Reexposure to a sensorimotor perturbation produces opposite effects on explicit and implicit learning processes.


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
03 2021
Historique:
received: 17 07 2020
accepted: 15 02 2021
revised: 17 03 2021
pubmed: 6 3 2021
medline: 27 7 2021
entrez: 5 3 2021
Statut: epublish

Résumé

The motor system demonstrates an exquisite ability to adapt to changes in the environment and to quickly reset when these changes prove transient. If similar environmental changes are encountered in the future, learning may be faster, a phenomenon known as savings. In studies of sensorimotor learning, a central component of savings is attributed to the explicit recall of the task structure and appropriate compensatory strategies. Whether implicit adaptation also contributes to savings remains subject to debate. We tackled this question by measuring, in parallel, explicit and implicit adaptive responses in a visuomotor rotation task, employing a protocol that typically elicits savings. While the initial rate of learning was faster in the second exposure to the perturbation, an analysis decomposing the 2 processes showed the benefit to be solely associated with explicit re-aiming. Surprisingly, we found a significant decrease after relearning in aftereffect magnitudes during no-feedback trials, a direct measure of implicit adaptation. In a second experiment, we isolated implicit adaptation using clamped visual feedback, a method known to eliminate the contribution of explicit learning processes. Consistent with the results of the first experiment, participants exhibited a marked reduction in the adaptation function, as well as an attenuated aftereffect when relearning from the clamped feedback. Motivated by these results, we reanalyzed data from prior studies and observed a consistent, yet unappreciated pattern of attenuation of implicit adaptation during relearning. These results indicate that explicit and implicit sensorimotor processes exhibit opposite effects upon relearning: Explicit learning shows savings, while implicit adaptation becomes attenuated.

Identifiants

pubmed: 33667219
doi: 10.1371/journal.pbio.3001147
pii: PBIOLOGY-D-20-02151
pmc: PMC7968744
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3001147

Subventions

Organisme : NICHD NIH HHS
ID : K12 HD055931
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS116883
Pays : United States

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

J Neurosci. 2015 Apr 1;35(13):5109-17
pubmed: 25834038
Curr Biol. 2014 May 19;24(10):1050-61
pubmed: 24794296
J Neurosci. 2019 Nov 13;39(46):9237-9250
pubmed: 31582527
eNeuro. 2016 Apr 29;3(2):
pubmed: 27280151
J Neurosci. 2006 Apr 5;26(14):3642-5
pubmed: 16597717
Cereb Cortex. 2015 Sep;25(9):3077-85
pubmed: 24846147
J Neurosci. 2011 Apr 6;31(14):5392-7
pubmed: 21471374
J Neurosci. 2020 Apr 8;40(15):3075-3088
pubmed: 32029533
J Neurophysiol. 2014 Apr;111(7):1444-54
pubmed: 24431403
Brain Cogn. 2014 Oct 17;92C:1-10
pubmed: 25463134
J Neurophysiol. 2017 Oct 1;118(4):2435-2447
pubmed: 28768744
Behav Neurosci. 1993 Dec;107(6):911-25
pubmed: 8136067
J Neurophysiol. 2012 Sep;108(6):1752-63
pubmed: 22773782
Nat Commun. 2019 Jan 3;10(1):40
pubmed: 30604759
J Neurophysiol. 2017 Jul 1;118(1):383-393
pubmed: 28404830
J Neurophysiol. 2021 Mar 3;:
pubmed: 33656948
J Neurophysiol. 2013 Feb;109(4):1164-73
pubmed: 23197450
Exp Brain Res. 2012 Apr;218(2):295-304
pubmed: 22430183
J Neurosci. 2010 Jul 7;30(27):9189-98
pubmed: 20610753
J Exp Psychol Anim Behav Process. 1992 Apr;18(2):182-92
pubmed: 1583447
Exp Brain Res. 1997 Jul;115(3):557-61
pubmed: 9262212
J Neurosci. 1997 Jan 1;17(1):409-19
pubmed: 8987766
J Neurosci. 2001 Jun 1;21(11):4081-9
pubmed: 11356896
Neurology. 1983 Jun;33(6):766-72
pubmed: 6682520
J Neurophysiol. 2020 Apr 1;123(4):1552-1565
pubmed: 32208878
J Neurophysiol. 2010 Apr;103(4):2275-84
pubmed: 20164398
J Neurosci. 2011 Oct 19;31(42):15136-43
pubmed: 22016547
J Neurophysiol. 2011 Jun;105(6):2843-51
pubmed: 21451054
J Neurophysiol. 2020 Oct 1;124(4):1122-1130
pubmed: 32902347
Biol Psychiatry. 2002 Nov 15;52(10):976-86
pubmed: 12437938
J Neurophysiol. 2008 Nov;100(5):2948-55
pubmed: 18784273
J Neurophysiol. 2009 Feb;101(2):655-64
pubmed: 19019979
J Neurosci. 2000 Dec 1;20(23):8916-24
pubmed: 11102502
J Neurosci. 2015 Oct 21;35(42):14386-96
pubmed: 26490874
Commun Biol. 2018 Mar 22;1:19
pubmed: 30271906
Neurobiol Learn Mem. 2014 Oct;114:148-54
pubmed: 24931828
Neuron. 2011 May 26;70(4):787-801
pubmed: 21609832
Brain. 1996 Aug;119 ( Pt 4):1183-98
pubmed: 8813282
J Neurophysiol. 2015 Aug;114(2):969-77
pubmed: 26063781
J Neurosci Methods. 2007 Aug 15;164(1):177-90
pubmed: 17517438
J Neurophysiol. 2017 Jan 1;117(1):412-428
pubmed: 27832611
J Neurophysiol. 2016 Aug 1;116(2):411-24
pubmed: 27121580
J Neurosci. 2004 Aug 25;24(34):7531-9
pubmed: 15329400
J Neurophysiol. 2020 Mar 1;123(3):1180-1192
pubmed: 32101495
J Cogn Neurosci. 2017 Jun;29(6):1061-1074
pubmed: 28195523
Eur J Neurosci. 2018 Dec;48(11):3397-3409
pubmed: 30339299
PLoS Biol. 2006 Jun;4(6):e179
pubmed: 16700627
Brain. 2019 Mar 1;142(3):662-673
pubmed: 30689760
Annu Rev Psychol. 2021 Jan 4;72:61-95
pubmed: 32976728
Neuropsychologia. 1971 Mar;9(1):97-113
pubmed: 5146491
J Neurophysiol. 2019 Apr 1;121(4):1575-1583
pubmed: 30840553
Elife. 2017 Feb 24;6:
pubmed: 28234229
J Neurosci. 2005 Jan 12;25(2):473-8
pubmed: 15647491
Neurobiol Aging. 2019 Aug;80:138-153
pubmed: 31170534
Science. 2014 Sep 12;345(6202):1349-53
pubmed: 25123484
Spat Vis. 1997;10(4):433-6
pubmed: 9176952
J Neurophysiol. 2008 Nov;100(5):2537-48
pubmed: 18596178
J Neurosci. 2014 Feb 19;34(8):3023-32
pubmed: 24553942
PLoS Comput Biol. 2011 Oct;7(10):e1002210
pubmed: 21998574
Biol Cybern. 1978 Apr 20;29(1):29-36
pubmed: 656477
J Neurophysiol. 2021 Jan 1;125(1):12-22
pubmed: 33236937
J Vis. 2008 Apr 23;8(4):20.1-19
pubmed: 18484859
Neural Comput. 2001 Oct;13(10):2201-20
pubmed: 11570996
Elife. 2019 Apr 29;8:
pubmed: 31033439
Brain Stimul. 2019 Jul - Aug;12(4):992-1000
pubmed: 30930208
J Neurophysiol. 2013 May;109(10):2632-44
pubmed: 23446696
Nature. 2000 Oct 12;407(6805):742-7
pubmed: 11048720
J Neurophysiol. 2015 Jun 1;113(10):3836-49
pubmed: 25855690
Nat Neurosci. 2007 Jun;10(6):779-86
pubmed: 17496891
Exp Brain Res. 2004 Jan;154(2):201-10
pubmed: 14608451
J Neurophysiol. 2007 Jul;98(1):54-62
pubmed: 17507504
J Neurophysiol. 2020 Jan 1;123(1):57-69
pubmed: 31721646
Cerebellum. 2010 Dec;9(4):580-6
pubmed: 20697860
J Neurosci. 2012 Mar 21;32(12):4230-9
pubmed: 22442085
J Neurophysiol. 2019 Sep 1;122(3):1050-1059
pubmed: 31389741

Auteurs

Guy Avraham (G)

Department of Psychology, University of California, Berkeley, Berkeley, California, United States of America.
Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, California, United States of America.

J Ryan Morehead (JR)

School of Psychology, University of Leeds, Leeds, United Kingdom.
John A. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts, United States of America.

Hyosub E Kim (HE)

Department of Physical Therapy, University of Delaware, Newark, Delaware, United States of America.
Department of Psychological and Brain Sciences, University of Delaware, Newark, Delaware, United States of America.

Richard B Ivry (RB)

Department of Psychology, University of California, Berkeley, Berkeley, California, United States of America.
Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, California, United States of America.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH