A critical role of action-related functional networks in Gilles de la Tourette syndrome
Abstract Gilles de la Tourette Syndrome (GTS) is a chronic tic disorder, characterized by unwanted motor actions and vocalizations. While brain stimulation techniques show promise in reducing tic severity, optimal target networks are not well-defined. Here, we leverage datasets from two independent...
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Nature Portfolio
2024-12-01
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| Series: | Nature Communications |
| Online Access: | https://doi.org/10.1038/s41467-024-55242-6 |
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| author | Juan Carlos Baldermann Jan Niklas Petry-Schmelzer Thomas Schüller Lin Mahfoud Gregor A. Brandt Till A. Dembek Christina van der Linden Joachim K. Krauss Natalia Szejko Kirsten R. Müller-Vahl Christos Ganos Bassam Al-Fatly Petra Heiden Domenico Servello Tommaso Galbiati Kara A. Johnson Christopher R. Butson Michael S. Okun Pablo Andrade Katharina Domschke Gereon R. Fink Michael D. Fox Andreas Horn Jens Kuhn Veerle Visser-Vandewalle Michael T. Barbe |
| author_facet | Juan Carlos Baldermann Jan Niklas Petry-Schmelzer Thomas Schüller Lin Mahfoud Gregor A. Brandt Till A. Dembek Christina van der Linden Joachim K. Krauss Natalia Szejko Kirsten R. Müller-Vahl Christos Ganos Bassam Al-Fatly Petra Heiden Domenico Servello Tommaso Galbiati Kara A. Johnson Christopher R. Butson Michael S. Okun Pablo Andrade Katharina Domschke Gereon R. Fink Michael D. Fox Andreas Horn Jens Kuhn Veerle Visser-Vandewalle Michael T. Barbe |
| author_sort | Juan Carlos Baldermann |
| collection | DOAJ |
| description | Abstract Gilles de la Tourette Syndrome (GTS) is a chronic tic disorder, characterized by unwanted motor actions and vocalizations. While brain stimulation techniques show promise in reducing tic severity, optimal target networks are not well-defined. Here, we leverage datasets from two independent deep brain stimulation (DBS) cohorts and a cohort of tic-inducing lesions to infer critical networks for treatment and occurrence of tics by mapping stimulation sites and lesions to a functional connectome derived from 1,000 healthy participants. We find that greater tic reduction is linked to higher connectivity of DBS sites (N = 37) with action-related functional resting-state networks, i.e., the cingulo-opercular (r = 0.62; p < 0.001) and somato-cognitive action networks (r = 0.47; p = 0.002). Regions of the cingulo-opercular network best match the optimal connectivity profiles of thalamic DBS. We replicate the significance of targeting cingulo-opercular and somato-cognitive action network connectivity in an independent DBS cohort (N = 10). Finally, we demonstrate that tic-inducing brain lesions (N = 22) exhibit similar connectivity to these networks. Collectively, these results suggest a critical role for these action-related networks in the pathophysiology and treatment of GTS. |
| format | Article |
| id | doaj-art-23d92c8b4b434dd185bcd62d30325cb6 |
| institution | OA Journals |
| issn | 2041-1723 |
| language | English |
| publishDate | 2024-12-01 |
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| series | Nature Communications |
| spelling | doaj-art-23d92c8b4b434dd185bcd62d30325cb62025-08-20T02:31:51ZengNature PortfolioNature Communications2041-17232024-12-0115111510.1038/s41467-024-55242-6A critical role of action-related functional networks in Gilles de la Tourette syndromeJuan Carlos Baldermann0Jan Niklas Petry-Schmelzer1Thomas Schüller2Lin Mahfoud3Gregor A. Brandt4Till A. Dembek5Christina van der Linden6Joachim K. Krauss7Natalia Szejko8Kirsten R. Müller-Vahl9Christos Ganos10Bassam Al-Fatly11Petra Heiden12Domenico Servello13Tommaso Galbiati14Kara A. Johnson15Christopher R. Butson16Michael S. Okun17Pablo Andrade18Katharina Domschke19Gereon R. Fink20Michael D. Fox21Andreas Horn22Jens Kuhn23Veerle Visser-Vandewalle24Michael T. Barbe25Department of Psychiatry and Psychotherapy, Medical Center – University of Freiburg, Faculty of Medicine, University of FreiburgDepartment of Psychiatry and Psychotherapy, Medical Center – University of Freiburg, Faculty of Medicine, University of FreiburgDepartment of Neurology, Faculty of Medicine and University Hospital Cologne, University of CologneDepartment of Psychiatry and Psychotherapy, Medical Center – University of Freiburg, Faculty of Medicine, University of FreiburgDepartment of Psychiatry and Psychotherapy, Medical Center – University of Freiburg, Faculty of Medicine, University of FreiburgDepartment of Psychiatry and Psychotherapy, Medical Center – University of Freiburg, Faculty of Medicine, University of FreiburgDepartment of Psychiatry and Psychotherapy, Medical Center – University of Freiburg, Faculty of Medicine, University of FreiburgDepartment of Neurosurgery, Hannover Medical SchoolDepartment of Neurology, University of CalgaryDepartment of Psychiatry, Socialpsychiatry and Psychotherapy, Hannover Medical SchoolMovement Disorder Clinic, Edmond J. Safra Program in Parkinson’s Disease, Division of Neurology University of Toronto, Toronto Western HospitalDepartment of Neurology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu BerlinDepartment of Stereotactic and Functional Neurosurgery, Faculty of Medicine and University Hospital Cologne, University of CologneNeurosurgical Department, IRCCS Istituto Ortopedico Galeazzi, MilanNeurosurgical Department, IRCCS Istituto Ortopedico Galeazzi, MilanNorman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, FL, USA; Department of Neurology, University of FloridaNorman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, FL, USA; Department of Neurology, University of FloridaNorman Fixel Institute for Neurological Diseases, University of Florida, Gainesville, FL, USA; Department of Neurology, University of FloridaDepartment of Stereotactic and Functional Neurosurgery, Faculty of Medicine and University Hospital Cologne, University of CologneDepartment of Psychiatry and Psychotherapy, Medical Center – University of Freiburg, Faculty of Medicine, University of FreiburgDepartment of Psychiatry and Psychotherapy, Medical Center – University of Freiburg, Faculty of Medicine, University of FreiburgCenter for Brain Circuit Therapeutics, Department of Neurology, Brigham & Women’s Hospital, Harvard Medical SchoolCenter for Brain Circuit Therapeutics, Department of Neurology, Brigham & Women’s Hospital, Harvard Medical SchoolAlexianer Hospital Cologne, Alexianer Köln GmbHDepartment of Stereotactic and Functional Neurosurgery, Faculty of Medicine and University Hospital Cologne, University of CologneDepartment of Neurology, Faculty of Medicine and University Hospital Cologne, University of CologneAbstract Gilles de la Tourette Syndrome (GTS) is a chronic tic disorder, characterized by unwanted motor actions and vocalizations. While brain stimulation techniques show promise in reducing tic severity, optimal target networks are not well-defined. Here, we leverage datasets from two independent deep brain stimulation (DBS) cohorts and a cohort of tic-inducing lesions to infer critical networks for treatment and occurrence of tics by mapping stimulation sites and lesions to a functional connectome derived from 1,000 healthy participants. We find that greater tic reduction is linked to higher connectivity of DBS sites (N = 37) with action-related functional resting-state networks, i.e., the cingulo-opercular (r = 0.62; p < 0.001) and somato-cognitive action networks (r = 0.47; p = 0.002). Regions of the cingulo-opercular network best match the optimal connectivity profiles of thalamic DBS. We replicate the significance of targeting cingulo-opercular and somato-cognitive action network connectivity in an independent DBS cohort (N = 10). Finally, we demonstrate that tic-inducing brain lesions (N = 22) exhibit similar connectivity to these networks. Collectively, these results suggest a critical role for these action-related networks in the pathophysiology and treatment of GTS.https://doi.org/10.1038/s41467-024-55242-6 |
| spellingShingle | Juan Carlos Baldermann Jan Niklas Petry-Schmelzer Thomas Schüller Lin Mahfoud Gregor A. Brandt Till A. Dembek Christina van der Linden Joachim K. Krauss Natalia Szejko Kirsten R. Müller-Vahl Christos Ganos Bassam Al-Fatly Petra Heiden Domenico Servello Tommaso Galbiati Kara A. Johnson Christopher R. Butson Michael S. Okun Pablo Andrade Katharina Domschke Gereon R. Fink Michael D. Fox Andreas Horn Jens Kuhn Veerle Visser-Vandewalle Michael T. Barbe A critical role of action-related functional networks in Gilles de la Tourette syndrome Nature Communications |
| title | A critical role of action-related functional networks in Gilles de la Tourette syndrome |
| title_full | A critical role of action-related functional networks in Gilles de la Tourette syndrome |
| title_fullStr | A critical role of action-related functional networks in Gilles de la Tourette syndrome |
| title_full_unstemmed | A critical role of action-related functional networks in Gilles de la Tourette syndrome |
| title_short | A critical role of action-related functional networks in Gilles de la Tourette syndrome |
| title_sort | critical role of action related functional networks in gilles de la tourette syndrome |
| url | https://doi.org/10.1038/s41467-024-55242-6 |
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