Structured and unstructured reactivations during REM sleep are modulated by novel experiences

Abstract Mammalian sleep is composed of two distinct phases characterized by unique neural activity patterns: rapid eye movement (REM) and non-REM (nREM) sleep. While both phases are essential for memory consolidation, neural replay of awake experience as a candidate mechanism for memory consolidation has only been shown for nREM sleep and it remains unclear whether awake experiences are reactivated during REM sleep. Here, we evaluated whether awake experiences are reactivated by hippocampal CA1 pyramidal neurons during REM sleep using a combination of approaches including Bayesian decoding, sequence factorization, and co-activation analysis. We confirmed that representations of awake exploration are recapitulated during subsequent REM episodes with varying levels of temporal structure. We also found that temporally organized sequences were replayed with a higher frequency during REM sleep following a novel experience. Finally, we find internalized structure in CA1 activity prior to novel task exposure that is expressed in subsequent behaviour. Altogether, these results suggest that while hippocampal ensembles appear as a result of structural priors, salient experiences refine temporal sequences during subsequent REM sleep, suggesting a unique role for REM sleep in salient-experience consolidation.