Motor Learning Promotes the Coupling between Fast Spindles and Slow Oscillations Locally over the Contralateral Motor Network

Abstract

Recent studies from us and others suggest that traditionally declarative structures mediate some aspects of the encoding and consolidation of procedural memories. This evidence points to the existence of converging physiological pathways across memory systems. Here, we examined whether the coupling between slow oscillations (SO) and spindles, a mechanism well established in the consolidation of declarative memories, is relevant for the stabilization of human motor memories. To this aim, we conducted an electroencephalography study in which we quantified various parameters of these oscillations during a night of sleep that took place immediately after learning a visuomotor adaptation (VMA) task. We found that VMA increased the overall density of fast (≥12 Hz), but not slow (<12 Hz), spindles during nonrapid eye movement sleep, stage 3 (NREM3). This modulation occurred rather locally over the hemisphere contralateral to the trained hand. Although adaptation learning did not affect the density of SOs, it substantially enhanced the number of fast spindles locked to the active phase of SOs. The fact that only coupled spindles predicted overnight memory retention points to the relevance of this association in motor memory consolidation. Our work provides evidence in favor of a common mechanism at the basis of the stabilization of declarative and motor memories.

Visuomotor Adaptation Modulates the Clustering of Sleep Spindles Into Trains

“…The experimental design of this study is fully described in a previous publication derived from the same dataset ( Solano et al, 2021 ). Briefly, we conducted a within-subject experiment consisting of three sessions separated by 7 days each: (i) a familiarization session, (ii) a visuomotor adaptation session (VMA) in which a visual rotation (ROT) was applied, and (iii) a control session (CTL) in which subjects performed unperturbed, null trials (N).…”

“…To assess how these measures differed between VMA and CTL sessions we computed their relative difference according to the function ((VMA-CTL)/CTL*100) for each EEG channel and each subject ( Huber et al, 2004 , 2006 ; Solano et al, 2021 ). To illustrate the spatial distribution of the effects, we report the results in topographic maps (MNE-Python; Gramfort et al, 2013 ).…”

“…Overnight reactivation of hippocampal memories appears to depend on sleep spindles, slow oscillations (SO) and their precise synchrony ( Maingret et al, 2016 ; Ladenbauer et al, 2017 ; Helfrich et al, 2018 ; Muehlroth et al, 2019 ; Navarro-Lobato and Genzel, 2019 ). Recently, we have shown that motor learning, specifically visuomotor adaptation (VMA), also promotes the coupling between spindles and SOs ( Solano et al, 2021 ). The fact that the level of spindle-SO synchrony predicts overnight memory retention opens the possibility that common mechanisms operate in the stabilization of declarative and motor memories.…”

“…Sleep spindles are bursts of oscillatory thalamocortical activity thought to support the reactivation of newly formed memories ( Rasch and Born, 2013 ; Staresina et al, 2015 ; Schönauer, 2018 ). Individual spindles may promote memory consolidation through the modulation of intrinsic features such as their amplitude ( Barakat et al, 2012 ; Bergmann et al, 2012 ; Boutin et al, 2018b ), duration ( Morin et al, 2008 ; Laventure et al, 2016 ), power ( Ngo et al, 2020 ) and density ( Nishida and Walker, 2007 ; Barakat et al, 2011 ; Albouy et al, 2013 ; Solano et al, 2021 ). In the last few years, it has been argued that the rhythmicity in their occurrence may also be a relevant parameter influencing memory stabilization ( Lecci et al, 2017 ; Antony et al, 2018 ; Boutin and Doyon, 2020 ).…”

“…Here, we followed up on our previous findings ( Solano et al, 2021 ), to examine if VMA learning promotes the temporal organization of sleep spindles into trains. We also explored if the spindle-SO coupling which, as we showed is modulated by VMA, is also influenced by spindle rhythmicity.…”