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Elevated representational similarity of voluntary action and inhibition in Tourette syndrome

Many people with Tourette syndrome are able to volitionally suppress tics, under certain circumstances. To understand better the neural mechanisms that underlie this ability, we used functional magnetic resonance neuroimaging to track regional brain activity during performance of an intentional inhi...

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Autores principales: Rae, Charlotte L, Raykov, Petar, Ambridge, Eleanor M, Colling, Lincoln J, Gould van Praag, Cassandra D, Bouyagoub, Samira, Polanski, Liliana, Larsson, Dennis E O, Critchley, Hugo D
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10497185/
https://www.ncbi.nlm.nih.gov/pubmed/37705680
http://dx.doi.org/10.1093/braincomms/fcad224
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author Rae, Charlotte L
Raykov, Petar
Ambridge, Eleanor M
Colling, Lincoln J
Gould van Praag, Cassandra D
Bouyagoub, Samira
Polanski, Liliana
Larsson, Dennis E O
Critchley, Hugo D
author_facet Rae, Charlotte L
Raykov, Petar
Ambridge, Eleanor M
Colling, Lincoln J
Gould van Praag, Cassandra D
Bouyagoub, Samira
Polanski, Liliana
Larsson, Dennis E O
Critchley, Hugo D
author_sort Rae, Charlotte L
collection PubMed
description Many people with Tourette syndrome are able to volitionally suppress tics, under certain circumstances. To understand better the neural mechanisms that underlie this ability, we used functional magnetic resonance neuroimaging to track regional brain activity during performance of an intentional inhibition task. On some trials, Tourette syndrome and comparison participants internally chose to make or withhold a motor action (a button press), while on other trials, they followed ‘Go’ and ‘NoGo’ instructions to make or withhold the same action. Using representational similarity analysis, a functional magnetic resonance neuroimaging multivariate pattern analysis technique, we assessed how Tourette syndrome and comparison participants differed in neural activity when choosing to make or to withhold an action, relative to externally cued responses on Go and NoGo trials. Analyses were pre-registered, and the data and code are publicly available. We considered similarity of action representations within regions implicated as critical to motor action release or inhibition and to symptom expression in Tourette syndrome, namely the pre-supplementary motor area, inferior frontal gyrus, insula, caudate nucleus and primary motor cortex. Strikingly, in the Tourette syndrome compared to the comparison group, neural activity within the pre-supplementary motor area displayed greater representational similarity across all action types. Within the pre-supplementary motor area, there was lower response-specific differentiation of activity relating to action and inhibition plans and to internally chosen and externally cued actions, implicating the region as a functional nexus in the symptomatology of Tourette syndrome. Correspondingly, patients with Tourette syndrome may experience volitional tic suppression as an effortful and tiring process because, at the top of the putative motor decision hierarchy, activity within the population of neurons facilitating action is overly similar to activity within the population of neurons promoting inhibition. However, not all pre-supplementary motor area group differences survived correction for multiple comparisons. Group differences in representational similarity were also present in the primary motor cortex. Here, representations of internally chosen and externally cued inhibition were more differentiated in the Tourette syndrome group than in the comparison group, potentially a consequence of a weaker voluntary capacity earlier in the motor hierarchy to suppress actions proactively. Tic severity and premonitory sensations correlated with primary motor cortex and caudate nucleus representational similarity, but these effects did not survive correction for multiple comparisons. In summary, more rigid pre-supplementary motor area neural coding across action categories may constitute a central feature of Tourette syndrome, which can account for patients’ experience of ‘unvoluntary’ tics and effortful tic suppression.
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spelling pubmed-104971852023-09-13 Elevated representational similarity of voluntary action and inhibition in Tourette syndrome Rae, Charlotte L Raykov, Petar Ambridge, Eleanor M Colling, Lincoln J Gould van Praag, Cassandra D Bouyagoub, Samira Polanski, Liliana Larsson, Dennis E O Critchley, Hugo D Brain Commun Original Article Many people with Tourette syndrome are able to volitionally suppress tics, under certain circumstances. To understand better the neural mechanisms that underlie this ability, we used functional magnetic resonance neuroimaging to track regional brain activity during performance of an intentional inhibition task. On some trials, Tourette syndrome and comparison participants internally chose to make or withhold a motor action (a button press), while on other trials, they followed ‘Go’ and ‘NoGo’ instructions to make or withhold the same action. Using representational similarity analysis, a functional magnetic resonance neuroimaging multivariate pattern analysis technique, we assessed how Tourette syndrome and comparison participants differed in neural activity when choosing to make or to withhold an action, relative to externally cued responses on Go and NoGo trials. Analyses were pre-registered, and the data and code are publicly available. We considered similarity of action representations within regions implicated as critical to motor action release or inhibition and to symptom expression in Tourette syndrome, namely the pre-supplementary motor area, inferior frontal gyrus, insula, caudate nucleus and primary motor cortex. Strikingly, in the Tourette syndrome compared to the comparison group, neural activity within the pre-supplementary motor area displayed greater representational similarity across all action types. Within the pre-supplementary motor area, there was lower response-specific differentiation of activity relating to action and inhibition plans and to internally chosen and externally cued actions, implicating the region as a functional nexus in the symptomatology of Tourette syndrome. Correspondingly, patients with Tourette syndrome may experience volitional tic suppression as an effortful and tiring process because, at the top of the putative motor decision hierarchy, activity within the population of neurons facilitating action is overly similar to activity within the population of neurons promoting inhibition. However, not all pre-supplementary motor area group differences survived correction for multiple comparisons. Group differences in representational similarity were also present in the primary motor cortex. Here, representations of internally chosen and externally cued inhibition were more differentiated in the Tourette syndrome group than in the comparison group, potentially a consequence of a weaker voluntary capacity earlier in the motor hierarchy to suppress actions proactively. Tic severity and premonitory sensations correlated with primary motor cortex and caudate nucleus representational similarity, but these effects did not survive correction for multiple comparisons. In summary, more rigid pre-supplementary motor area neural coding across action categories may constitute a central feature of Tourette syndrome, which can account for patients’ experience of ‘unvoluntary’ tics and effortful tic suppression. Oxford University Press 2023-08-24 /pmc/articles/PMC10497185/ /pubmed/37705680 http://dx.doi.org/10.1093/braincomms/fcad224 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 Original Article
Rae, Charlotte L
Raykov, Petar
Ambridge, Eleanor M
Colling, Lincoln J
Gould van Praag, Cassandra D
Bouyagoub, Samira
Polanski, Liliana
Larsson, Dennis E O
Critchley, Hugo D
Elevated representational similarity of voluntary action and inhibition in Tourette syndrome
title Elevated representational similarity of voluntary action and inhibition in Tourette syndrome
title_full Elevated representational similarity of voluntary action and inhibition in Tourette syndrome
title_fullStr Elevated representational similarity of voluntary action and inhibition in Tourette syndrome
title_full_unstemmed Elevated representational similarity of voluntary action and inhibition in Tourette syndrome
title_short Elevated representational similarity of voluntary action and inhibition in Tourette syndrome
title_sort elevated representational similarity of voluntary action and inhibition in tourette syndrome
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10497185/
https://www.ncbi.nlm.nih.gov/pubmed/37705680
http://dx.doi.org/10.1093/braincomms/fcad224
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