Distinctive tics suppression network in Gilles de la Tourette syndrome distinguished from suppression of natural urges using multimodal imaging

Sandra M.A. van der Salm, Johan N. van der Meer, Daniëlle C. Cath, Paul F.C. Groot, Ysbrand D. van der Werf, Eelke Brouwers, Stella J. de Wit, Joris C. Coppens, Aart J. Nederveen, Anne Fleur van Rootselaar, Marina A.J. Tijssen

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

Background and objectives: Gilles de la Tourette syndrome (GTS) is a neuropsychiatric disorder characterized by tics. A hallmark of GTS is the ability to voluntarily suppress tics. Our aim was to distinguish the neural circuits involved in the voluntary suppression of ocular tics in GTS patients from blink suppression in healthy subjects. Methods: Fifteen GTS patients and 22 healthy control subjects were included in a multimodal study using eye-tracker recordings during functional MRI (fMRI). The ability to suppress tics/blinks was compared both on subjective (self-rating) and objective (eye-tracker) performance. For fMRI analysis we used a novel designed performance-adapted block design analysis of tic/blink suppression and release based on eye-tracker monitoring. Results: We found that the subjective self-reported ability to suppress tics or blinks showed no significant correlation with objective task performance. In GTS during successful suppression of tics, the dorsal anterior cingulate cortex and associated limbic areas showed increased activation. During successful suppression of eye blinks in healthy subjects, the right ventrolateral prefrontal cortex and supplementary and cingulate motor areas showed increased activation. Conclusions: These findings demonstrate that GTS patients use a characteristic limbic suppression strategy. In contrast, control subjects use the voluntary sensorimotor circuits and the classical ‘stop’ network to suppress natural urges. The employment of different neural suppression networks provides support for cognitive behavioral therapy in GTS.

Original languageEnglish
Pages (from-to)783-792
Number of pages10
JournalNeuroImage: Clinical
Volume20
DOIs
Publication statusPublished - 1 Jan 2018

Cite this

van der Salm, Sandra M.A. ; van der Meer, Johan N. ; Cath, Daniëlle C. ; Groot, Paul F.C. ; van der Werf, Ysbrand D. ; Brouwers, Eelke ; de Wit, Stella J. ; Coppens, Joris C. ; Nederveen, Aart J. ; van Rootselaar, Anne Fleur ; Tijssen, Marina A.J. / Distinctive tics suppression network in Gilles de la Tourette syndrome distinguished from suppression of natural urges using multimodal imaging. In: NeuroImage: Clinical. 2018 ; Vol. 20. pp. 783-792.
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title = "Distinctive tics suppression network in Gilles de la Tourette syndrome distinguished from suppression of natural urges using multimodal imaging",
abstract = "Background and objectives: Gilles de la Tourette syndrome (GTS) is a neuropsychiatric disorder characterized by tics. A hallmark of GTS is the ability to voluntarily suppress tics. Our aim was to distinguish the neural circuits involved in the voluntary suppression of ocular tics in GTS patients from blink suppression in healthy subjects. Methods: Fifteen GTS patients and 22 healthy control subjects were included in a multimodal study using eye-tracker recordings during functional MRI (fMRI). The ability to suppress tics/blinks was compared both on subjective (self-rating) and objective (eye-tracker) performance. For fMRI analysis we used a novel designed performance-adapted block design analysis of tic/blink suppression and release based on eye-tracker monitoring. Results: We found that the subjective self-reported ability to suppress tics or blinks showed no significant correlation with objective task performance. In GTS during successful suppression of tics, the dorsal anterior cingulate cortex and associated limbic areas showed increased activation. During successful suppression of eye blinks in healthy subjects, the right ventrolateral prefrontal cortex and supplementary and cingulate motor areas showed increased activation. Conclusions: These findings demonstrate that GTS patients use a characteristic limbic suppression strategy. In contrast, control subjects use the voluntary sensorimotor circuits and the classical ‘stop’ network to suppress natural urges. The employment of different neural suppression networks provides support for cognitive behavioral therapy in GTS.",
keywords = "Functional magnetic resonance imaging, Gilles de la Tourette syndrome, Suppression, Tics, Urges",
author = "{van der Salm}, {Sandra M.A.} and {van der Meer}, {Johan N.} and Cath, {Dani{\"e}lle C.} and Groot, {Paul F.C.} and {van der Werf}, {Ysbrand D.} and Eelke Brouwers and {de Wit}, {Stella J.} and Coppens, {Joris C.} and Nederveen, {Aart J.} and {van Rootselaar}, {Anne Fleur} and Tijssen, {Marina A.J.}",
year = "2018",
month = "1",
day = "1",
doi = "10.1016/j.nicl.2018.09.014",
language = "English",
volume = "20",
pages = "783--792",
journal = "NeuroImage: Clinical",
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van der Salm, SMA, van der Meer, JN, Cath, DC, Groot, PFC, van der Werf, YD, Brouwers, E, de Wit, SJ, Coppens, JC, Nederveen, AJ, van Rootselaar, AF & Tijssen, MAJ 2018, 'Distinctive tics suppression network in Gilles de la Tourette syndrome distinguished from suppression of natural urges using multimodal imaging' NeuroImage: Clinical, vol. 20, pp. 783-792. https://doi.org/10.1016/j.nicl.2018.09.014

Distinctive tics suppression network in Gilles de la Tourette syndrome distinguished from suppression of natural urges using multimodal imaging. / van der Salm, Sandra M.A.; van der Meer, Johan N.; Cath, Daniëlle C.; Groot, Paul F.C.; van der Werf, Ysbrand D.; Brouwers, Eelke; de Wit, Stella J.; Coppens, Joris C.; Nederveen, Aart J.; van Rootselaar, Anne Fleur; Tijssen, Marina A.J.

In: NeuroImage: Clinical, Vol. 20, 01.01.2018, p. 783-792.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Distinctive tics suppression network in Gilles de la Tourette syndrome distinguished from suppression of natural urges using multimodal imaging

AU - van der Salm, Sandra M.A.

AU - van der Meer, Johan N.

AU - Cath, Daniëlle C.

AU - Groot, Paul F.C.

AU - van der Werf, Ysbrand D.

AU - Brouwers, Eelke

AU - de Wit, Stella J.

AU - Coppens, Joris C.

AU - Nederveen, Aart J.

AU - van Rootselaar, Anne Fleur

AU - Tijssen, Marina A.J.

PY - 2018/1/1

Y1 - 2018/1/1

N2 - Background and objectives: Gilles de la Tourette syndrome (GTS) is a neuropsychiatric disorder characterized by tics. A hallmark of GTS is the ability to voluntarily suppress tics. Our aim was to distinguish the neural circuits involved in the voluntary suppression of ocular tics in GTS patients from blink suppression in healthy subjects. Methods: Fifteen GTS patients and 22 healthy control subjects were included in a multimodal study using eye-tracker recordings during functional MRI (fMRI). The ability to suppress tics/blinks was compared both on subjective (self-rating) and objective (eye-tracker) performance. For fMRI analysis we used a novel designed performance-adapted block design analysis of tic/blink suppression and release based on eye-tracker monitoring. Results: We found that the subjective self-reported ability to suppress tics or blinks showed no significant correlation with objective task performance. In GTS during successful suppression of tics, the dorsal anterior cingulate cortex and associated limbic areas showed increased activation. During successful suppression of eye blinks in healthy subjects, the right ventrolateral prefrontal cortex and supplementary and cingulate motor areas showed increased activation. Conclusions: These findings demonstrate that GTS patients use a characteristic limbic suppression strategy. In contrast, control subjects use the voluntary sensorimotor circuits and the classical ‘stop’ network to suppress natural urges. The employment of different neural suppression networks provides support for cognitive behavioral therapy in GTS.

AB - Background and objectives: Gilles de la Tourette syndrome (GTS) is a neuropsychiatric disorder characterized by tics. A hallmark of GTS is the ability to voluntarily suppress tics. Our aim was to distinguish the neural circuits involved in the voluntary suppression of ocular tics in GTS patients from blink suppression in healthy subjects. Methods: Fifteen GTS patients and 22 healthy control subjects were included in a multimodal study using eye-tracker recordings during functional MRI (fMRI). The ability to suppress tics/blinks was compared both on subjective (self-rating) and objective (eye-tracker) performance. For fMRI analysis we used a novel designed performance-adapted block design analysis of tic/blink suppression and release based on eye-tracker monitoring. Results: We found that the subjective self-reported ability to suppress tics or blinks showed no significant correlation with objective task performance. In GTS during successful suppression of tics, the dorsal anterior cingulate cortex and associated limbic areas showed increased activation. During successful suppression of eye blinks in healthy subjects, the right ventrolateral prefrontal cortex and supplementary and cingulate motor areas showed increased activation. Conclusions: These findings demonstrate that GTS patients use a characteristic limbic suppression strategy. In contrast, control subjects use the voluntary sensorimotor circuits and the classical ‘stop’ network to suppress natural urges. The employment of different neural suppression networks provides support for cognitive behavioral therapy in GTS.

KW - Functional magnetic resonance imaging

KW - Gilles de la Tourette syndrome

KW - Suppression

KW - Tics

KW - Urges

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DO - 10.1016/j.nicl.2018.09.014

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