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Learning fast accurate movements requires intact frontostriatal circuits

The basal ganglia are known to play a crucial role in movement execution, but their importance for motor skill learning remains unclear. Obstacles to our understanding include the lack of a universally accepted definition of motor skill learning (definition confound), and difficulties in distinguish...

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Autores principales: Shabbott, Britne, Ravindran, Roshni, Schumacher, Joseph W., Wasserman, Paula B., Marder, Karen S., Mazzoni, Pietro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2013
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3826079/
https://www.ncbi.nlm.nih.gov/pubmed/24312037
http://dx.doi.org/10.3389/fnhum.2013.00752
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author Shabbott, Britne
Ravindran, Roshni
Schumacher, Joseph W.
Wasserman, Paula B.
Marder, Karen S.
Mazzoni, Pietro
author_facet Shabbott, Britne
Ravindran, Roshni
Schumacher, Joseph W.
Wasserman, Paula B.
Marder, Karen S.
Mazzoni, Pietro
author_sort Shabbott, Britne
collection PubMed
description The basal ganglia are known to play a crucial role in movement execution, but their importance for motor skill learning remains unclear. Obstacles to our understanding include the lack of a universally accepted definition of motor skill learning (definition confound), and difficulties in distinguishing learning deficits from execution impairments (performance confound). We studied how healthy subjects and subjects with a basal ganglia disorder learn fast accurate reaching movements. We addressed the definition and performance confounds by: (1) focusing on an operationally defined core element of motor skill learning (speed-accuracy learning), and (2) using normal variation in initial performance to separate movement execution impairment from motor learning abnormalities. We measured motor skill learning as performance improvement in a reaching task with a speed-accuracy trade-off. We compared the performance of subjects with Huntington's disease (HD), a neurodegenerative basal ganglia disorder, to that of premanifest carriers of the HD mutation and of control subjects. The initial movements of HD subjects were less skilled (slower and/or less accurate) than those of control subjects. To factor out these differences in initial execution, we modeled the relationship between learning and baseline performance in control subjects. Subjects with HD exhibited a clear learning impairment that was not explained by differences in initial performance. These results support a role for the basal ganglia in both movement execution and motor skill learning.
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spelling pubmed-38260792013-12-05 Learning fast accurate movements requires intact frontostriatal circuits Shabbott, Britne Ravindran, Roshni Schumacher, Joseph W. Wasserman, Paula B. Marder, Karen S. Mazzoni, Pietro Front Hum Neurosci Neuroscience The basal ganglia are known to play a crucial role in movement execution, but their importance for motor skill learning remains unclear. Obstacles to our understanding include the lack of a universally accepted definition of motor skill learning (definition confound), and difficulties in distinguishing learning deficits from execution impairments (performance confound). We studied how healthy subjects and subjects with a basal ganglia disorder learn fast accurate reaching movements. We addressed the definition and performance confounds by: (1) focusing on an operationally defined core element of motor skill learning (speed-accuracy learning), and (2) using normal variation in initial performance to separate movement execution impairment from motor learning abnormalities. We measured motor skill learning as performance improvement in a reaching task with a speed-accuracy trade-off. We compared the performance of subjects with Huntington's disease (HD), a neurodegenerative basal ganglia disorder, to that of premanifest carriers of the HD mutation and of control subjects. The initial movements of HD subjects were less skilled (slower and/or less accurate) than those of control subjects. To factor out these differences in initial execution, we modeled the relationship between learning and baseline performance in control subjects. Subjects with HD exhibited a clear learning impairment that was not explained by differences in initial performance. These results support a role for the basal ganglia in both movement execution and motor skill learning. Frontiers Media S.A. 2013-11-13 /pmc/articles/PMC3826079/ /pubmed/24312037 http://dx.doi.org/10.3389/fnhum.2013.00752 Text en Copyright © 2013 Shabbott, Ravindran, Schumacher, Wasserman, Marder and Mazzoni. http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Shabbott, Britne
Ravindran, Roshni
Schumacher, Joseph W.
Wasserman, Paula B.
Marder, Karen S.
Mazzoni, Pietro
Learning fast accurate movements requires intact frontostriatal circuits
title Learning fast accurate movements requires intact frontostriatal circuits
title_full Learning fast accurate movements requires intact frontostriatal circuits
title_fullStr Learning fast accurate movements requires intact frontostriatal circuits
title_full_unstemmed Learning fast accurate movements requires intact frontostriatal circuits
title_short Learning fast accurate movements requires intact frontostriatal circuits
title_sort learning fast accurate movements requires intact frontostriatal circuits
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3826079/
https://www.ncbi.nlm.nih.gov/pubmed/24312037
http://dx.doi.org/10.3389/fnhum.2013.00752
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