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Altered sense of agency in Gilles de la Tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings

Current neurocognitive models of motor control postulate that accurate action monitoring is crucial for a normal experience of agency—the ability to attribute the authorship of our actions and their consequences to ourselves. Recent studies demonstrated that action monitoring is impaired in Gilles d...

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Autores principales: Zapparoli, Laura, Seghezzi, Silvia, Devoto, Francantonio, Mariano, Marika, Banfi, Giuseppe, Porta, Mauro, Paulesu, Eraldo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7772095/
https://www.ncbi.nlm.nih.gov/pubmed/33409491
http://dx.doi.org/10.1093/braincomms/fcaa204
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author Zapparoli, Laura
Seghezzi, Silvia
Devoto, Francantonio
Mariano, Marika
Banfi, Giuseppe
Porta, Mauro
Paulesu, Eraldo
author_facet Zapparoli, Laura
Seghezzi, Silvia
Devoto, Francantonio
Mariano, Marika
Banfi, Giuseppe
Porta, Mauro
Paulesu, Eraldo
author_sort Zapparoli, Laura
collection PubMed
description Current neurocognitive models of motor control postulate that accurate action monitoring is crucial for a normal experience of agency—the ability to attribute the authorship of our actions and their consequences to ourselves. Recent studies demonstrated that action monitoring is impaired in Gilles de la Tourette syndrome, a movement disorder characterized by motor and vocal tics. It follows that Tourette syndrome patients may suffer from a perturbed sense of agency, the hypothesis tested in this study. To this end, we recruited 25 Tourette syndrome patients and 25 matched healthy controls in a case-control behavioural and functional magnetic resonance imaging study. As an implicit index of the sense of agency, we measured the intentional binding phenomenon, i.e., the perceived temporal compression between voluntary movements and their external consequences. We found evidence of an impaired sense of agency in Tourette syndrome patients who, as a group, did not show a significant intentional binding. The more reduced was the individual intentional binding, the more severe were the motor symptoms. Specific differences between the two groups were also observed in terms of brain activation patterns. In the healthy controls group, the magnitude of the intentional binding was associated with the activity of a premotor–parietal–cerebellar network. This relationship was not present in the Tourette syndrome group, suggesting an altered activation of the agency brain network for self-generated acts. We conclude that the less accurate action monitoring described in Tourette syndrome also involves the assessment of the consequences of actions in the outside world. We discuss that this may lead to difficulties in distinguishing external consequences produced by their own actions from the ones caused by others in Tourette syndrome patients.
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spelling pubmed-77720952021-01-05 Altered sense of agency in Gilles de la Tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings Zapparoli, Laura Seghezzi, Silvia Devoto, Francantonio Mariano, Marika Banfi, Giuseppe Porta, Mauro Paulesu, Eraldo Brain Commun Original Article Current neurocognitive models of motor control postulate that accurate action monitoring is crucial for a normal experience of agency—the ability to attribute the authorship of our actions and their consequences to ourselves. Recent studies demonstrated that action monitoring is impaired in Gilles de la Tourette syndrome, a movement disorder characterized by motor and vocal tics. It follows that Tourette syndrome patients may suffer from a perturbed sense of agency, the hypothesis tested in this study. To this end, we recruited 25 Tourette syndrome patients and 25 matched healthy controls in a case-control behavioural and functional magnetic resonance imaging study. As an implicit index of the sense of agency, we measured the intentional binding phenomenon, i.e., the perceived temporal compression between voluntary movements and their external consequences. We found evidence of an impaired sense of agency in Tourette syndrome patients who, as a group, did not show a significant intentional binding. The more reduced was the individual intentional binding, the more severe were the motor symptoms. Specific differences between the two groups were also observed in terms of brain activation patterns. In the healthy controls group, the magnitude of the intentional binding was associated with the activity of a premotor–parietal–cerebellar network. This relationship was not present in the Tourette syndrome group, suggesting an altered activation of the agency brain network for self-generated acts. We conclude that the less accurate action monitoring described in Tourette syndrome also involves the assessment of the consequences of actions in the outside world. We discuss that this may lead to difficulties in distinguishing external consequences produced by their own actions from the ones caused by others in Tourette syndrome patients. Oxford University Press 2020-11-19 /pmc/articles/PMC7772095/ /pubmed/33409491 http://dx.doi.org/10.1093/braincomms/fcaa204 Text en © The Author(s) (2020). 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 Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/ (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
Zapparoli, Laura
Seghezzi, Silvia
Devoto, Francantonio
Mariano, Marika
Banfi, Giuseppe
Porta, Mauro
Paulesu, Eraldo
Altered sense of agency in Gilles de la Tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings
title Altered sense of agency in Gilles de la Tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings
title_full Altered sense of agency in Gilles de la Tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings
title_fullStr Altered sense of agency in Gilles de la Tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings
title_full_unstemmed Altered sense of agency in Gilles de la Tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings
title_short Altered sense of agency in Gilles de la Tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings
title_sort altered sense of agency in gilles de la tourette syndrome: behavioural, clinical and functional magnetic resonance imaging findings
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7772095/
https://www.ncbi.nlm.nih.gov/pubmed/33409491
http://dx.doi.org/10.1093/braincomms/fcaa204
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