CA3 place cells that represent a novel waking experience are preferentially reactivated during sharp wave-ripples in subsequent sleep.

Abstract

A popular model of memory consolidation posits that recent memories stored in the hippocampus are reactivated during sleep and thereby transferred to neocortex for long-term storage. This process is thought to occur during sharp wave-ripples (SWRs) in nonrapid eye movement sleep (NREM). However, whether the hippocampus consolidates all recent memories in the same manner remains unclear. An efficient memory system may extract novel information from recent experiences for preferential consolidation. In the hippocampus, memories are thought to be stored initially in CA3. Therefore, CA3 place cells that encode novel experiences may be preferentially reactivated during SWRs in subsequent sleep. To test this hypothesis, we recorded CA3 place cells in rats during exposure to a familiar and a novel environment and during subsequent overnight sleep. We found that CA3 place cells that preferentially coded a novel environment showed larger firing rate increases during SWRs in NREM than place cells that preferentially coded a familiar environment. Moreover, CA3 place cell ensembles replayed trajectories from a novel environment during NREM with higher fidelity than trajectories from a familiar environment. Together, these results suggest that CA3 representations of novel experiences are preferentially processed during subsequent sleep.