Dorso-ventral hippocampus neural assemblies reactivate during sleep following an aversive experience

Abstract

The integration of spatial and emotional components into episodic memory relies on coordinated interactions between hippocampal circuits and emotion-processing regions. While the dorsal hippocampus (dHPC) supports memory consolidation through sharp-wave ripple (SWR)-associated reactivation of spatial representations, it lacks direct connectivity with key emotional centers such as the amygdala. In contrast, the ventral hippocampus (vHPC) is anatomically and functionally embedded within the emotional network. How the dHPC and vHPC coordinate during sleep to support the processing of complex contextual and emotional experiences remains unclear. Here, we used simultaneous electrophysiological recordings from the dHPC and vHPC in rats performing a spatial alternation task under opposite emotional valence and during subsequent sleep. We show that dorso-ventral neuronal assemblies better disambiguate the between valence than isolated dorsal or ventral assemblies. During non-REM sleep, coordinated SWRs orchestrate assembly reactivation across the dorso-ventral hippocampal axis following both aversive and rewarding experiences; however, reactivation after aversive trials more closely mirrors the original neural patterns. This enhanced fidelity is driven by the heightened recruitment of shock-responsive neurons of the ventral hippocampus and spatial replay of the dorsal hippocampus into coordinated SWRs. Our findings identify a mechanism by which the hippocampus integrates the spatial and emotional dimensions of an experience during sleep, potentially routing information to the broader emotional memory network via synchronized SWRs.