Sensorimotor feedback loops are selectively sensitive to reward.

human motor control neuroscience proprioception reinforcement learning sensorimotor feedback vision

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
13 01 2023
Historique:
received: 05 07 2022
accepted: 29 12 2022
pubmed: 14 1 2023
medline: 14 2 2023
entrez: 13 1 2023
Statut: epublish

Résumé

Although it is well established that motivational factors such as earning more money for performing well improve motor performance, how the motor system implements this improvement remains unclear. For instance, feedback-based control, which uses sensory feedback from the body to correct for errors in movement, improves with greater reward. But feedback control encompasses many feedback loops with diverse characteristics such as the brain regions involved and their response time. Which specific loops drive these performance improvements with reward is unknown, even though their diversity makes it unlikely that they are contributing uniformly. We systematically tested the effect of reward on the latency (how long for a corrective response to arise?) and gain (how large is the corrective response?) of seven distinct sensorimotor feedback loops in humans. Only the fastest feedback loops were insensitive to reward, and the earliest reward-driven changes were consistently an increase in feedback gains, not a reduction in latency. Rather, a reduction of response latencies only tended to occur in slower feedback loops. These observations were similar across sensory modalities (vision and proprioception). Our results may have implications regarding feedback control performance in athletic coaching. For instance, coaching methodologies that rely on reinforcement or 'reward shaping' may need to specifically target aspects of movement that rely on reward-sensitive feedback responses.

Identifiants

pubmed: 36637162
doi: 10.7554/eLife.81325
pii: 81325
pmc: PMC9910828
doi:
pii:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : CIHR
ID : PJT-156241
Pays : Canada

Informations de copyright

© 2023, Codol et al.

Déclaration de conflit d'intérêts

OC, MK, CF, JG, JP, PG No competing interests declared

Références

Brain. 2004 Aug;127(Pt 8):1755-73
pubmed: 15215215
J Physiol. 1956 Apr 27;132(1):17-8P
pubmed: 13320395
Nat Neurosci. 2009 Nov;12(11):1444-9
pubmed: 19801988
J Neurophysiol. 1976 Sep;39(5):1069-80
pubmed: 824410
J Neurophysiol. 2015 Dec;114(6):3242-54
pubmed: 26445871
J Neurophysiol. 1987 Feb;57(2):443-59
pubmed: 3559687
J Physiol. 1993 May;464:575-93
pubmed: 8229819
J Neurosci. 2015 Apr 1;35(13):5109-17
pubmed: 25834038
Exp Brain Res. 2012 May;218(3):341-59
pubmed: 22370742
Nat Neurosci. 2000 Aug;3(8):827-30
pubmed: 10903577
J Neurosci. 2019 May 15;39(20):3906-3920
pubmed: 30850511
Behav Brain Res. 2011 May 16;219(1):8-14
pubmed: 21138745
eNeuro. 2022 Mar 28;9(2):
pubmed: 35277452
Electroencephalogr Clin Neurophysiol. 1991 Oct;81(5):353-8
pubmed: 1718721
Trends Cogn Sci. 2014 Apr;18(4):194-202
pubmed: 24581556
Elife. 2017 Jul 28;6:
pubmed: 28753125
J Neurosci. 2014 Jan 29;34(5):1769-80
pubmed: 24478359
Neural Comput. 2005 May;17(5):1084-108
pubmed: 15829101
Neuron. 2019 Jul 17;103(2):335-348.e5
pubmed: 31174960
J Rehabil Res Dev. 2014;51(2):213-27
pubmed: 24933720
J Abnorm Child Psychol. 1983 Jun;11(2):313-26
pubmed: 6619440
Neuroscience. 2021 Nov 1;475:163-184
pubmed: 34302907
Nat Neurosci. 2019 Apr;22(4):529-533
pubmed: 30742115
Curr Biol. 2021 Apr 12;31(7):1476-1487.e5
pubmed: 33592191
Cereb Cortex. 2021 Nov 23;32(1):231-247
pubmed: 34231854
J Physiol. 1992 Apr;449:429-40
pubmed: 1522516
J Neurosci Methods. 1990 Feb;31(2):145-52
pubmed: 2319815
J Neurophysiol. 2008 Jul;100(1):224-38
pubmed: 18463184
Neuron. 2020 Apr 22;106(2):329-339.e4
pubmed: 32053768
J Physiol. 1991 Feb;433:41-57
pubmed: 1841949
Exp Brain Res. 2008 Mar;185(3):359-81
pubmed: 18251019
Acta Physiol Scand. 1994 Dec;152(4):351-63
pubmed: 7701936
Brain. 2007 Apr;130(Pt 4):887-94
pubmed: 17438014
PLoS Comput Biol. 2018 Jul 6;14(7):e1006304
pubmed: 29979685
PLoS Comput Biol. 2017 Apr 24;13(4):e1005503
pubmed: 28437451
J Neurophysiol. 2016 Nov 1;116(5):2236-2249
pubmed: 27535378
Trends Neurosci. 2020 Dec;43(12):980-997
pubmed: 33092893
Neuron. 2018 Jun 6;98(5):1005-1019.e5
pubmed: 29879384
Trends Neurosci. 2016 Aug;39(8):512-526
pubmed: 27378546
PLoS Biol. 2007 Nov;5(11):e316
pubmed: 18044990
J Neurosci. 2008 Mar 12;28(11):2804-13
pubmed: 18337410
J Neurosci. 2018 May 9;38(19):4521-4530
pubmed: 29650698
Exp Brain Res. 2020 Aug;238(7-8):1781-1793
pubmed: 32274520
J Physiol. 1984 Apr;349:249-72
pubmed: 6737294
Nat Commun. 2016 Oct 27;7:13239
pubmed: 27807345
Nat Neurosci. 2015 Apr;18(4):597-602
pubmed: 25706473
Neuron. 2006 Dec 21;52(6):1085-96
pubmed: 17178410
Eur J Neurosci. 2010 Sep;32(6):1049-57
pubmed: 20726884
Neuropsychologia. 2019 Feb 4;123:19-29
pubmed: 30005926
Sci Rep. 2019 Dec 27;9(1):20053
pubmed: 31882745
Atten Percept Psychophys. 2019 Oct;81(7):2265-2287
pubmed: 31161495
Elife. 2023 Jan 13;12:
pubmed: 36637162
J Neurosci. 2020 Apr 29;40(18):3604-3620
pubmed: 32234779
Nature. 2011 Sep 28;478(7369):387-90
pubmed: 21964335
J Neurophysiol. 2021 Apr 1;125(4):1339-1347
pubmed: 33689494
J Neurosci. 2014 Mar 26;34(13):4608-17
pubmed: 24672006
Psychon Bull Rev. 2010 Dec;17(6):821-6
pubmed: 21169575
J Neurol Neurosurg Psychiatry. 2017 Sep;88(9):730-736
pubmed: 28377451
Hum Brain Mapp. 2009 Feb;30(2):575-87
pubmed: 18172849
J Physiol. 1992 Oct;456:373-91
pubmed: 1338100
J Neurosci. 2012 Jan 18;32(3):890-902
pubmed: 22262887
Trends Cogn Sci. 2012 Nov;16(11):541-9
pubmed: 23031541
Curr Biol. 2015 Jun 29;25(13):1707-16
pubmed: 26096975
Elife. 2016 Apr 14;5:
pubmed: 27077949
Sci Rep. 2021 Jun 15;11(1):12544
pubmed: 34131162
Ann N Y Acad Sci. 2019 Sep;1452(1):34-51
pubmed: 31294872
J Neurophysiol. 2018 Jun 1;119(6):2347-2357
pubmed: 29537911
Neuron. 2019 Sep 4;103(5):934-947.e5
pubmed: 31320220
Biol Cybern. 2012 Dec;106(11-12):757-65
pubmed: 22895830
Science. 2001 Jan 12;291(5502):260-3
pubmed: 11253215
J Neurosci. 2013 Jun 26;33(26):10898-909
pubmed: 23804109
Curr Biol. 2020 Sep 21;30(18):R1025-R1030
pubmed: 32961152
J Neurosci. 2012 Feb 15;32(7):2276-86
pubmed: 22396403
Nat Neurosci. 2004 Sep;7(9):907-15
pubmed: 15332089
Nat Neurosci. 2013 Dec;16(12):1857-1863
pubmed: 24162654
Brain. 2001 Sep;124(Pt 9):1832-40
pubmed: 11522585
J Neurophysiol. 2020 Mar 1;123(3):1193-1205
pubmed: 32101490
Nature. 1999 Oct 7;401(6753):590-4
pubmed: 10524626
Science. 1997 Mar 14;275(5306):1593-9
pubmed: 9054347
Psychol Sci. 2017 Jul;28(7):1016-1026
pubmed: 28488927
J Neurosci. 2018 Dec 5;38(49):10505-10514
pubmed: 30355628

Auteurs

Olivier Codol (O)

Brain and Mind Institute, University of Western Ontario, London, Canada.
Department of Psychology, University of Western Ontario, London, Canada.
School of Psychology, University of Birmingham, Birmingham, United Kingdom.

Mehrdad Kashefi (M)

Brain and Mind Institute, University of Western Ontario, London, Canada.
Department of Psychology, University of Western Ontario, London, Canada.
Department of Physiology & Pharmacology, Schulich School of Medicine & Dentistry, University of Western Ontario, Ontario, Canada.
Robarts Research Institute, University of Western Ontario, London, Canada.

Christopher J Forgaard (CJ)

Brain and Mind Institute, University of Western Ontario, London, Canada.
Department of Psychology, University of Western Ontario, London, Canada.

Joseph M Galea (JM)

School of Psychology, University of Birmingham, Birmingham, United Kingdom.

J Andrew Pruszynski (JA)

Brain and Mind Institute, University of Western Ontario, London, Canada.
Department of Psychology, University of Western Ontario, London, Canada.
Department of Physiology & Pharmacology, Schulich School of Medicine & Dentistry, University of Western Ontario, Ontario, Canada.
Robarts Research Institute, University of Western Ontario, London, Canada.

Paul L Gribble (PL)

Brain and Mind Institute, University of Western Ontario, London, Canada.
Department of Psychology, University of Western Ontario, London, Canada.
Department of Physiology & Pharmacology, Schulich School of Medicine & Dentistry, University of Western Ontario, Ontario, Canada.
Haskins Laboratories, New Haven, United States.

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