Acquisition and consolidation of sequential footstep movements with physical and motor imagery practice.


Journal

Scandinavian journal of medicine & science in sports
ISSN: 1600-0838
Titre abrégé: Scand J Med Sci Sports
Pays: Denmark
ID NLM: 9111504

Informations de publication

Date de publication:
Dec 2020
Historique:
received: 19 02 2020
revised: 01 07 2020
accepted: 24 07 2020
pubmed: 11 8 2020
medline: 13 4 2021
entrez: 11 8 2020
Statut: ppublish

Résumé

Sleep-dependent performance enhancement has been consistently reported after explicit sequential finger learning, even using motor imagery practice (MIP), but whether similar sleep benefits occur after explicit sequential gross motor learning with the lower limbs has been addressed less often. Here, we investigated both acquisition and consolidation processes in an innovative sequential footstep task performed either physically or mentally. Forty-eight healthy young participants were tested before and after physical practice (PP) or MIP on the footstep task, following either a night of sleep (PPsleep and MIPsleep groups) or an equivalent daytime period (PPday and MIPday groups). Results showed that all groups improved motor performance following the acquisition session, albeit the magnitude of enhancement in the MIP groups remained lower relative to the PP groups. Importantly, only the MIPsleep group further improved performance after a night of sleep, while the other groups stabilized their performance after consolidation. Together, these findings demonstrate a sleep-dependent gain in performance after MIP in a sequential motor task with the lower limbs but not after PP. Overall, the present study is of particular importance in the context of motor learning and functional rehabilitation.

Identifiants

pubmed: 32777113
doi: 10.1111/sms.13799
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2477-2484

Informations de copyright

© 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.

Références

Doyon J. Motor sequence learning and movement disorders. Curr Opin Neurol. 2008;21(4):478-483.
King BR, Hoedlmoser K, Hirschauer F, Dolfen N, Albouy G. Sleeping on the motor engram: the multifaceted nature of sleep-related motor memory consolidation. Neurosci Biobehav Rev. 2017;80:1-22.
Christova M, Aftenberger H, Nardone R. Adult gross motor learning and sleep: is there a mutual benefit? Neural Plast. 2018;2018:3076986.
Hoedlmoser K, Birklbauer J, Schabus M, Eibenberger P, Rigler S, Mueller E. The impact of diurnal sleep on the consolidation of a complex gross motor adaptation task. J Sleep Res. 2015;24(1):100-109.
Blischke K, Malangre A. Task complexity modulates sleep-related offline learning in sequential motor skills. Front Hum Neurosci. 2017;11:374.
Lugassy D, Herszage J, Pilo R, Brosh T, Censor N. Consolidation of complex motor skill learning: evidence for a delayed offline process. Sleep. 2018;41(9).
Genzel L, Quack A, Jager E, Konrad B, Steiger A, Dresler M. Complex motor sequence skills profit from sleep. Neuropsychobiology. 2012;66(4):237-243.
Debarnot U, Sperduti M, Di Rienzo F, Guillot A. Experts bodies, experts minds: how physical and mental training shape the brain. Front Hum Neurosci. 2014;8:280.
Jeannerod M. Mental imagery in the motor context. Neuropsychologia. 1995;33(11):1419-1432.
Holmes PS, Collins DJ. The PETTLEP approach to motor imagery: a functional equivalence model for sport psychologists. J Appl Sport Psychol. 2001;13:60-83.
Hetu S, Gregoire M, Saimpont A, et al. The neural network of motor imagery: an ALE meta-analysis. Neurosci Biobehav Rev. 2013;37(5):930-949.
Kraeutner SN, MacKenzie LA, Westwood DA, Boe SG. Characterizing skill acquisition through motor imagery with no prior physical practice. Journal of experimental psychology. Human Percept Perform. 2016;42(2):257-265.
Mulder T, Zijlstra S, Zijlstra W, Hochstenbach J. The role of motor imagery in learning a totally novel movement. Exp Brain Res. 2004;154(2):211-217.
Bonassi G, Biggio M, Bisio A. Provision of somatosensory inputs during motor imagery enhances learning-induced plasticity in human motor cortex. Sci Rep. 2017;7(1):9300.
Debarnot U, Creveaux T, Collet C, Doyon J, Guillot A. Sleep contribution to motor memory consolidation: a motor imagery study. Sleep. 2009;32(12):1559-1565.
Debarnot U, Maley L, Rossi DD, Guillot A. Motor interference does not impair the memory consolidation of imagined movements. Brain Cogn. 2010;74(1):52-57.
Pavlik K, Nordin-Bates S. Imagery in Dance: A Literature Review. J Dance Med Sci. 2016;20(2):51-63.
Di Rienzo F, Collet C, Hoyek N, Guillot A. Impact of neurologic deficits on motor imagery: a systematic review of clinical evaluations. Neuropsychol Rev. 2014;24(2):116-147.
Elias LJ, Bryden MP, Bulman-Fleming MB. Footedness is a better predictor than is handedness of emotional lateralization. Neuropsychologia. 1998;36(1):37-43.
Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ. The Pittsburgh sleep quality index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193-213.
Horne JA, Ostberg O. A self-assessment questionnaire to determine morningness-eveningness in human circadian rhythms. Int J Chronobiol. 1976;4(2):97-110.
Malouin F, Richards CL, Jackson PL, Lafleur MF, Durand A, Doyon J. The Kinesthetic and Visual Imagery Questionnaire (KVIQ) for assessing motor imagery in persons with physical disabilities: a reliability and construct validity study. JNPT. 2007;31(1):20-29.
Milner B. Interhemispheric differences in the localization of psychological processes in man. Br Med Bull. 1971;27(3):272-277.
Hoddes E, Dement WC, Zarcone V. The development and use of the Stanford sleepiness scale. Psychophysiology. 1972;9:150.
Lafleur MF, Jackson PL, Malouin F, Richards CL, Evans AC, Doyon J. Motor learning produces parallel dynamic functional changes during the execution and imagination of sequential foot movements. NeuroImage. 2002;16(1):142-157.
Feltz D, Landers DM, Becker BJ. A revised meta-analysis of the mental practice literature on motor skill learning. In: Druckmann D, Swets JA, eds. Enhancing Human Performance: Issues, Theories, and Techniques. Washington, DC: National Academy Press; 1988:61-101.
Pan SC, Rickard TC. Sleep and motor learning: is there room for consolidation? Psychol Bull. 2015;141(4):812-834.
Nettersheim A, Hallschmid M, Born J, Diekelmann S. The role of sleep in motor sequence consolidation: stabilization rather than enhancement. J Neurosci. 2015;35(17):6696-6702.
Landry S, Anderson C, Conduit R. The effects of sleep, wake activity and time-on-task on offline motor sequence learning. Neurobiol Learn Mem. 2016;127:56-63.
Rickard TC, Cai DJ, Rieth CA, Jones J, Ard MC. Sleep does not enhance motor sequence learning. J Exp Psychol. Learn, Mem Cogn. 2008;34(4):834-842.
Walker MP, Brakefield T, Morgan A, Hobson JA, Stickgold R. Practice with sleep makes perfect: sleep-dependent motor skill learning. Neuron. 2002;35(1):205-211.
Carrier J, Monk TH. Circadian rhythms of performance: new trends. Chronobiol Int. 2000;17(6):719-732.
Hull JT, Wright KP Jr, Czeisler CA. The influence of subjective alertness and motivation on human performance independent of circadian and homeostatic regulation. J Biol Rhythms. 2003;18(4):329-338.
Debarnot U, Sahraoui D, Champely S, Collet C, Guillot A. Selective influence of circadian modulation and task characteristics on motor imagery time. Res Q Exerc Sport. 2012;83(3):442-450.
Wulf G, Shea CH. Principles derived from the study of simple skills do not generalize to complex skill learning. Psychon Bull Rev. 2002;9(2):185-211.
Magill RA. Motor Learning and Control, Vol. 9. New York, NY: McGraw-Hill; 2011.
Arima M, Shimodozono M, Etoh S, Tanaka N, Kawahira K. Examining procedural consolidation with visuomotor learning in the lower limb. Int J Neurosci. 2010;120(5):344-351.
Tjernstrom F, Fransson PA, Magnusson M. Improved postural control through repetition and consolidation. J Vestib Res. 2005;15(1):31-39.
Elion O, Sela I, Bahat Y, Siev-Ner I, Weiss PL, Karni A. Balance maintenance as an acquired motor skill: delayed gains and robust retention after a single session of training in a virtual environment. Brain Res. 2015;1609:54-62.
Hauptmann B, Reinhart E, Brandt SA, Karni A. The predictive value of the leveling off of within session performance for procedural memory consolidation. Brain Res Cogn Brain Res. 2005;24(2):181-189.
Debarnot U, Castellani E, Valenza G, Sebastiani L, Guillot A. Daytime naps improve motor imagery learning. Cogn, Affect Behav Neurosci. 2011;11(4):541-550.
Debarnot U, Castellani E, Guillot A. Selective delayed gains following motor imagery of complex movements. Arch Ital Biol. 2012;150(4):238-250.
Debarnot U, Abichou K, Kalenzaga S, Sperduti M, Piolino P. Variable motor imagery training induces sleep memory consolidation and transfer improvements. Neurobiol Learn Mem. 2015;119:85-92.
Kuriyama K, Mishima K, Suzuki H, Aritake S, Uchiyama M. Sleep accelerates the improvement in working memory performance. J Neurosci. 2008;28(40):10145-10150.
Ferrarelli F, Kaskie R, Laxminarayan S, Ramakrishnan S, Reifman J, Germain A. An increase in sleep slow waves predicts better working memory performance in healthy individuals. NeuroImage. 2019;191:1-9.

Auteurs

Emilie Freitas (E)

Inter-University Laboratory of Human Movement Biology-EA 7424, University Claude Bernard-Lyon1, University of Lyon, Villeurbanne, France.

Arnaud Saimpont (A)

Inter-University Laboratory of Human Movement Biology-EA 7424, University Claude Bernard-Lyon1, University of Lyon, Villeurbanne, France.

Yoann Blache (Y)

Inter-University Laboratory of Human Movement Biology-EA 7424, University Claude Bernard-Lyon1, University of Lyon, Villeurbanne, France.

Ursula Debarnot (U)

Inter-University Laboratory of Human Movement Biology-EA 7424, University Claude Bernard-Lyon1, University of Lyon, Villeurbanne, France.

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