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Impaired automatic but intact volitional inhibition in primary tic disorders

The defining character of tics is that they can be transiently suppressed by volitional effort of will, and at a behavioural level this has led to the concept that tics result from a failure of inhibition. However, this logic conflates the mechanism responsible for the production of tics with that u...

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Autores principales: Rawji, Vishal, Modi, Sachin, Latorre, Anna, Rocchi, Lorenzo, Hockey, Leanne, Bhatia, Kailash, Joyce, Eileen, Rothwell, John C, Jahanshahi, Marjan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7089661/
https://www.ncbi.nlm.nih.gov/pubmed/32125364
http://dx.doi.org/10.1093/brain/awaa024
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author Rawji, Vishal
Modi, Sachin
Latorre, Anna
Rocchi, Lorenzo
Hockey, Leanne
Bhatia, Kailash
Joyce, Eileen
Rothwell, John C
Jahanshahi, Marjan
author_facet Rawji, Vishal
Modi, Sachin
Latorre, Anna
Rocchi, Lorenzo
Hockey, Leanne
Bhatia, Kailash
Joyce, Eileen
Rothwell, John C
Jahanshahi, Marjan
author_sort Rawji, Vishal
collection PubMed
description The defining character of tics is that they can be transiently suppressed by volitional effort of will, and at a behavioural level this has led to the concept that tics result from a failure of inhibition. However, this logic conflates the mechanism responsible for the production of tics with that used in suppressing them. Volitional inhibition of motor output could be increased to prevent the tic from reaching the threshold for expression, although this has been extensively investigated with conflicting results. Alternatively, automatic inhibition could prevent the initial excitation of the striatal tic focus—a hypothesis we have previously introduced. To reconcile these competing hypotheses, we examined different types of motor inhibition in a group of 19 patients with primary tic disorders and 15 healthy volunteers. We probed proactive and reactive inhibition using the conditional stop-signal task, and applied transcranial magnetic stimulation to the motor cortex, to assess movement preparation and execution. We assessed automatic motor inhibition with the masked priming task. We found that volitional movement preparation, execution and inhibition (proactive and reactive) were not impaired in tic disorders. We speculate that these mechanisms are recruited during volitional tic suppression, and that they prevent expression of the tic by inhibiting the nascent excitation released by the tic generator. In contrast, automatic inhibition was abnormal/impaired in patients with tic disorders. In the masked priming task, positive and negative compatibility effects were found for healthy controls, whereas patients with tics exhibited strong positive compatibility effects, but no negative compatibility effect indicative of impaired automatic inhibition. Patients also made more errors on the masked priming task than healthy control subjects and the types of errors were consistent with impaired automatic inhibition. Errors associated with impaired automatic inhibition were positively correlated with tic severity. We conclude that voluntary movement preparation/generation and volitional inhibition are normal in tic disorders, whereas automatic inhibition is impaired—a deficit that correlated with tic severity and thus may constitute a potential mechanism by which tics are generated.
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spelling pubmed-70896612020-03-27 Impaired automatic but intact volitional inhibition in primary tic disorders Rawji, Vishal Modi, Sachin Latorre, Anna Rocchi, Lorenzo Hockey, Leanne Bhatia, Kailash Joyce, Eileen Rothwell, John C Jahanshahi, Marjan Brain Original Articles The defining character of tics is that they can be transiently suppressed by volitional effort of will, and at a behavioural level this has led to the concept that tics result from a failure of inhibition. However, this logic conflates the mechanism responsible for the production of tics with that used in suppressing them. Volitional inhibition of motor output could be increased to prevent the tic from reaching the threshold for expression, although this has been extensively investigated with conflicting results. Alternatively, automatic inhibition could prevent the initial excitation of the striatal tic focus—a hypothesis we have previously introduced. To reconcile these competing hypotheses, we examined different types of motor inhibition in a group of 19 patients with primary tic disorders and 15 healthy volunteers. We probed proactive and reactive inhibition using the conditional stop-signal task, and applied transcranial magnetic stimulation to the motor cortex, to assess movement preparation and execution. We assessed automatic motor inhibition with the masked priming task. We found that volitional movement preparation, execution and inhibition (proactive and reactive) were not impaired in tic disorders. We speculate that these mechanisms are recruited during volitional tic suppression, and that they prevent expression of the tic by inhibiting the nascent excitation released by the tic generator. In contrast, automatic inhibition was abnormal/impaired in patients with tic disorders. In the masked priming task, positive and negative compatibility effects were found for healthy controls, whereas patients with tics exhibited strong positive compatibility effects, but no negative compatibility effect indicative of impaired automatic inhibition. Patients also made more errors on the masked priming task than healthy control subjects and the types of errors were consistent with impaired automatic inhibition. Errors associated with impaired automatic inhibition were positively correlated with tic severity. We conclude that voluntary movement preparation/generation and volitional inhibition are normal in tic disorders, whereas automatic inhibition is impaired—a deficit that correlated with tic severity and thus may constitute a potential mechanism by which tics are generated. Oxford University Press 2020-03 2020-03-03 /pmc/articles/PMC7089661/ /pubmed/32125364 http://dx.doi.org/10.1093/brain/awaa024 Text en © The Author(s) (2020). Published by Oxford University Press on behalf of the Guarantors of Brain. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://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 Articles
Rawji, Vishal
Modi, Sachin
Latorre, Anna
Rocchi, Lorenzo
Hockey, Leanne
Bhatia, Kailash
Joyce, Eileen
Rothwell, John C
Jahanshahi, Marjan
Impaired automatic but intact volitional inhibition in primary tic disorders
title Impaired automatic but intact volitional inhibition in primary tic disorders
title_full Impaired automatic but intact volitional inhibition in primary tic disorders
title_fullStr Impaired automatic but intact volitional inhibition in primary tic disorders
title_full_unstemmed Impaired automatic but intact volitional inhibition in primary tic disorders
title_short Impaired automatic but intact volitional inhibition in primary tic disorders
title_sort impaired automatic but intact volitional inhibition in primary tic disorders
topic Original Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7089661/
https://www.ncbi.nlm.nih.gov/pubmed/32125364
http://dx.doi.org/10.1093/brain/awaa024
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