Gross motor adaptation benefits from sleep after training

Abstract

Sleep has been shown to facilitate the consolidation of newly acquired motor memories. However, the role of sleep in gross motor learning, especially in motor adaptation, is less clear. Thus, we investigated the effects of nocturnal sleep on the performance of a gross motor adaptation task, i.e. riding an inverse steering bicycle. Twenty‐six male participants (M = 24.19, SD = 3.70 years) were randomly assigned to a PM‐AM‐PM (n = 13) or an AM‐PM‐AM (n = 13) group, i.e. they trained in the evening/morning and were re‐tested the next morning/evening and the following evening/morning (PM‐AM‐PM/AM‐PM‐AM group) so that every participant spent one sleep as well as one wake interval between the three test sessions. Inverse cycling performance was assessed by speed (riding time) and accuracy (standard deviation of steering angle) measures. Behavioural results showed that in the PM‐AM‐PM group a night of sleep right after training stabilized performance (accuracy and speed) and was further improved over the subsequent wake interval. In the AM‐PM‐AM group, a significant performance deterioration after the initial wake interval was followed by the restoration of subjects' performance levels from right after training when a full night of sleep was granted. Regarding sleep, right hemispheric fast N2 sleep spindle activity was related to better stabilization of inverse cycling skills, thus possibly reflecting the ongoing process of updating the participants' mental model from “how to ride a bicycle” to “how to ride an inverse steering bicycle”. Our results demonstrate that sleep facilitates the consolidation of gross motor adaptation, thus adding further insights to the role of sleep for tasks with real‐life relevance.

Slow oscillation-spindle coupling strength predicts real-life gross-motor learning in adolescents and adults

“…Two accounts might explain the absence of a sleep effect on task proficiency. (1) Sleep rather stabilizes than improves gross-motor memory, which is in line with previous gross-motor adaption studies (Bothe et al, 2019; Bothe et al, 2020). (2) Pre-sleep performance is critical for sleep to improve motor skills (Wilhelm et al, 2012).…”

“…Hippocampal memory reactivation during sleep is one cornerstone of the active systems consolidation theory, where coordinated SO-spindle activity route subcortical information to the cortex for long-term storage (Diekelmann & Born, 2010; Helfrich et al, 2019; Klinzing et al, 2019; Ngo et al, 2020). Quantitative markers of spindle and SO activity but not the quality of their interaction have been frequently related to motor memory in the past (Barakat et al, 2011; Bothe et al, 2019; Bothe et al, 2020; Huber et al, 2004; Morita et al, 2012; Nishida & Walker, 2007; Tamaki et al, 2008). Our results now complement the active systems consolidation theories’ mechanistic assumption of interacting oscillations by demonstrating that a precise SO-spindle interplay subserves gross-motor skill learning ( Figure 3DE ).…”

“…Only few studies have investigated the effect of sleep on complex real-life motor tasks. Overnight performance benefits for riding an inverse steering bike have been shown to be related to spindle activity in adolescents and adults (Bothe et al, 2019; Bothe et al, 2020). Similarly, juggling performance was supported by sleep and juggling training induced power increments in the spindle and SO frequency range during a nap (Morita et al, 2012, 2016).…”

Slow oscillation–spindle coupling strength predicts real-life gross-motor learning in adolescents and adults

“…Only few studies have investigated the effect of sleep on complex real-life motor tasks. Overnight performance benefits for riding an inverse steering bike have been shown to be related to spindle activity in adolescents and adults ( Bothe et al, 2019 ; Bothe et al, 2020 ). Similarly, juggling performance was supported by sleep and juggling training induced power increments in the spindle and SO frequency range during a nap ( Morita et al, 2012 ; Morita et al, 2016 ).…”

Does sleep contribute to the consolidation of motor memory?

“…The research literature is less extensive than for MSL. In a study on gross motor learning of a MA task (riding an inverse bike), Bothe et al [3] have shown that a training set-up of eveningmorning-evening (PM-AM-PM) is superior compared to AM-PM-AM in speed and accuracy. The authors related the stabilization to sleep spindles in the right hemisphere.…”