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...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2018-01-01
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| Series: | NeuroImage: Clinical |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S2213158218300524 |
| _version_ | 1828932041171795968 |
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| author | Hang Joon Jo Kevin W. McCairn William S. Gibson Paola Testini Cong Zhi Zhao Krzysztof R. Gorny Joel P. Felmlee Kirk M. Welker Charles D. Blaha Bryan T. Klassen Hoon-Ki Min Kendall H. Lee |
| author_facet | Hang Joon Jo Kevin W. McCairn William S. Gibson Paola Testini Cong Zhi Zhao Krzysztof R. Gorny Joel P. Felmlee Kirk M. Welker Charles D. Blaha Bryan T. Klassen Hoon-Ki Min Kendall H. Lee |
| author_sort | Hang Joon Jo |
| collection | DOAJ |
| 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. Keywords: Neurological disorders, Deep brain stimulation, Functional magnetic resonance imaging, Basal ganglia-cerebellar-thalamo-cortical networks, Vocal/motor tics |
| first_indexed | 2024-12-14T00:56:07Z |
| format | Article |
| id | doaj.art-9ec930085b3940bea7de10b0b33598d1 |
| institution | Directory Open Access Journal |
| issn | 2213-1582 |
| language | English |
| last_indexed | 2024-12-14T00:56:07Z |
| publishDate | 2018-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | NeuroImage: Clinical |
| spelling | doaj.art-9ec930085b3940bea7de10b0b33598d12022-12-21T23:23:33ZengElsevierNeuroImage: Clinical2213-15822018-01-0118502509Global network modulation during thalamic stimulation for Tourette syndromeHang Joon Jo0Kevin W. McCairn1William S. Gibson2Paola Testini3Cong Zhi Zhao4Krzysztof R. Gorny5Joel P. Felmlee6Kirk M. Welker7Charles D. Blaha8Bryan T. Klassen9Hoon-Ki Min10Kendall H. Lee11Department of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USA; Department of Neurology, Mayo Clinic, Rochester, MN 55905, USASystems Neuroscience Section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, JapanDepartment of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USADepartment of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USADepartment of Neurology, Mayo Clinic, Rochester, MN 55905, USADepartment of Radiology, Mayo Clinic, Rochester, MN 55905, USADepartment of Radiology, Mayo Clinic, Rochester, MN 55905, USADepartment of Radiology, Mayo Clinic, Rochester, MN 55905, USADepartment of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USADepartment of Neurology, Mayo Clinic, Rochester, MN 55905, USADepartment of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USA; Department of Radiology, Mayo Clinic, Rochester, MN 55905, USA; Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN 55905, USA; Corresponding authors at: Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA.Department of Neurologic Surgery, Mayo Clinic, Rochester, MN 55905, USA; Department of Physiology and Biomedical Engineering, Mayo Clinic, Rochester, MN 55905, USA; Corresponding authors at: Mayo Clinic, 200 First Street SW, Rochester, MN 55905, USA.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. Keywords: Neurological disorders, Deep brain stimulation, Functional magnetic resonance imaging, Basal ganglia-cerebellar-thalamo-cortical networks, Vocal/motor ticshttp://www.sciencedirect.com/science/article/pii/S2213158218300524 |
| spellingShingle | Hang Joon Jo Kevin W. McCairn William S. Gibson Paola Testini Cong Zhi Zhao Krzysztof R. Gorny Joel P. Felmlee Kirk M. Welker Charles D. Blaha Bryan T. Klassen Hoon-Ki Min Kendall H. Lee Global network modulation during thalamic stimulation for Tourette syndrome NeuroImage: Clinical |
| 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 |
| url | http://www.sciencedirect.com/science/article/pii/S2213158218300524 |
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