Subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulation

Background: Deep brain stimulation (DBS) targeting the globus pallidus internus (GPi) and subthalamic nucleus (STN) is employed for the treatment of dystonia. Pallidal low-frequency oscillations have been proposed as a pathophysiological marker for dystonia. However, the role of subthalamic oscillat...

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Published in:Neurobiology of Disease
Main Authors: Xinyi Geng, Zhaoyu Quan, Ruili Zhang, Guanyu Zhu, Yingnan Nie, Shouyan Wang, Edmund Rolls, Jianguo Zhang, Li Hu
Format: Article
Language:English
Published: Elsevier 2024-09-01
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0969996124001815
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author Xinyi Geng
Zhaoyu Quan
Ruili Zhang
Guanyu Zhu
Yingnan Nie
Shouyan Wang
Edmund Rolls
Jianguo Zhang
Li Hu
author_facet Xinyi Geng
Zhaoyu Quan
Ruili Zhang
Guanyu Zhu
Yingnan Nie
Shouyan Wang
Edmund Rolls
Jianguo Zhang
Li Hu
author_sort Xinyi Geng
collection DOAJ
container_title Neurobiology of Disease
description Background: Deep brain stimulation (DBS) targeting the globus pallidus internus (GPi) and subthalamic nucleus (STN) is employed for the treatment of dystonia. Pallidal low-frequency oscillations have been proposed as a pathophysiological marker for dystonia. However, the role of subthalamic oscillations and STN-GPi coupling in relation to dystonia remains unclear. Objective: We aimed to explore oscillatory activities within the STN-GPi circuit and their correlation with the severity of dystonia and efficacy achieved by DBS treatment. Methods: Local field potentials were recorded simultaneously from the STN and GPi from 13 dystonia patients. Spectral power analysis was conducted for selected frequency bands from both nuclei, while power correlation and the weighted phase lag index were used to evaluate power and phase couplings between these two nuclei, respectively. These features were incorporated into generalized linear models to assess their associations with dystonia severity and DBS efficacy. Results: The results revealed that pallidal theta power, subthalamic beta power and subthalamic-pallidal theta phase coupling and beta power coupling all correlated with clinical severity. The model incorporating all selected features predicts empirical clinical scores and DBS-induced improvements, whereas the model relying solely on pallidal theta power failed to demonstrate significant correlations. Conclusions: Beyond pallidal theta power, subthalamic beta power, STN-GPi couplings in theta and beta bands, play a crucial role in understanding the pathophysiological mechanism of dystonia and developing optimal strategies for DBS.
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spelling doaj-art-e298f3cd5d1d4fca8131476506d4ab5b2025-08-20T00:49:48ZengElsevierNeurobiology of Disease1095-953X2024-09-0119910658110.1016/j.nbd.2024.106581Subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulationXinyi Geng0Zhaoyu Quan1Ruili Zhang2Guanyu Zhu3Yingnan Nie4Shouyan Wang5Edmund Rolls6Jianguo Zhang7Li Hu8Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, China; Correspondence to: Xinyi Geng, CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, 16 Yard of Lincui Rd, Chaoyang District, Beijing, China.Academy for Engineering and Technology, Fudan University, Shanghai, ChinaInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, ChinaDepartment of Neurosurgery, Beijing Tian-Tan Hospital, Beijing Neurosurgical Institute, Capital Medical University, ChinaInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, ChinaInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Key Laboratory of Computational Neuroscience and Brain-Inspired Intelligence (Fudan University), Ministry of Education, ChinaInstitute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Oxford Centre for Computational Neuroscience, University of Oxford, Oxford, UKDepartment of Neurosurgery, Beijing Tian-Tan Hospital, Beijing Neurosurgical Institute, Capital Medical University, China; Correspondence to: Jianguo Zhang, Department of Neurosurgery, Beijing Tian-Tan Hospital, Beijing Neurosurgical Institute, Capital Medical University, 119 West of the South Fourth Ring Road, Fengtai District, China.CAS Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China; Department of Psychology, University of Chinese Academy of Sciences, Beijing, ChinaBackground: Deep brain stimulation (DBS) targeting the globus pallidus internus (GPi) and subthalamic nucleus (STN) is employed for the treatment of dystonia. Pallidal low-frequency oscillations have been proposed as a pathophysiological marker for dystonia. However, the role of subthalamic oscillations and STN-GPi coupling in relation to dystonia remains unclear. Objective: We aimed to explore oscillatory activities within the STN-GPi circuit and their correlation with the severity of dystonia and efficacy achieved by DBS treatment. Methods: Local field potentials were recorded simultaneously from the STN and GPi from 13 dystonia patients. Spectral power analysis was conducted for selected frequency bands from both nuclei, while power correlation and the weighted phase lag index were used to evaluate power and phase couplings between these two nuclei, respectively. These features were incorporated into generalized linear models to assess their associations with dystonia severity and DBS efficacy. Results: The results revealed that pallidal theta power, subthalamic beta power and subthalamic-pallidal theta phase coupling and beta power coupling all correlated with clinical severity. The model incorporating all selected features predicts empirical clinical scores and DBS-induced improvements, whereas the model relying solely on pallidal theta power failed to demonstrate significant correlations. Conclusions: Beyond pallidal theta power, subthalamic beta power, STN-GPi couplings in theta and beta bands, play a crucial role in understanding the pathophysiological mechanism of dystonia and developing optimal strategies for DBS.http://www.sciencedirect.com/science/article/pii/S0969996124001815Subthalamic nucleusGlobus pallidus internusDystoniaOscillations and couplingsDeep brain stimulation
spellingShingle Xinyi Geng
Zhaoyu Quan
Ruili Zhang
Guanyu Zhu
Yingnan Nie
Shouyan Wang
Edmund Rolls
Jianguo Zhang
Li Hu
Subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulation
Subthalamic nucleus
Globus pallidus internus
Dystonia
Oscillations and couplings
Deep brain stimulation
title Subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulation
title_full Subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulation
title_fullStr Subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulation
title_full_unstemmed Subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulation
title_short Subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulation
title_sort subthalamic and pallidal oscillations and their couplings reflect dystonia severity and improvements by deep brain stimulation
topic Subthalamic nucleus
Globus pallidus internus
Dystonia
Oscillations and couplings
Deep brain stimulation
url http://www.sciencedirect.com/science/article/pii/S0969996124001815
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