The impact of sleep on complex gross‐motor adaptation in adolescents

Abstract

Sleep has been shown to facilitate the consolidation of newly acquired motor memories in adults. However, the role of sleep in motor memory consolidation is less clear in children and adolescents, especially concerning real‐life gross‐motor skills. Therefore, we investigated the effects of sleep and wakefulness on a complex gross‐motor adaptation task by using a bicycle with an inverse steering device. A total of 29 healthy adolescents aged between 11 and 14 years (five female) were either trained to ride an inverse steering bicycle (learning condition) or a stationary bicycle (control condition). Training took place in the morning (wake, n = 14) or in the evening (sleep, n = 15) followed by a 9‐hr retention interval and a subsequent re‐test session. Slalom cycling performance was assessed by speed (riding time) and accuracy (standard deviation of steering angle) measures. Behavioural results showed no evidence for sleep‐dependent memory consolidation. However, overnight gains in accuracy were associated with an increase in left hemispheric N2 slow sleep spindle activity from control to learning night. Furthermore, decreases in REM and tonic REM duration were related to higher overnight improvements in accuracy. Regarding speed, an increase in REM and tonic REM duration was favourable for higher overnight gains in riding time. Thus, although not yet detectable on a behavioural level, sleep seemed to play a role in the acquisition of gross‐motor skills. A promising direction for future research is to focus on the possibility of delayed performance gains in adolescent populations.

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).…”

Sleep Macrostructure and NREM Sleep Instability Analysis in Pediatric Developmental Coordination Disorder

“…There are more studies about the role of sleep in motor ability and motor learning [12,22] at any age of life [22,23]. Particularly, an interesting report of Bothe et al [22] in 2018 showed the impact of sleep on gross motor adaptation in a group of adolescents with typical developing profile, pinpointing the role of an increase in REM sleep on cortico-cerebellar network activity that organizes dynamic aspects of movement such as motor coordination. From this perspective, we can explain the REM% reduction in our sample as a sign of the alteration in cortico-cerebellar network activity that could be considered as a cause of DCD [24].…”

Wide awake at bedtime? The effects of caffeine on sleep and circadian timing in teenagers - a randomized crossover trial

“…This approach combines the reliability of standardized automatic scouring with the validity of human expert scoring and has successfully applied in earlier studies on sleep of adolescents (e.g. (63,64)). Due to technical problems, the recordings of two nights (1 x placebo condition, 1 x caffeine condition) were incomplete.…”