non-rapid-eye-movement (non-REM) sleep and whose disruption impairs spatial memory. Although the hippocampus also encodes a wide range of non-spatial forms of declarative memory, it is not yet known whether SWRs are necessary for such memories. Moreover, although SWRs can arise from either the CA3 or the CA2 region of the hippocampus, the relative importance of SWRs from these regions for memory consolidation is unknown. Here we examine the role of SWRs during the consolidation of social memory—the ability of an animal to recognize and remember a member of the same species—focusing on CA2 because of its essential role in social memory. We find that ensembles of CA2 pyramidal neurons that are active during social exploration of previously unknown conspecifics are reactivated during SWRs. Notably, disruption or enhancement of CA2 SWRs suppresses or prolongs social memory, respectively. Thus, SWR-mediated reactivation of hippocampal firing related to recent experience appears to be a general mechanism for binding spatial, temporal and sensory information into high-order memory representations, including social memory.
This work was supported by the NVIDIA Corporation, an EMBO Postdoctoral Fellowship (ALTF 120-2017) and a K99 grant from the US National Institutes of Health (NIH; K99MH122582) (to A.O.); a Sir Henry Wellcome Postdoctoral Fellowship and K99 grant (K99MH120343) (to A.F.-R.); a National Alliance for Research on Schizophrenia and Depression (NARSAD) Young Investigator award from the Brain and Behavior Foundation founded by the Osterhaus family (to F.L.); and grants MH-104602 and MH-106629 from the National Institute of Mental Health (NIMH) and a grant from the Zegar Family Foundation (to S.A.S.).