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. 2021 May 25;12(1):3112.
doi: 10.1038/s41467-021-23520-2.

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

Thomas Schreiner  1 , Marit Petzka  2 , Tobias Staudigl  1 , Bernhard P Staresina  3
Affiliations

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

Thomas Schreiner et al. Nat Commun. .

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.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Experimental procedure, behavioral results, and localizer task.
a During encoding, participants were presented with 120 verb-object or verb-scene combinations (depending on experimental session). Memory performance was tested before and after a 120 min nap period. At the end of each session, participants performed a localizer task in which they processed a new set of object and scene images. b Behavioral results for both experimental sessions pre- (light gray) and post-sleep (dark gray). Bar graphs show mean (±SEM) percentage of recalled image exemplars out of correctly recognized verbs. Dots indicate individual memory performance of participants (N = 20). Stars denote significant differences as derived from a repeated measures ANOVA (p = 0.001). c Stimulus categories (objects vs. scenes) could be reliably decoded (above chance) from the localizer EEG data, starting around 150 ms post stimulus onset (the black solid line indicates decoding performance (±SEM)). The horizontal dashed line indicates surrogate decoding performance, which was estimated by shuffling the training labels 250 times. The vertical solid line indicates stimulus onset (time = 0). The lower horizontal gray line shows the temporal extent of significant decoding results as derived from a dependent-samples t-test (two-sided, p = 0.002, cluster corrected across time). Source data are provided as a Source Data file.
Fig. 2
Fig. 2. SO-spindle locked memory reactivation.
a Time–frequency representation of all SO-spindle segments (z-scored across time; only positive values are displayed, with yellow indicating power increases). b Learning-related brain patterns (objects vs. scenes) were decodable during SO-spindle complexes (contour lines indicate the extent of the significant cluster, p = 0.016 corrected; color range (blue to yellow) represents t values against surrogate decoding performance, which was estimated by shuffling the training labels 250 times). The averaged EEG trace (all instances in which SO downstates were followed by sleep spindles within 1.5 s at channel Cz in microvolt [μV]) illustrates the relationship of the observed reactivation signal with ongoing oscillatory activity. The topographical insert illustrates the results of a “searchlight decoding procedure”, indicating that bilateral parietal and occipital areas exhibited stimulus-category related effects (please note that statistical tests were done for illustrative purposes only). c Phases of the SO-spindle modulation derived from channel Cz, illustrating the clustering of spindle power toward the SO upstate (upstate corresponding to 0 and downstate to ± π, with –π/2 reflecting the down- to upstate transition; Rayleigh test: p < 0.0001; z = 16.71). The black line illustrates the mean coupling direction and vector length (−36.78° ± 5.48°, mean vector length = 0.91). Circular-linear correlation analysis between the individual mean SO-spindle coupling phase (circles) and the mean reactivation strength (area under the curve [AUC] scores; color coded, with white indicating high classification performance and black low classification performance) revealed a positive association (r = 0.66; p = 0.011). d Reactivation strength correlated positively with behavioral levels of associative memory consolidation (Spearman’s Rank Correlation, r = 0.45, p = 0.048). Source data are provided as a Source Data file.
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