The Role of Experience in Prioritizing Hippocampal Replay

Abstract During sleep, recent memories are consolidated, whereby behavioral episodes first encoded by the hippocampus get transformed into long-term memories. However, the brain cannot consolidate every experience and much like the triage of an emergency room, the hippocampus is hypothesized to give precedence to more important memories first, and deprioritize or even skip over less relevant memories if needed. Here we examine two factors that are postulated to influence this memory triage process- 1) repetition, arising from the number of times a behavioral episode is repeated, increasing the priority to consolidate and 2) familiarity, resulting from previously experiencing a similar behavioral episode, in turn decreasing the need for further consolidation. Recording from large ensembles of hippocampal place cells while rats ran repeated spatial trajectories, and afterwards during periods of sleep, we examined how these two factors influenced replay, a hypothesized mechanism of consolidation involving the offline spontaneous reactivation of memory traces. We observed that during sleep, the rate of replay events for a given track increased proportionally with the number of spatial trajectories run by the rat. In contrast to this, the rate of sleep replay events decreased if the rat was more familiar with the track, arising from previously running on the same track before its most recent sleep session. Furthermore, we find that the cumulative number of awake replay events that occur during behavior, influenced by both the novelty and duration of an experience, predicts which memories are prioritized for sleep replay, and provides a more parsimonious mechanism for the selectively strengthening and triaging of memories.