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Intact finger representation within primary sensorimotor cortex of musician’s dystonia

Musician’s dystonia presents with a persistent deterioration of motor control during musical performance. A predominant hypothesis has been that this is underpinned by maladaptive neural changes to the somatotopic organization of finger representations within primary somatosensory cortex. Here, we t...

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Autores principales: Sadnicka, Anna, Wiestler, Tobias, Butler, Katherine, Altenmüller, Eckart, Edwards, Mark J, Ejaz, Naveed, Diedrichsen, Jörn
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10115231/
https://www.ncbi.nlm.nih.gov/pubmed/36170332
http://dx.doi.org/10.1093/brain/awac356
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author Sadnicka, Anna
Wiestler, Tobias
Butler, Katherine
Altenmüller, Eckart
Edwards, Mark J
Ejaz, Naveed
Diedrichsen, Jörn
author_facet Sadnicka, Anna
Wiestler, Tobias
Butler, Katherine
Altenmüller, Eckart
Edwards, Mark J
Ejaz, Naveed
Diedrichsen, Jörn
author_sort Sadnicka, Anna
collection PubMed
description Musician’s dystonia presents with a persistent deterioration of motor control during musical performance. A predominant hypothesis has been that this is underpinned by maladaptive neural changes to the somatotopic organization of finger representations within primary somatosensory cortex. Here, we tested this hypothesis by investigating the finger-specific activity patterns in the primary somatosensory and motor cortex using functional MRI and multivariate pattern analysis in nine musicians with dystonia and nine healthy musicians. A purpose-built keyboard device allowed characterization of activity patterns elicited during passive extension and active finger presses of individual fingers. We analysed the data using both traditional spatial analysis and state-of-the art multivariate analyses. Our analysis reveals that digit representations in musicians were poorly captured by spatial analyses. An optimized spatial metric found clear somatotopy but no difference in the spatial geometry between fingers with dystonia. Representational similarity analysis was confirmed as a more reliable technique than all spatial metrics evaluated. Significantly, the dissimilarity architecture was equivalent for musicians with and without dystonia. No expansion or spatial shift of digit representation maps were found in the symptomatic group. Our results therefore indicate that the neural representation of generic finger maps in primary sensorimotor cortex is intact in musician’s dystonia. These results speak against the idea that task-specific dystonia is associated with a distorted hand somatotopy and lend weight to an alternative hypothesis that task-specific dystonia is due to a higher-order disruption of skill encoding. Such a formulation can better explain the task-specific deficit and offers alternative inroads for therapeutic interventions.
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spelling pubmed-101152312023-04-20 Intact finger representation within primary sensorimotor cortex of musician’s dystonia Sadnicka, Anna Wiestler, Tobias Butler, Katherine Altenmüller, Eckart Edwards, Mark J Ejaz, Naveed Diedrichsen, Jörn Brain Original Article Musician’s dystonia presents with a persistent deterioration of motor control during musical performance. A predominant hypothesis has been that this is underpinned by maladaptive neural changes to the somatotopic organization of finger representations within primary somatosensory cortex. Here, we tested this hypothesis by investigating the finger-specific activity patterns in the primary somatosensory and motor cortex using functional MRI and multivariate pattern analysis in nine musicians with dystonia and nine healthy musicians. A purpose-built keyboard device allowed characterization of activity patterns elicited during passive extension and active finger presses of individual fingers. We analysed the data using both traditional spatial analysis and state-of-the art multivariate analyses. Our analysis reveals that digit representations in musicians were poorly captured by spatial analyses. An optimized spatial metric found clear somatotopy but no difference in the spatial geometry between fingers with dystonia. Representational similarity analysis was confirmed as a more reliable technique than all spatial metrics evaluated. Significantly, the dissimilarity architecture was equivalent for musicians with and without dystonia. No expansion or spatial shift of digit representation maps were found in the symptomatic group. Our results therefore indicate that the neural representation of generic finger maps in primary sensorimotor cortex is intact in musician’s dystonia. These results speak against the idea that task-specific dystonia is associated with a distorted hand somatotopy and lend weight to an alternative hypothesis that task-specific dystonia is due to a higher-order disruption of skill encoding. Such a formulation can better explain the task-specific deficit and offers alternative inroads for therapeutic interventions. Oxford University Press 2022-09-28 /pmc/articles/PMC10115231/ /pubmed/36170332 http://dx.doi.org/10.1093/brain/awac356 Text en © The Author(s) 2022. Published by Oxford University Press on behalf of the Guarantors of Brain. https://creativecommons.org/licenses/by-nc/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Original Article
Sadnicka, Anna
Wiestler, Tobias
Butler, Katherine
Altenmüller, Eckart
Edwards, Mark J
Ejaz, Naveed
Diedrichsen, Jörn
Intact finger representation within primary sensorimotor cortex of musician’s dystonia
title Intact finger representation within primary sensorimotor cortex of musician’s dystonia
title_full Intact finger representation within primary sensorimotor cortex of musician’s dystonia
title_fullStr Intact finger representation within primary sensorimotor cortex of musician’s dystonia
title_full_unstemmed Intact finger representation within primary sensorimotor cortex of musician’s dystonia
title_short Intact finger representation within primary sensorimotor cortex of musician’s dystonia
title_sort intact finger representation within primary sensorimotor cortex of musician’s dystonia
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10115231/
https://www.ncbi.nlm.nih.gov/pubmed/36170332
http://dx.doi.org/10.1093/brain/awac356
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