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      Gross motor adaptation benefits from sleep after training

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          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.

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          Most cited references35

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          Causal evidence for the role of REM sleep theta rhythm in contextual memory consolidation.

          Rapid eye movement sleep (REMS) has been linked with spatial and emotional memory consolidation. However, establishing direct causality between neural activity during REMS and memory consolidation has proven difficult because of the transient nature of REMS and significant caveats associated with REMS deprivation techniques. In mice, we optogenetically silenced medial septum γ-aminobutyric acid-releasing (MS(GABA)) neurons, allowing for temporally precise attenuation of the memory-associated theta rhythm during REMS without disturbing sleeping behavior. REMS-specific optogenetic silencing of MS(GABA) neurons selectively during a REMS critical window after learning erased subsequent novel object place recognition and impaired fear-conditioned contextual memory. Silencing MS(GABA) neurons for similar durations outside REMS episodes had no effect on memory. These results demonstrate that MS(GABA) neuronal activity specifically during REMS is required for normal memory consolidation.
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            Principles derived from the study of simple skills do not generalize to complex skill learning.

            We review research related to the learning of complex motor skills with respect to principles developed on the basis of simple skill learning. Although some factors seem to have opposite effects on the learning of simple and of complex skills, other factors appear to be relevant mainly for the learning of more complex skills. We interpret these apparently contradictory findings as suggesting that situations with low processing demands benefit from practice conditions that increase the load and challenge the performer, whereas practice conditions that result in extremely high load should benefit from conditions that reduce the load to more manageable levels. The findings reviewed here call into question the generalizability of results from studies using simple laboratory tasks to the learning of complex motor skills. They also demonstrate the need to use more complex skills in motor-learning research in order to gain further insights into the learning process.
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              Daytime Naps, Motor Memory Consolidation and Regionally Specific Sleep Spindles

              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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                Author and article information

                Contributors
                kerstin.hoedlmoser@sbg.ac.at
                juergen.birklbauer@sbg.ac.at
                Journal
                J Sleep Res
                J Sleep Res
                10.1111/(ISSN)1365-2869
                JSR
                Journal of Sleep Research
                John Wiley and Sons Inc. (Hoboken )
                0962-1105
                1365-2869
                23 December 2019
                October 2020
                : 29
                : 5 ( doiID: 10.1111/jsr.v29.5 )
                : e12961
                Affiliations
                [ 1 ] Laboratory for Sleep, Cognition and Consciousness Research Centre for Cognitive Neuroscience University of Salzburg Salzburg Austria
                [ 2 ] Department of Sport and Exercise Science University of Salzburg Salzburg Austria
                [ 3 ] Department of Psychiatry and Psychotherapy Medical University of Vienna Vienna Austria
                Author notes
                [*] [* ] Correspondence

                Juergen Birklbauer, Department of Sport and Exercise Science, University of Salzburg, Schlossallee 49, 5400 Hallein, Austria.

                Email: juergen.birklbauer@ 123456sbg.ac.at

                Kerstin Hoedlmoser, Laboratory for Sleep, Cognition and Consciousness Research, Centre for Cognitive Neuroscience, University of Salzburg, Hellbrunnerstrasse 34, 5020 Salzburg, Austria.

                Email: kerstin.hoedlmoser@ 123456sbg.ac.at

                Author information
                https://orcid.org/0000-0001-5177-4389
                Article
                JSR12961
                10.1111/jsr.12961
                7540033
                31868978
                624d7cbb-767f-4c17-a641-effae3783dae
                © 2019 The Authors. Journal of Sleep Research published by John Wiley & Sons Ltd on behalf of European Sleep Research Society.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 16 June 2019
                : 13 November 2019
                : 13 November 2019
                Page count
                Figures: 6, Tables: 4, Pages: 12, Words: 9520
                Funding
                Funded by: Austrian Science Fund , open-funder-registry 10.13039/501100002428;
                Award ID: P25000‐B24
                Categories
                Regular Research Paper
                Sleep and Learning
                Custom metadata
                2.0
                October 2020
                Converter:WILEY_ML3GV2_TO_JATSPMC version:5.9.2 mode:remove_FC converted:07.10.2020

                gross motor learning,motor memory consolidation,rapid eye movement,sleep spindles

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