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Global network modulation during thalamic stimulation for Tourette syndrome

BACKGROUND AND OBJECTIVES: Deep brain stimulation (DBS) of the thalamus is a promising therapeutic alternative for treating medically refractory Tourette syndrome (TS). However, few human studies have examined its mechanism of action. Therefore, the networks that mediate the therapeutic effects of t...

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Autores principales: Jo, Hang Joon, McCairn, Kevin W., Gibson, William S., Testini, Paola, Zhao, Cong Zhi, Gorny, Krzysztof R., Felmlee, Joel P., Welker, Kirk M., Blaha, Charles D., Klassen, Bryan T., Min, Hoon-Ki, Lee, Kendall H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5857897/
https://www.ncbi.nlm.nih.gov/pubmed/29560306
http://dx.doi.org/10.1016/j.nicl.2018.02.018
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author Jo, Hang Joon
McCairn, Kevin W.
Gibson, William S.
Testini, Paola
Zhao, Cong Zhi
Gorny, Krzysztof R.
Felmlee, Joel P.
Welker, Kirk M.
Blaha, Charles D.
Klassen, Bryan T.
Min, Hoon-Ki
Lee, Kendall H.
author_facet Jo, Hang Joon
McCairn, Kevin W.
Gibson, William S.
Testini, Paola
Zhao, Cong Zhi
Gorny, Krzysztof R.
Felmlee, Joel P.
Welker, Kirk M.
Blaha, Charles D.
Klassen, Bryan T.
Min, Hoon-Ki
Lee, Kendall H.
author_sort Jo, Hang Joon
collection PubMed
description BACKGROUND AND OBJECTIVES: Deep brain stimulation (DBS) of the thalamus is a promising therapeutic alternative for treating medically refractory Tourette syndrome (TS). However, few human studies have examined its mechanism of action. Therefore, the networks that mediate the therapeutic effects of thalamic DBS remain poorly understood. METHODS: Five participants diagnosed with severe medically refractory TS underwent bilateral thalamic DBS stereotactic surgery. Intraoperative fMRI characterized the blood oxygen level-dependent (BOLD) response evoked by thalamic DBS and determined whether the therapeutic effectiveness of thalamic DBS, as assessed using the Modified Rush Video Rating Scale test, would correlate with evoked BOLD responses in motor and limbic cortical and subcortical regions. RESULTS: Our results reveal that thalamic stimulation in TS participants has wide-ranging effects that impact the frontostriatal, limbic, and motor networks. Thalamic stimulation induced suppression of motor and insula networks correlated with motor tic reduction, while suppression of frontal and parietal networks correlated with vocal tic reduction. These regions mapped closely to major regions of interest (ROI) identified in a nonhuman primate model of TS. CONCLUSIONS: Overall, these findings suggest that a critical factor in TS treatment should involve modulation of both frontostriatal and motor networks, rather than be treated as a focal disorder of the brain. Using the novel combination of DBS-evoked tic reduction and fMRI in human subjects, we provide new insights into the basal ganglia-cerebellar-thalamo-cortical network-level mechanisms that influence the effects of thalamic DBS. Future translational research should identify whether these network changes are cause or effect of TS symptoms.
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spelling pubmed-58578972018-03-20 Global network modulation during thalamic stimulation for Tourette syndrome Jo, Hang Joon McCairn, Kevin W. Gibson, William S. Testini, Paola Zhao, Cong Zhi Gorny, Krzysztof R. Felmlee, Joel P. Welker, Kirk M. Blaha, Charles D. Klassen, Bryan T. Min, Hoon-Ki Lee, Kendall H. Neuroimage Clin Regular Article BACKGROUND AND OBJECTIVES: Deep brain stimulation (DBS) of the thalamus is a promising therapeutic alternative for treating medically refractory Tourette syndrome (TS). However, few human studies have examined its mechanism of action. Therefore, the networks that mediate the therapeutic effects of thalamic DBS remain poorly understood. METHODS: Five participants diagnosed with severe medically refractory TS underwent bilateral thalamic DBS stereotactic surgery. Intraoperative fMRI characterized the blood oxygen level-dependent (BOLD) response evoked by thalamic DBS and determined whether the therapeutic effectiveness of thalamic DBS, as assessed using the Modified Rush Video Rating Scale test, would correlate with evoked BOLD responses in motor and limbic cortical and subcortical regions. RESULTS: Our results reveal that thalamic stimulation in TS participants has wide-ranging effects that impact the frontostriatal, limbic, and motor networks. Thalamic stimulation induced suppression of motor and insula networks correlated with motor tic reduction, while suppression of frontal and parietal networks correlated with vocal tic reduction. These regions mapped closely to major regions of interest (ROI) identified in a nonhuman primate model of TS. CONCLUSIONS: Overall, these findings suggest that a critical factor in TS treatment should involve modulation of both frontostriatal and motor networks, rather than be treated as a focal disorder of the brain. Using the novel combination of DBS-evoked tic reduction and fMRI in human subjects, we provide new insights into the basal ganglia-cerebellar-thalamo-cortical network-level mechanisms that influence the effects of thalamic DBS. Future translational research should identify whether these network changes are cause or effect of TS symptoms. Elsevier 2018-02-21 /pmc/articles/PMC5857897/ /pubmed/29560306 http://dx.doi.org/10.1016/j.nicl.2018.02.018 Text en © 2018 Published by Elsevier Inc. http://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Regular Article
Jo, Hang Joon
McCairn, Kevin W.
Gibson, William S.
Testini, Paola
Zhao, Cong Zhi
Gorny, Krzysztof R.
Felmlee, Joel P.
Welker, Kirk M.
Blaha, Charles D.
Klassen, Bryan T.
Min, Hoon-Ki
Lee, Kendall H.
Global network modulation during thalamic stimulation for Tourette syndrome
title Global network modulation during thalamic stimulation for Tourette syndrome
title_full Global network modulation during thalamic stimulation for Tourette syndrome
title_fullStr Global network modulation during thalamic stimulation for Tourette syndrome
title_full_unstemmed Global network modulation during thalamic stimulation for Tourette syndrome
title_short Global network modulation during thalamic stimulation for Tourette syndrome
title_sort global network modulation during thalamic stimulation for tourette syndrome
topic Regular Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5857897/
https://www.ncbi.nlm.nih.gov/pubmed/29560306
http://dx.doi.org/10.1016/j.nicl.2018.02.018
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