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The Effect of Motivation on Movement: A Study of Bradykinesia in Parkinson’s Disease

BACKGROUND: Bradykinesia is a cardinal feature of Parkinson’s disease (PD). Despite its disabling impact, the precise cause of this symptom remains elusive. Recent thinking suggests that bradykinesia may be more than simply a manifestation of motor slowness, and may in part reflect a specific defici...

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Autores principales: Shiner, Tamara, Seymour, Ben, Symmonds, Mkael, Dayan, Peter, Bhatia, Kailash P., Dolan, Raymond J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2012
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3471921/
https://www.ncbi.nlm.nih.gov/pubmed/23077557
http://dx.doi.org/10.1371/journal.pone.0047138
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author Shiner, Tamara
Seymour, Ben
Symmonds, Mkael
Dayan, Peter
Bhatia, Kailash P.
Dolan, Raymond J.
author_facet Shiner, Tamara
Seymour, Ben
Symmonds, Mkael
Dayan, Peter
Bhatia, Kailash P.
Dolan, Raymond J.
author_sort Shiner, Tamara
collection PubMed
description BACKGROUND: Bradykinesia is a cardinal feature of Parkinson’s disease (PD). Despite its disabling impact, the precise cause of this symptom remains elusive. Recent thinking suggests that bradykinesia may be more than simply a manifestation of motor slowness, and may in part reflect a specific deficit in the operation of motivational vigour in the striatum. In this paper we test the hypothesis that movement time in PD can be modulated by the specific nature of the motivational salience of possible action-outcomes. METHODOLOGY/PRINCIPAL FINDINGS: We developed a novel movement time paradigm involving winnable rewards and avoidable painful electrical stimuli. The faster the subjects performed an action the more likely they were to win money (in appetitive blocks) or to avoid a painful shock (in aversive blocks). We compared PD patients when OFF dopaminergic medication with controls. Our key finding is that PD patients OFF dopaminergic medication move faster to avoid aversive outcomes (painful electric shocks) than to reap rewarding outcomes (winning money) and, unlike controls, do not speed up in the current trial having failed to win money in the previous one. We also demonstrate that sensitivity to distracting stimuli is valence specific. CONCLUSIONS/SIGNIFICANCE: We suggest this pattern of results can be explained in terms of low dopamine levels in the Parkinsonian state leading to an insensitivity to appetitive outcomes, and thus an inability to modulate movement speed in the face of rewards. By comparison, sensitivity to aversive stimuli is relatively spared. Our findings point to a rarely described property of bradykinesia in PD, namely its selective regulation by everyday outcomes.
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spelling pubmed-34719212012-10-17 The Effect of Motivation on Movement: A Study of Bradykinesia in Parkinson’s Disease Shiner, Tamara Seymour, Ben Symmonds, Mkael Dayan, Peter Bhatia, Kailash P. Dolan, Raymond J. PLoS One Research Article BACKGROUND: Bradykinesia is a cardinal feature of Parkinson’s disease (PD). Despite its disabling impact, the precise cause of this symptom remains elusive. Recent thinking suggests that bradykinesia may be more than simply a manifestation of motor slowness, and may in part reflect a specific deficit in the operation of motivational vigour in the striatum. In this paper we test the hypothesis that movement time in PD can be modulated by the specific nature of the motivational salience of possible action-outcomes. METHODOLOGY/PRINCIPAL FINDINGS: We developed a novel movement time paradigm involving winnable rewards and avoidable painful electrical stimuli. The faster the subjects performed an action the more likely they were to win money (in appetitive blocks) or to avoid a painful shock (in aversive blocks). We compared PD patients when OFF dopaminergic medication with controls. Our key finding is that PD patients OFF dopaminergic medication move faster to avoid aversive outcomes (painful electric shocks) than to reap rewarding outcomes (winning money) and, unlike controls, do not speed up in the current trial having failed to win money in the previous one. We also demonstrate that sensitivity to distracting stimuli is valence specific. CONCLUSIONS/SIGNIFICANCE: We suggest this pattern of results can be explained in terms of low dopamine levels in the Parkinsonian state leading to an insensitivity to appetitive outcomes, and thus an inability to modulate movement speed in the face of rewards. By comparison, sensitivity to aversive stimuli is relatively spared. Our findings point to a rarely described property of bradykinesia in PD, namely its selective regulation by everyday outcomes. Public Library of Science 2012-10-15 /pmc/articles/PMC3471921/ /pubmed/23077557 http://dx.doi.org/10.1371/journal.pone.0047138 Text en © 2012 Shiner et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Shiner, Tamara
Seymour, Ben
Symmonds, Mkael
Dayan, Peter
Bhatia, Kailash P.
Dolan, Raymond J.
The Effect of Motivation on Movement: A Study of Bradykinesia in Parkinson’s Disease
title The Effect of Motivation on Movement: A Study of Bradykinesia in Parkinson’s Disease
title_full The Effect of Motivation on Movement: A Study of Bradykinesia in Parkinson’s Disease
title_fullStr The Effect of Motivation on Movement: A Study of Bradykinesia in Parkinson’s Disease
title_full_unstemmed The Effect of Motivation on Movement: A Study of Bradykinesia in Parkinson’s Disease
title_short The Effect of Motivation on Movement: A Study of Bradykinesia in Parkinson’s Disease
title_sort effect of motivation on movement: a study of bradykinesia in parkinson’s disease
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3471921/
https://www.ncbi.nlm.nih.gov/pubmed/23077557
http://dx.doi.org/10.1371/journal.pone.0047138
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