Dynamic coupling between slow waves and sleep spindles during slow wave sleep in humans is modulated by functional pre-sleep activation

Juliana Yordanova,Vasil Kolev,Roumen Kirov,Rolf Verleger

doi:10.1038/s41598-017-15195-x

Juliana Yordanova, Vasil Kolev + Show 2 more

Open Access

https://doi.org/10.1038/s41598-017-15195-x

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Abstract

Co-existent sleep spindles and slow waves have been viewed as a mechanism for offline information processing. Here we explored if the temporal synchronization between slow waves and spindle activity during slow wave sleep (SWS) in humans was modulated by preceding functional activations during pre-sleep learning. We activated differentially the left and right hemisphere before sleep by using a lateralized variant of serial response time task (SRTT) and verified these inter-hemispheric differences by analysing alpha and beta electroencephalographic (EEG) activities during learning. The stability and timing of coupling between positive and negative phases of slow waves and sleep spindle activity during SWS were quantified. Spindle activity was temporally synchronized with both positive (up-state) and negative (down-state) slow half waves. Synchronization of only the fast spindle activity was laterally asymmetric after learning, corresponding to hemisphere-specific activations before sleep. However, the down state was associated with decoupling, whereas the up-state was associated with increased coupling of fast spindle activity over the pre-activated hemisphere. These observations provide original evidence that (1) the temporal grouping of fast spindles by slow waves is a dynamic property of human SWS modulated by functional pre-sleep activation patterns, and (2) fast spindles synchronized by slow waves are functionally distinct.

Highlights

Slow wave activity (SWA) and sleep spindles are fundamental electrophysiological signatures of non-rapid eye movement (NREM) sleep in both humans and animals
To control for the statistical validity of functional asymmetries induced by the side of the trained hemisphere, individual gain of implicit knowledge (ImK) before sleep and amount of explicit knowledge (ExK) after sleep were included as covariates in the analyses
Recent sleep studies imply that major neuroelectric events during NREM sleep, sleep spindles and slow oscillations, support concurrently behavioural improvement after sleep (e.g.,10,16,17)

Summary

Introduction

Slow wave activity (SWA) and sleep spindles are fundamental electrophysiological signatures of non-rapid eye movement (NREM) sleep in both humans and animals. In support to the notion that co-occurring SWA and sleep spindles potentiate sleep-dependent memory consolidation[9,13,14,15], a variety of studies have correlated coordinated changes with behavioural improvements after sleep[6,12,16,17,18], as well as with general mental ability[19] It remains less well known whether the temporal locking between slow wave and spindle activities vary as a function of preceding brain activations in a use-dependent way[9]. The objective of the present study was to explore if the topographic patterns of coupling between co-existing slow-wave and sleep spindle activities depend on pre-sleep functional activations. We validated pre-sleep inter-hemispheric differences by the topographic patterns of alpha and beta EEG desynchronization

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