Hippocampal Ripple Diversity organises Neuronal Reactivation Dynamics in the Offline Brain

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Abstract

Hippocampal ripples are highly synchronized neuronal population patterns reactivating past waking experiences in the offline brain. Whether the level, structure, and content of ripple-nested activity are consistent across consecutive events or are tuned in each event remains unclear. By profiling individual ripples using laminar currents in the mouse hippocampus during sleep/rest, we identified Rad sink and LM sink ripples featuring current sinks in stratum radiatum versus stratum lacunosum-moleculare , respectively. These two ripple profiles recruit neurons differently. Rad sink ripples integrate recent motifs of waking coactivity, combining superficial and deep CA1 principal cells into denser, higher-dimensional patterns that undergo hour-long stable reactivation. In contrast, LM sink ripples contain core motifs of prior coactivity, engaging deep cells into sparser, lower-dimensional patterns that undergo a reactivation drift, gradually updating their pre-structured content for recent wakefulness. We propose that ripple-by-ripple diversity instantiates parallel reactivation channels for stable integration of recent wakefulness and flexible updating of prior internal representations.

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