Abstract

Emerging evidence suggests that sleep plays a key role in procedural learning, particularly in the continued development of motor skill learning following initial acquisition. We argue that a detailed examination of the time course of performance across sleep on the finger-tapping task, established as the paradigm for studying the effect of sleep on motor learning, will help distinguish a restorative role of sleep in motor skill learning from a proactive one. Healthy subjects rehearsed for 12 trials and, following a night of sleep, were tested. Early training rapidly improved speed as well as accuracy on pre-sleep training. Additional rehearsal caused a marked slow-down in further improvement or partial reversal in performance to observed levels below theoretical upper limits derived on the basis of early pre-sleep rehearsal. This decrement in learning efficacy does not occur always, but if and only if it does, overnight sleep has an effect in fully or partly restoring the efficacy and actual performance to the optimal theoretically achieveable level. Our findings re-interpret the sleep-dependent memory enhancement in motor learning reported in the literature as a restoration of fatigued circuitry specialized for the skill. In providing restitution to the fatigued brain, sleep eliminates the rehearsal-induced synaptic fatigue of the circuitry specialized for the task and restores the benefit of early pre-sleep rehearsal. The present findings lend support to the notion that latent sleep-dependent enhancement of performance is a behavioral expression of the brain's restitution in sleep.

Highlights

  • Following an initial stage of learning and memory acquisition, there is a stage termed memory consolidation, during which the newly-formed, labile memories that arise in the brain as a result of the learning stabilize

  • The best evidence to date on procedural learning in humans has been observed in the continued development of motor-skill learning following initial acquisition: sleep, and not the passage of time, has been shown to be critical for further enhancement of the skill following the initial training

  • Overnight increase in speed was greater than that predicted on the basis of additional training alone [6]: this overnight improvement is known as latent sleepdependent memory enhancement, has been observed in both visual [1,4,8] and motor [5,9,10] skill learning paradigms, and is a centerpiece of the claim that sleep is required for memory consolidation and enhancement [7,11]

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Summary

Introduction

Following an initial stage of learning and memory acquisition, there is a stage termed memory consolidation, during which the newly-formed, labile memories that arise in the brain as a result of the learning stabilize. Overnight increase in speed (and accuracy) was greater than that predicted on the basis of additional training alone [6]: this overnight improvement is known as latent sleepdependent memory enhancement, has been observed in both visual [1,4,8] and motor [5,9,10] skill learning paradigms, and is a centerpiece of the claim that sleep is required for memory consolidation and enhancement [7,11]. It was further found that the sleep-dependent learning process selectively improved the speed of the key press transitions that were the slowest prior to sleep [12]. This suggests that sleep involves the amalgamation of disparate memory units into a larger single memory representation or chunk. Sleep has been found to be critical in at least some tasks that involve retention of motor skill

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