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

Xinyi Geng; Zhaoyu Quan; Ruili Zhang; Guanyu Zhu; Yingnan Nie; Shouyan Wang; Edmund Rolls; Jianguo Zhang; Li Hu

Neurobiology of Disease (Sep 2024)

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

Xinyi Geng,
Zhaoyu Quan,
Ruili Zhang,
Guanyu Zhu,
Yingnan Nie,
Shouyan Wang,
Edmund Rolls,
Jianguo Zhang,
Li Hu

Affiliations

Xinyi Geng: Institute 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.
Zhaoyu Quan: Academy for Engineering and Technology, Fudan University, Shanghai, China
Ruili Zhang: Institute 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, China
Guanyu Zhu: Department of Neurosurgery, Beijing Tian-Tan Hospital, Beijing Neurosurgical Institute, Capital Medical University, China
Yingnan Nie: Institute 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, China
Shouyan Wang: Institute 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, China
Edmund Rolls: Institute of Science and Technology for Brain-Inspired Intelligence, Fudan University, Shanghai, China; Oxford Centre for Computational Neuroscience, University of Oxford, Oxford, UK
Jianguo Zhang: Department 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.
Li Hu: 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

Journal volume & issue: Vol. 199
p. 106581

Abstract

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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.

Published in Neurobiology of Disease

ISSN: 0969-9961 (Print); 1095-953X (Online)
Publisher: Elsevier
Country of publisher: United States
LCC subjects: Medicine: Internal medicine: Neurosciences. Biological psychiatry. Neuropsychiatry
Website: https://www.journals.elsevier.com/neurobiology-of-disease

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