Daytime Naps, Motor Memory Consolidation and Regionally Specific Sleep Spindles

In the last 14 years has your doctor created a napping protocol?

Do you prefer your  incompetence NOT KNOWING? OR NOT DOING?

 

Daytime Naps, Motor Memory Consolidation and Regionally Specific Sleep Spindles

Masaki Nishida and Matthew P. Walker ^*

Chris Miall, Academic Editor

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This article has been cited by other articles in PMC.

PLoS One. 2007; 2(4): e341.

Published online 2007 Apr 4. doi: 10.1371/journal.pone.0000341

 

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Abstract

Background

Increasing evidence demonstrates that motor-skill memories improve across a night of sleep, and that non-rapid eye movement (NREM) sleep commonly plays a role in orchestrating these consolidation enhancements. Here we show the benefit of a daytime nap on motor memory consolidation and its relationship not simply with global sleep-stage measures, but unique characteristics of sleep spindles at regionally specific locations; mapping to the corresponding memory representation.

Methodology/Principal Findings

Two groups of subjects trained on a motor-skill task using their left hand – a paradigm known to result in overnight plastic changes in the contralateral, right motor cortex. Both groups trained in the morning and were tested 8 hr later, with one group obtaining a 60–90 minute intervening midday nap, while the other group remained awake. At testing, subjects that did not nap showed no significant performance improvement, yet those that did nap expressed a highly significant consolidation enhancement. Within the nap group, the amount of offline improvement showed a significant correlation with the global measure of stage-2 NREM sleep. However, topographical sleep spindle analysis revealed more precise correlations. Specifically, when spindle activity at the central electrode of the non-learning hemisphere (left) was subtracted from that in the learning hemisphere (right), representing the homeostatic difference following learning, strong positive relationships with offline memory improvement emerged–correlations that were not evident for either hemisphere alone.

Conclusions/Significance

These results demonstrate that motor memories are dynamically facilitated across daytime naps, enhancements that are uniquely associated with electrophysiological events expressed at local, anatomically discrete locations of the brain.

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Introduction

A growing corpus of literature continues to demonstrate that, following learning, additional “offline” memory improvements develop during sleep [1], [2]. Evidence of sleep-dependent consolidation now exists across numerous memory domains, including procedural as well as declarative memory [3]. Regarding procedural motor memory, several studies have demonstrated that the extent of initial learning, and the subsequent offline enhancement, commonly correlate with non-rapid eye movement (NREM) sleep, and neurophysiological characteristics of NREM [4]–[8], although see [9]. For example, it has been shown that offline motor-memory enhancements specifically develop across a night of sleep, with the extent of improvement demonstrating a positive relationship with the amount of stage-2 NREM sleep, especially in the last quarter of the night [4]. Considering sleep spindles – a defining electrophysiological signature of NREM involving short (∼1 ) synchronous burst of activity (12–15 Hz) – may represent candidate triggers of synaptic potentiation leading to neural plasticity [10]–[12], and that spindle activity is highest late in the night [13], this latter correlation was hypothesized to reflected an association between spindle activity and offline memory improvement [4].

At a neural level, recent functional imaging data have also demonstrated that these overnight motor memory improvements are associated with a systems-level, plastic reorganization within the brain, including a lateralized expansion and increased activation in the right primary motor cortex; contralateral to the hand (left) learning the motor skill memory [14]. While sleep stage correlations represent a global measure of association with memory enhancement, such neuroimaging data illustrate that sleep produces highly localized changes in discrete brain circuits. Therefore, if sleep and specific electrophysiological characteristics of sleep are contributing to these circuit changes, then topographical EEG examination should reveal more selective, local associations with memory improvement.

Here we investigate the relationship between regionally specific sleep spindle activity and motor memory consolidation, using a nap paradigm, incorporating the above described motor-sequence task. The advantage of this design is twofold; a) the offline motor-skill enhancements are associated with a localized plastic change in the contralateral motor cortex, situated proximal to standard EEG recording sites where sleep spindles are commonly expressed [15], and b) it allows a within subject comparison of spindle activity between the predominant “learning” (right) hemisphere relative to the “non-learning” (left) hemisphere. We use the terms “learning” and “non-learning” hemispheres simply to reflect the known lateralized, offline plastic changes observe across a night of sleep using this task [14]; although it should be noted that practice-dependent motor learning using the non-dominant hand often involves bilateral motor cortex activation (e.g. [16]). We tested the hypothesis that i) daytime naps would result in significant offline learning enhancements of motor-skill memory, and ii) the magnitude of enhancement would not only be proportional to the amount of stage-2 NREM and the extent of sleep spindle activity, but specifically with spindle activity in the hemisphere associated with offline learning (right), relative to homeostatic/non-task relevant spindle activity in the “non-learning” hemisphere (left).