Dorso-ventral hippocampal neural assemblies are preferentially reactivated during NREM sleep following an aversive experience

Abstract

AbstractSleep plays a crucial role in memory stabilization. In the dorsal hippocampus (dHPC), fast oscillations (sharp-wave ripples) during non-REM sleep consolidate spatial memories through place cell reactivation. The hippocampal formation is heterogeneous; the dHPC processes mostly contextual information, while the ventral part (vHPC) encodes valence and anxiety. We propose that dorsal- ventral communication during sleep is involved in the consolidation of emotional memories, potentially integrating or segregating contextual and valence information. To test this, we recorded the electrophysiological activity in the dHPC and vHPC in rats during reward and aversion-motivated exploration of a linear track and subsequent sleep. We detected dorsal and ventral SWRs during NREM sleep as well as neuronal assemblies during each exploration type and identified dorsal, ventral, and joint (dorso-ventral) assemblies. We found that dorso-ventral hippocampal coordination involves coordinated ripples and bursts of ripples. Aversive joint assemblies exhibited higher reactivation during non-REM sleep than the joint assemblies from the reward condition. Interestingly, joint aversive assemblies reactivated selectively during dorso-ventral coordinated ripples. Furthermore, their reactivation strength positively correlated with their strength of activation during the task. These results suggest the existence of dorsal-ventral hippocampal functional communication capable of sustaining the selective reactivation of experiences based on their emotional valence.