Sleep-related motor skill consolidation and generalizability after physical practice, motor imagery, and action observation.

Health sciences Medical imaging Medicine Neurology

Journal

iScience
ISSN: 2589-0042
Titre abrégé: iScience
Pays: United States
ID NLM: 101724038

Informations de publication

Date de publication:
18 Aug 2023
Historique:
received: 03 03 2023
revised: 15 05 2023
accepted: 04 07 2023
medline: 31 7 2023
pubmed: 31 7 2023
entrez: 31 7 2023
Statut: epublish

Résumé

Sleep benefits the consolidation of motor skills learned by physical practice, mainly through periodic thalamocortical sleep spindle activity. However, motor skills can be learned without overt movement through motor imagery or action observation. Here, we investigated whether sleep spindle activity also supports the consolidation of non-physically learned movements. Forty-five electroencephalographic sleep recordings were collected during a daytime nap after motor sequence learning by physical practice, motor imagery, or action observation. Our findings reveal that a temporal cluster-based organization of sleep spindles underlies motor memory consolidation in all groups, albeit with distinct behavioral outcomes. A daytime nap offers an early sleep window promoting the retention of motor skills learned by physical practice and motor imagery, and its generalizability toward the inter-manual transfer of skill after action observation. Findings may further have practical impacts with the development of non-physical rehabilitation interventions for patients having to remaster skills following peripherical or brain injury.

Identifiants

pubmed: 37520714
doi: 10.1016/j.isci.2023.107314
pii: S2589-0042(23)01391-3
pmc: PMC10374463
doi:

Types de publication

Journal Article

Langues

eng

Pagination

107314

Informations de copyright

© 2023 The Author(s).

Déclaration de conflit d'intérêts

The authors declare no competing interest.

Références

Acta Psychol (Amst). 2010 Oct;135(2):240-51
pubmed: 20673569
Nat Neurosci. 2007 Sep;10(9):1206-13
pubmed: 17694051
BMC Res Notes. 2009 Aug 26;2:170
pubmed: 19709401
Brain Res. 2006 May 23;1090(1):163-71
pubmed: 16677617
PLoS Biol. 2018 Mar 19;16(3):e2004633
pubmed: 29554094
Proc Natl Acad Sci U S A. 2009 Nov 10;106(45):18926-30
pubmed: 19884499
Proc Natl Acad Sci U S A. 2005 Dec 13;102(50):18237-41
pubmed: 16330773
Neuron. 2015 Oct 7;88(1):20-32
pubmed: 26447570
Neuropsychologia. 2021 Jan 8;150:107701
pubmed: 33276035
Brain Res. 2010 Jul 9;1343:93-103
pubmed: 20423702
Physiol Rev. 2020 Apr 1;100(2):805-868
pubmed: 31804897
Nat Rev Neurosci. 2012 Sep;13(9):658-64
pubmed: 22903222
Acta Psychol (Amst). 2009 Sep;132(1):54-61
pubmed: 19631919
Arch Ital Biol. 2012 Dec;150(4):238-50
pubmed: 23479457
Sci Adv. 2017 Feb 08;3(2):e1602026
pubmed: 28246641
J Neurosci. 1995 May;15(5 Pt 1):3526-38
pubmed: 7751928
J Exp Psychol Learn Mem Cogn. 2008 Jul;34(4):823-33
pubmed: 18605871
Psychon Bull Rev. 2018 Apr;25(2):643-650
pubmed: 28752378
J Cogn Neurosci. 1997 Jan;9(1):27-38
pubmed: 23968178
Nat Commun. 2015 Oct 28;6:8729
pubmed: 26507814
PLoS One. 2011;6(10):e26717
pubmed: 22046337
Neurobiol Learn Mem. 2015 Mar;119:85-92
pubmed: 25562401
Behav Neurosci. 2016 Apr;130(2):252-60
pubmed: 26854741
Hum Brain Mapp. 2013 Nov;34(11):2918-28
pubmed: 22674673
Q J Exp Psychol (Hove). 2011 Jun;64(6):1111-23
pubmed: 21302186
Comput Intell Neurosci. 2011;2011:879716
pubmed: 21584256
Curr Biol. 2018 Jun 4;28(11):1736-1743.e4
pubmed: 29804809
Neuroimage. 2010 Apr 15;50(3):1148-67
pubmed: 20056149
J Neurophysiol. 2010 Aug;104(2):774-83
pubmed: 20538766
Sleep. 2009 Dec;32(12):1559-65
pubmed: 20041591
Brain Cogn. 2021 Jun;150:105705
pubmed: 33652364
Neuroscience. 2006 Feb;137(3):761-72
pubmed: 16338093
Exp Brain Res. 2005 Aug;165(1):19-27
pubmed: 15883806
Psychol Res. 2012 Sep;76(5):611-25
pubmed: 21671102
Neuroimage. 2008 Jul 15;41(4):1471-83
pubmed: 18479943
PLoS One. 2016 Apr 06;11(4):e0152228
pubmed: 27050168
Learn Mem. 2006 Sep-Oct;13(5):580-3
pubmed: 16980543
Neurosci Biobehav Rev. 2018 Nov;94:31-44
pubmed: 30098990
J Neurosci Methods. 2019 Mar 15;316:22-34
pubmed: 30571990
J Bodyw Mov Ther. 2021 Oct;28:540-546
pubmed: 34776192
NPJ Sci Learn. 2020 Jun 4;5:7
pubmed: 32550003
Curr Biol. 2016 Aug 22;26(16):2127-36
pubmed: 27476602
Trends Neurosci. 2019 Jan;42(1):1-3
pubmed: 30340875
Front Behav Neurosci. 2015 Apr 28;9:105
pubmed: 25972791
Exp Brain Res. 2009 May;195(1):15-26
pubmed: 19277618
Psychol Bull. 2015 Jul;141(4):812-34
pubmed: 25822130
Neuron. 2002 Jul 3;35(1):205-11
pubmed: 12123620
PLoS One. 2017 Apr 19;12(4):e0174755
pubmed: 28422976
PLoS One. 2007 Apr 04;2(4):e341
pubmed: 17406665
Sleep. 2023 May 10;46(5):
pubmed: 36433753
Neuroimage. 2001 Jul;14(1 Pt 2):S103-9
pubmed: 11373140
Eur J Neurosci. 2008 Sep;28(6):1216-21
pubmed: 18783369
Neurosci Biobehav Rev. 2013 Jun;37(5):930-49
pubmed: 23583615
Sci Rep. 2017 Aug 24;7(1):9406
pubmed: 28839217
Q J Exp Psychol A. 2002 Apr;55(2):593-607
pubmed: 12047061
Cogn Affect Behav Neurosci. 2011 Dec;11(4):541-50
pubmed: 21842279
Front Hum Neurosci. 2016 Jun 28;10:315
pubmed: 27445755
Elife. 2019 Mar 05;8:
pubmed: 30832766
Sci Rep. 2021 Apr 26;11(1):8928
pubmed: 33903619
Elife. 2017 Sep 11;6:
pubmed: 28892464
J Physiol. 1997 Dec 15;505 ( Pt 3):851-8
pubmed: 9457658
J Neurosci. 2015 Apr 29;35(17):6696-702
pubmed: 25926448
J Exp Psychol Hum Percept Perform. 2009 Apr;35(2):390-407
pubmed: 19331496
Acta Psychol (Amst). 2010 Feb;133(2):119-26
pubmed: 19939342
Neuropsychologia. 1971 Mar;9(1):97-113
pubmed: 5146491
Philos Trans R Soc Lond B Biol Sci. 2020 May 25;375(1799):20190232
pubmed: 32248783
Sleep. 2018 Sep 1;41(9):
pubmed: 30137521
J Mot Behav. 2000 Sep;32(3):268-76
pubmed: 10975274
Br J Psychol. 2005 Aug;96(Pt 3):371-88
pubmed: 16131413
Compr Physiol. 2019 Mar 14;9(2):613-663
pubmed: 30873583
Neurosci Lett. 2014 Oct 3;581:69-74
pubmed: 25150928
PLoS Biol. 2016 Mar 31;14(3):e1002429
pubmed: 27032084
Exp Brain Res. 2011 Mar;209(2):181-92
pubmed: 21279634
Neuroimage. 2018 Apr 1;169:419-430
pubmed: 29277652
Neuroimage. 2018 Apr 1;169:57-68
pubmed: 29217404
Curr Biol. 2019 Apr 22;29(8):1346-1351.e4
pubmed: 30930043
Curr Biol. 2018 Jun 4;28(11):R656-R658
pubmed: 29870702
J Neurosci. 2010 Oct 20;30(42):13977-82
pubmed: 20962219
Psychol Bull. 1992 Jul;112(1):155-9
pubmed: 19565683
J Biol Rhythms. 2005 Aug;20(4):279-90
pubmed: 16077148
J Sleep Res. 2006 Sep;15(3):250-5
pubmed: 16911026
Curr Biol. 2012 Jan 24;22(2):R66-71
pubmed: 22280913

Auteurs

Adrien Conessa (A)

Université Paris-Saclay, CIAMS, 91405 Orsay, France.
Université d'Orléans, CIAMS, 45067 Orléans, France.

Ursula Debarnot (U)

University Lyon, UCBL-Lyon 1, Inter-University Laboratory of Human Movement Biology, EA7424, 69622 Villeurbanne, France.
Institut Universitaire de France, Paris, France.

Isabelle Siegler (I)

Université Paris-Saclay, CIAMS, 91405 Orsay, France.
Université d'Orléans, CIAMS, 45067 Orléans, France.

Arnaud Boutin (A)

Université Paris-Saclay, CIAMS, 91405 Orsay, France.
Université d'Orléans, CIAMS, 45067 Orléans, France.

Classifications MeSH