Endogenous memory reactivation during sleep in humans is clocked by slow oscillation-spindle complexes

Thomas Schreiner,Bernhard P Staresina,Tobias Staudigl,Marit Petzka

doi:10.1038/s41467-021-23520-2

Thomas Schreiner, Bernhard P Staresina + Show 2 more

Open Access

https://doi.org/10.1038/s41467-021-23520-2

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Abstract

Sleep is thought to support memory consolidation via reactivation of prior experiences, with particular electrophysiological sleep signatures (slow oscillations (SOs) and sleep spindles) gating the information flow between relevant brain areas. However, empirical evidence for a role of endogenous memory reactivation (i.e., without experimentally delivered memory cues) for consolidation in humans is lacking. Here, we devised a paradigm in which participants acquired associative memories before taking a nap. Multivariate decoding was then used to capture endogenous memory reactivation during non-rapid eye movement (NREM) sleep in surface EEG recordings. Our results reveal reactivation of learning material during SO-spindle complexes, with the precision of SO-spindle coupling predicting reactivation strength. Critically, reactivation strength (i.e. classifier evidence in favor of the previously studied stimulus category) in turn predicts the level of consolidation across participants. These results elucidate the memory function of sleep in humans and emphasize the importance of SOs and spindles in clocking endogenous consolidation processes.

Highlights

Sleep is thought to support memory consolidation via reactivation of prior experiences, with particular electrophysiological sleep signatures (slow oscillations (SOs) and sleep spindles) gating the information flow between relevant brain areas
We show that memory reactivation is bound to the presence of SOspindle complexes, with the precision of their coupling correlating with reactivation strength
Our results demonstrate that consolidation relies on endogenous memory reactivation clocked by SO-spindle complexes

Summary

Introduction

Sleep is thought to support memory consolidation via reactivation of prior experiences, with particular electrophysiological sleep signatures (slow oscillations (SOs) and sleep spindles) gating the information flow between relevant brain areas. Reactivation strength (i.e. classifier evidence in favor of the previously studied stimulus category) in turn predicts the level of consolidation across participants These results elucidate the memory function of sleep in humans and emphasize the importance of SOs and spindles in clocking endogenous consolidation processes. Building on the work summarized above, we propose that SOspindle complexes might clock endogenous memory reactivation in service of consolidation during human sleep To test this notion, we devised an experimental paradigm in which participants acquired associative memories before taking a nap. Reactivation strength in turn predicts the extent of consolidation across participants These findings elucidate the memory function of sleep in humans and illustrate the importance of SO-spindle coupling for clocking endogenous consolidation processes

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