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Moving, fast and slow: behavioural insights into bradykinesia in Parkinson’s disease

The debilitating symptoms of Parkinson’s disease, including the hallmark slowness of movement, termed bradykinesia, were described more than 100 years ago. Despite significant advances in elucidating the genetic, molecular and neurobiological changes in Parkinson’s disease, it remains conceptually u...

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Autores principales: Herz, Damian M, Brown, Peter
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10473574/
https://www.ncbi.nlm.nih.gov/pubmed/36864683
http://dx.doi.org/10.1093/brain/awad069
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author Herz, Damian M
Brown, Peter
author_facet Herz, Damian M
Brown, Peter
author_sort Herz, Damian M
collection PubMed
description The debilitating symptoms of Parkinson’s disease, including the hallmark slowness of movement, termed bradykinesia, were described more than 100 years ago. Despite significant advances in elucidating the genetic, molecular and neurobiological changes in Parkinson’s disease, it remains conceptually unclear exactly why patients with Parkinson’s disease move slowly. To address this, we summarize behavioural observations of movement slowness in Parkinson’s disease and discuss these findings in a behavioural framework of optimal control. In this framework, agents optimize the time it takes to gather and harvest rewards by adapting their movement vigour according to the reward that is at stake and the effort that needs to be expended. Thus, slow movements can be favourable when the reward is deemed unappealing or the movement very costly. While reduced reward sensitivity, which makes patients less inclined to work for reward, has been reported in Parkinson’s disease, this appears to be related mainly to motivational deficits (apathy) rather than bradykinesia. Increased effort sensitivity has been proposed to underlie movement slowness in Parkinson’s disease. However, careful behavioural observations of bradykinesia are inconsistent with abnormal computations of effort costs due to accuracy constraints or movement energetic expenditure. These inconsistencies can be resolved when considering that a general disability to switch between stable and dynamic movement states can contribute to an abnormal composite effort cost related to movement in Parkinson’s disease. This can account for paradoxical observations such as the abnormally slow relaxation of isometric contractions or difficulties in halting a movement in Parkinson’s disease, both of which increase movement energy expenditure. A sound understanding of the abnormal behavioural computations mediating motor impairment in Parkinson’s disease will be vital for linking them to their underlying neural dynamics in distributed brain networks and for grounding future experimental studies in well-defined behavioural frameworks.
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spelling pubmed-104735742023-09-02 Moving, fast and slow: behavioural insights into bradykinesia in Parkinson’s disease Herz, Damian M Brown, Peter Brain Review Article The debilitating symptoms of Parkinson’s disease, including the hallmark slowness of movement, termed bradykinesia, were described more than 100 years ago. Despite significant advances in elucidating the genetic, molecular and neurobiological changes in Parkinson’s disease, it remains conceptually unclear exactly why patients with Parkinson’s disease move slowly. To address this, we summarize behavioural observations of movement slowness in Parkinson’s disease and discuss these findings in a behavioural framework of optimal control. In this framework, agents optimize the time it takes to gather and harvest rewards by adapting their movement vigour according to the reward that is at stake and the effort that needs to be expended. Thus, slow movements can be favourable when the reward is deemed unappealing or the movement very costly. While reduced reward sensitivity, which makes patients less inclined to work for reward, has been reported in Parkinson’s disease, this appears to be related mainly to motivational deficits (apathy) rather than bradykinesia. Increased effort sensitivity has been proposed to underlie movement slowness in Parkinson’s disease. However, careful behavioural observations of bradykinesia are inconsistent with abnormal computations of effort costs due to accuracy constraints or movement energetic expenditure. These inconsistencies can be resolved when considering that a general disability to switch between stable and dynamic movement states can contribute to an abnormal composite effort cost related to movement in Parkinson’s disease. This can account for paradoxical observations such as the abnormally slow relaxation of isometric contractions or difficulties in halting a movement in Parkinson’s disease, both of which increase movement energy expenditure. A sound understanding of the abnormal behavioural computations mediating motor impairment in Parkinson’s disease will be vital for linking them to their underlying neural dynamics in distributed brain networks and for grounding future experimental studies in well-defined behavioural frameworks. Oxford University Press 2023-03-02 /pmc/articles/PMC10473574/ /pubmed/36864683 http://dx.doi.org/10.1093/brain/awad069 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Review Article
Herz, Damian M
Brown, Peter
Moving, fast and slow: behavioural insights into bradykinesia in Parkinson’s disease
title Moving, fast and slow: behavioural insights into bradykinesia in Parkinson’s disease
title_full Moving, fast and slow: behavioural insights into bradykinesia in Parkinson’s disease
title_fullStr Moving, fast and slow: behavioural insights into bradykinesia in Parkinson’s disease
title_full_unstemmed Moving, fast and slow: behavioural insights into bradykinesia in Parkinson’s disease
title_short Moving, fast and slow: behavioural insights into bradykinesia in Parkinson’s disease
title_sort moving, fast and slow: behavioural insights into bradykinesia in parkinson’s disease
topic Review Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10473574/
https://www.ncbi.nlm.nih.gov/pubmed/36864683
http://dx.doi.org/10.1093/brain/awad069
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