Motor network reorganization associated with rTMS-induced writing improvement in writer's cramp dystonia
Background: Writer's cramp (WC) dystonia is an involuntary movement disorder with distributed abnormalities in the brain's motor network. Prior studies established the potential for repetitive transcranial magnetic stimulation (rTMS) to either premotor cortex (PMC) or primary somatosensory...
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Elsevier
2025-03-01
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| Series: | Brain Stimulation |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S1935861X25000361 |
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| author | Noreen Bukhari-Parlakturk Patrick J. Mulcahey Michael W. Lutz Rabia Ghazi Ziping Huang Moritz Dannhauer Pichet Termsarasab Burton Scott Zeynep B. Simsek Skylar Groves Mikaela Lipp Michael Fei Tiffany K. Tran Eleanor Wood Lysianne Beynel Chris Petty James T. Voyvodic Lawrence G. Appelbaum Hussein R. Al-Khalidi Simon W. Davis Andrew M. Michael Angel V. Peterchev Nicole Calakos |
| author_facet | Noreen Bukhari-Parlakturk Patrick J. Mulcahey Michael W. Lutz Rabia Ghazi Ziping Huang Moritz Dannhauer Pichet Termsarasab Burton Scott Zeynep B. Simsek Skylar Groves Mikaela Lipp Michael Fei Tiffany K. Tran Eleanor Wood Lysianne Beynel Chris Petty James T. Voyvodic Lawrence G. Appelbaum Hussein R. Al-Khalidi Simon W. Davis Andrew M. Michael Angel V. Peterchev Nicole Calakos |
| author_sort | Noreen Bukhari-Parlakturk |
| collection | DOAJ |
| description | Background: Writer's cramp (WC) dystonia is an involuntary movement disorder with distributed abnormalities in the brain's motor network. Prior studies established the potential for repetitive transcranial magnetic stimulation (rTMS) to either premotor cortex (PMC) or primary somatosensory cortex (PSC) to modify symptoms. However, clinical effects have been modest with limited understanding of the neural mechanisms hindering therapeutic advancement of this promising approach. Objective: This study aimed to understand the motor network effects of rTMS in WC that correspond with behavioral efficacy. We hypothesized that behavioral efficacy is associated with modulation of cortical and subcortical regions of the motor network. Methods: In a double-blind, cross-over design, twelve WC participants underwent rTMS in one of three conditions (Sham-TMS, 10 Hz PSC-rTMS, 10 Hz PMC-rTMS) while engaged in a writing task to activate dystonic movements and measure writing fluency. Brain connectivity was evaluated using task-based fMRI after each TMS session. Results: 10 Hz rTMS to PSC, but not PMC, significantly improved writing dysfluency. PSC-TMS also significantly weakened cortico-basal ganglia, cortico-cerebellum, and intra-cerebellum functional connectivity (FC), and strengthened striatal FC relative to Sham. Change in PSC and SPC BOLD activity were associated with reduced dysfluent writing behavior. Conclusions: 10 Hz rTMS to PSC improved writing dysfluency by redistributing motor network connectivity and strengthening somatosensory-parietal connectivity. A key signature for effective stimulation at PSC and improvement in writing dysfluency may be strengthening of intra-cortical connectivity between primary somatosensory and superior parietal cortices. These findings offer mechanistic hypotheses to advance the therapeutic application of TMS for dystonia. |
| format | Article |
| id | doaj-art-83292cbf40cf4e3487e254b667eec779 |
| institution | OA Journals |
| issn | 1935-861X |
| language | English |
| publishDate | 2025-03-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Brain Stimulation |
| spelling | doaj-art-83292cbf40cf4e3487e254b667eec7792025-08-20T02:12:08ZengElsevierBrain Stimulation1935-861X2025-03-0118219821010.1016/j.brs.2025.02.005Motor network reorganization associated with rTMS-induced writing improvement in writer's cramp dystoniaNoreen Bukhari-Parlakturk0Patrick J. Mulcahey1Michael W. Lutz2Rabia Ghazi3Ziping Huang4Moritz Dannhauer5Pichet Termsarasab6Burton Scott7Zeynep B. Simsek8Skylar Groves9Mikaela Lipp10Michael Fei11Tiffany K. Tran12Eleanor Wood13Lysianne Beynel14Chris Petty15James T. Voyvodic16Lawrence G. Appelbaum17Hussein R. Al-Khalidi18Simon W. Davis19Andrew M. Michael20Angel V. Peterchev21Nicole Calakos22Department of Neurology, Duke University School of Medicine, USA; Duke Institute for Brain Sciences, Duke University, USA; Corresponding author. DUMC Box 2900, Bryan Research Building, 311 Research Drive, Durham, NC, 27710, USA.Department of Neurology, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USADepartment of Computer Science, Center for Brain Stimulation, East Carolina University, Greenville, NC, USADepartment of Medicine, Faculty of Medicine Ramathibodi Hospital, Mahidol University, Bangkok, ThailandDepartment of Neurology, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USADrexel University College of Medicine, Philadelphia, PA, USANon Invasive Neuromodulation Unit, Experimental Therapeutics and Pathophysiology Branch, National Institute of Mental Health, National Institute of Health, Bethesda, MD, USABrain Imaging & Analysis Center, Duke University School of Medicine, USADuke Institute for Brain Sciences, Duke University, USA; Brain Imaging & Analysis Center, Duke University School of Medicine, USADepartment of Psychiatry, University of California, San Diego, CA, USADepartment of Biostatistics and Bioinformatics, Duke University School of Medicine, USADepartment of Neurology, Duke University School of Medicine, USA; Duke Institute for Brain Sciences, Duke University, USADuke Institute for Brain Sciences, Duke University, USADuke Institute for Brain Sciences, Duke University, USA; Department of Psychiatry and Behavioral Sciences, Duke University School of Medicine, USA; Department of Electrical and Computer Engineering, Duke University, USA; Department of Neurosurgery, Duke University School of Medicine, USA; Department of Biomedical Engineering, Duke University, USADepartment of Neurology, Duke University School of Medicine, USA; Duke Institute for Brain Sciences, Duke University, USA; Department of Neurobiology, Duke University School of Medicine, Durham, NC, USABackground: Writer's cramp (WC) dystonia is an involuntary movement disorder with distributed abnormalities in the brain's motor network. Prior studies established the potential for repetitive transcranial magnetic stimulation (rTMS) to either premotor cortex (PMC) or primary somatosensory cortex (PSC) to modify symptoms. However, clinical effects have been modest with limited understanding of the neural mechanisms hindering therapeutic advancement of this promising approach. Objective: This study aimed to understand the motor network effects of rTMS in WC that correspond with behavioral efficacy. We hypothesized that behavioral efficacy is associated with modulation of cortical and subcortical regions of the motor network. Methods: In a double-blind, cross-over design, twelve WC participants underwent rTMS in one of three conditions (Sham-TMS, 10 Hz PSC-rTMS, 10 Hz PMC-rTMS) while engaged in a writing task to activate dystonic movements and measure writing fluency. Brain connectivity was evaluated using task-based fMRI after each TMS session. Results: 10 Hz rTMS to PSC, but not PMC, significantly improved writing dysfluency. PSC-TMS also significantly weakened cortico-basal ganglia, cortico-cerebellum, and intra-cerebellum functional connectivity (FC), and strengthened striatal FC relative to Sham. Change in PSC and SPC BOLD activity were associated with reduced dysfluent writing behavior. Conclusions: 10 Hz rTMS to PSC improved writing dysfluency by redistributing motor network connectivity and strengthening somatosensory-parietal connectivity. A key signature for effective stimulation at PSC and improvement in writing dysfluency may be strengthening of intra-cortical connectivity between primary somatosensory and superior parietal cortices. These findings offer mechanistic hypotheses to advance the therapeutic application of TMS for dystonia.http://www.sciencedirect.com/science/article/pii/S1935861X25000361Writer's crampMotor networkTranscranial magnetic stimulationDystonia |
| spellingShingle | Noreen Bukhari-Parlakturk Patrick J. Mulcahey Michael W. Lutz Rabia Ghazi Ziping Huang Moritz Dannhauer Pichet Termsarasab Burton Scott Zeynep B. Simsek Skylar Groves Mikaela Lipp Michael Fei Tiffany K. Tran Eleanor Wood Lysianne Beynel Chris Petty James T. Voyvodic Lawrence G. Appelbaum Hussein R. Al-Khalidi Simon W. Davis Andrew M. Michael Angel V. Peterchev Nicole Calakos Motor network reorganization associated with rTMS-induced writing improvement in writer's cramp dystonia Brain Stimulation Writer's cramp Motor network Transcranial magnetic stimulation Dystonia |
| title | Motor network reorganization associated with rTMS-induced writing improvement in writer's cramp dystonia |
| title_full | Motor network reorganization associated with rTMS-induced writing improvement in writer's cramp dystonia |
| title_fullStr | Motor network reorganization associated with rTMS-induced writing improvement in writer's cramp dystonia |
| title_full_unstemmed | Motor network reorganization associated with rTMS-induced writing improvement in writer's cramp dystonia |
| title_short | Motor network reorganization associated with rTMS-induced writing improvement in writer's cramp dystonia |
| title_sort | motor network reorganization associated with rtms induced writing improvement in writer s cramp dystonia |
| topic | Writer's cramp Motor network Transcranial magnetic stimulation Dystonia |
| url | http://www.sciencedirect.com/science/article/pii/S1935861X25000361 |
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