Dynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometry
Abstract Patients with drug-resistant essential tremor (ET) may undergo Gamma Knife stereotactic radiosurgical thalamotomy (SRS-T), where the ventro-intermediate nucleus of the thalamus (Vim) is lesioned by focused beams of gamma radiations to induce clinical improvement. Here, we studied SRS-T impa...
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| Format: | Article |
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Nature Portfolio
2024-01-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-024-52410-y |
| _version_ | 1827327560276508672 |
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| author | Thomas A. W. Bolton Dimitri Van De Ville Jean Régis Tatiana Witjas Nadine Girard Marc Levivier Constantin Tuleasca |
| author_facet | Thomas A. W. Bolton Dimitri Van De Ville Jean Régis Tatiana Witjas Nadine Girard Marc Levivier Constantin Tuleasca |
| author_sort | Thomas A. W. Bolton |
| collection | DOAJ |
| description | Abstract Patients with drug-resistant essential tremor (ET) may undergo Gamma Knife stereotactic radiosurgical thalamotomy (SRS-T), where the ventro-intermediate nucleus of the thalamus (Vim) is lesioned by focused beams of gamma radiations to induce clinical improvement. Here, we studied SRS-T impacts on left Vim dynamic functional connectivity (dFC, n = 23 ET patients scanned before and 1 year after intervention), and on surface-based morphometric brain features (n = 34 patients, including those from dFC analysis). In matched healthy controls (HCs), three dFC states were extracted from resting-state functional MRI data. In ET patients, state 1 spatial stability increased upon SRS-T (F 1,22 = 19.13, p = 0.004). More frequent expression of state 3 over state 1 before SRS-T correlated with greater clinical recovery in a way that depended on the MR signature volume (t 6 = 4.6, p = 0.004). Lower pre-intervention spatial variability in state 3 expression also did (t 6 = − 4.24, p = 0.005) and interacted with the presence of familial ET so that these patients improved less (t 6 = 4.14, p = 0.006). ET morphometric profiles showed significantly lower similarity to HCs in 13 regions upon SRS-T (z ≤ − 3.66, p ≤ 0.022), and a joint analysis revealed that before thalamotomy, morphometric similarity and states 2/3 mean spatial similarity to HCs were anticorrelated, a relationship that disappeared upon SRS-T (z ≥ 4.39, p < 0.001). Our results show that left Vim functional dynamics directly relates to upper limb tremor lowering upon intervention, while morphometry instead has a supporting role in reshaping such dynamics. |
| first_indexed | 2024-03-07T15:03:03Z |
| format | Article |
| id | doaj.art-24d6f369869f4f099d0216b1dabdb0b9 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-03-07T15:03:03Z |
| publishDate | 2024-01-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-24d6f369869f4f099d0216b1dabdb0b92024-03-05T19:00:29ZengNature PortfolioScientific Reports2045-23222024-01-0114111610.1038/s41598-024-52410-yDynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometryThomas A. W. Bolton0Dimitri Van De Ville1Jean Régis2Tatiana Witjas3Nadine Girard4Marc Levivier5Constantin Tuleasca6Department of Clinical Neurosciences, Neurosurgery Service and Gamma Knife Center, Centre Hospitalier Universitaire VaudoisNeuro-X Institute, Ecole Polytechnique Fédérale de LausanneStereotactic and Functional Neurosurgery Service and Gamma Knife Unit, Assistance Publique-Hôpitaux de Marseille, Centre Hospitalier Universitaire de la TimoneNeurology Department, Assistance Publique-Hôpitaux de Marseille, Centre Hospitalier Universitaire de la TimoneDepartment of Diagnostic and Interventional Neuroradiology, Centre de Résonance Magnétique Biologique et Médicale, Assistance Publique-Hôpitaux de Marseille, Centre Hospitalier Universitaire de la TimoneDepartment of Clinical Neurosciences, Neurosurgery Service and Gamma Knife Center, Centre Hospitalier Universitaire VaudoisDepartment of Clinical Neurosciences, Neurosurgery Service and Gamma Knife Center, Centre Hospitalier Universitaire VaudoisAbstract Patients with drug-resistant essential tremor (ET) may undergo Gamma Knife stereotactic radiosurgical thalamotomy (SRS-T), where the ventro-intermediate nucleus of the thalamus (Vim) is lesioned by focused beams of gamma radiations to induce clinical improvement. Here, we studied SRS-T impacts on left Vim dynamic functional connectivity (dFC, n = 23 ET patients scanned before and 1 year after intervention), and on surface-based morphometric brain features (n = 34 patients, including those from dFC analysis). In matched healthy controls (HCs), three dFC states were extracted from resting-state functional MRI data. In ET patients, state 1 spatial stability increased upon SRS-T (F 1,22 = 19.13, p = 0.004). More frequent expression of state 3 over state 1 before SRS-T correlated with greater clinical recovery in a way that depended on the MR signature volume (t 6 = 4.6, p = 0.004). Lower pre-intervention spatial variability in state 3 expression also did (t 6 = − 4.24, p = 0.005) and interacted with the presence of familial ET so that these patients improved less (t 6 = 4.14, p = 0.006). ET morphometric profiles showed significantly lower similarity to HCs in 13 regions upon SRS-T (z ≤ − 3.66, p ≤ 0.022), and a joint analysis revealed that before thalamotomy, morphometric similarity and states 2/3 mean spatial similarity to HCs were anticorrelated, a relationship that disappeared upon SRS-T (z ≥ 4.39, p < 0.001). Our results show that left Vim functional dynamics directly relates to upper limb tremor lowering upon intervention, while morphometry instead has a supporting role in reshaping such dynamics.https://doi.org/10.1038/s41598-024-52410-y |
| spellingShingle | Thomas A. W. Bolton Dimitri Van De Ville Jean Régis Tatiana Witjas Nadine Girard Marc Levivier Constantin Tuleasca Dynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometry Scientific Reports |
| title | Dynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometry |
| title_full | Dynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometry |
| title_fullStr | Dynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometry |
| title_full_unstemmed | Dynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometry |
| title_short | Dynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometry |
| title_sort | dynamic functional changes upon thalamotomy in essential tremor depend on baseline brain morphometry |
| url | https://doi.org/10.1038/s41598-024-52410-y |
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