Abstract
Sleep spindle activity has repeatedly been found to contribute to brain plasticity and consolidation of both declarative and procedural memories. Here we propose a framework for motor memory consolidation that outlines the essential contribution of the hierarchical and multi-scale periodicity of spindle activity, as well as of the synchronization and interaction of brain oscillations during this sleep-dependent process. We posit that the clustering of sleep spindles in 'trains', together with the temporally organized alternation between spindles and associated refractory periods, is critical for efficient reprocessing and consolidation of motor memories. We further argue that the long-term retention of procedural memories relies on the synchronized (functional connectivity) local reprocessing of new information across segregated, but inter-connected brain regions that are involved in the initial learning process. Finally, we propose that oscillatory synchrony in the spindle frequency band may reflect the cross-structural reactivation, reorganization and consolidation of motor, and potentially declarative, memory traces within broader subcortical-cortical networks during sleep. This article is part of the Theo Murphy meeting issue 'Memory reactivation: replaying events past, present and future'.
Highlights
A plethora of studies using a large variety of methodological approaches in animal models and humans have clearly demonstrated that memory is not a unitary process
To study this type of procedural memory, researchers have used a variety of motor sequence learning (MSL) paradigms which test the process by which discrete, independent actions become unified and performed effortlessly as a unitary sequence through repeated practice
Studies using MSL paradigms have repeatedly shown that the procedural memory consolidation process of motor skill representations is primarily observed hours or days after the first training session, Cohen et al [11] have recently reported that the same offline phenomena may occur rapidly between blocks of practice executed during the initial training session
Summary
A plethora of studies using a large variety of methodological approaches in animal models and humans have clearly demonstrated that memory is not a unitary process. Results from our laboratory [24,56] and that of other researchers have shown that the groups of periodically recurring spindles (called ‘trains’) appear to cycle at an infraslow frequency scale (about 0.02 Hz) during both light NREM stage 2 sleep [54,55] and deep NREM stage 3 slowwave sleep (SWS) [23] Such ‘trains’ of sleep spindles closely spaced in time are operationalized in our framework (figure 1a) as groups of two or more consecutive and region-specific spindles interspaced by less than or equal to 6 s [24], in comparison to those occurring in isolation royalsocietypublishing.org/journal/rstb Phil. (a) train of spindles isolated spindles (≥2 consecutive spindles interspaced by £6s) (>6s from neighbour spindles)
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