Network-wide reorganization of procedural memory during NREM sleep revealed by fMRI.

Shahabeddin Vahdat,Stuart Fogel,Habib Benali,Julien Doyon

doi:10.7554/elife.24987

Abstract

Sleep is necessary for the optimal consolidation of newly acquired procedural memories. However, the mechanisms by which motor memory traces develop during sleep remain controversial in humans, as this process has been mainly investigated indirectly by comparing pre- and post-sleep conditions. Here, we used functional magnetic resonance imaging and electroencephalography during sleep following motor sequence learning to investigate how newly-formed memory traces evolve dynamically over time. We provide direct evidence for transient reactivation followed by downscaling of functional connectivity in a cortically-dominant pattern formed during learning, as well as gradual reorganization of this representation toward a subcortically-dominant consolidated trace during non-rapid eye movement (NREM) sleep. Importantly, the putamen functional connectivity within the consolidated network during NREM sleep was related to overnight behavioral gains. Our results demonstrate that NREM sleep is necessary for two complementary processes: the restoration and reorganization of newly-learned information during sleep, which underlie human motor memory consolidation.

Highlights

There is ample evidence that sleep plays a crucial role in the consolidation of newly-acquired procedural memory, for explicitly instructed sequential motor skills (Walker et al, 2002; Korman et al, 2003; Doyon and Benali, 2005; Korman et al, 2007; Debas et al, 2010)
In the motor sequence learning (MSL) task, subjects practiced a selfpaced, explicitly known 5-item finger sequence task, which was compared with performance on a motor control task (CTL) in which participants were asked to produce simultaneous movements of all four fingers at the same average frequency, and for the same number of times as in the MSL task
We found that the ventrolateral putamen was the primary brain region within the consolidated pattern whose functional connectivity was significantly elevated during non-rapid eye movement (NREM) sleep in the MSL compared to the CTL night (corrected for multiple comparisons using Gaussian random field theory (GRF), p

Summary

Introduction

There is ample evidence that sleep plays a crucial role in the consolidation of newly-acquired procedural memory, for explicitly instructed sequential motor skills (Walker et al, 2002; Korman et al, 2003; Doyon and Benali, 2005; Korman et al, 2007; Debas et al, 2010). Several mechanistic hypotheses have been proposed regarding the contribution of sleep in this memory process (see [Frankland and Bontempi, 2005; Rasch and Born, 2007; Tononi and Cirelli, 2014] for comprehensive reviews). The dynamic neural changes that drive motor memory consolidation during sleep still remain controversial (Frankland and Bontempi, 2005; Rasch and Born, 2013; Tononi and Cirelli, 2014). There is mounting evidence in support of this hypothesis including the replay of hippocampal place cell firing (Skaggs and McNaughton, 1996; Lee and Wilson, 2002) in rodents, as well as human studies employing targeted memory reactivation paradigms using auditory or olfactory cues (Rasch et al, 2007; Cousins et al, 2014; Laventure et al, 2016), and neuroimaging studies showing the reactivation of learning-related brain

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