Pallidal activities during sleep and sleep decoding in dystonia, Huntington's, and Parkinson's disease

Zixiao Yin; Yin Jiang; Timon Merk; Wolf-Julian Neumann; Ruoyu Ma; Qi An; Yutong Bai; Baotian Zhao; Yichen Xu; Houyou Fan; Quan Zhang; Guofan Qin; Ning Zhang; Jun Ma; Hua Zhang; Huanguang Liu; Lin Shi; Anchao Yang; Fangang Meng; Guanyu Zhu; Jianguo Zhang

doi:10.1016/j.nbd.2023.106143

Pallidal activities during sleep and sleep decoding in dystonia, Huntington's, and Parkinson's disease

Neurobiol Dis. 2023 Jun 15:182:106143. doi: 10.1016/j.nbd.2023.106143. Epub 2023 May 3.

Authors

Zixiao Yin¹, Yin Jiang², Timon Merk³, Wolf-Julian Neumann³, Ruoyu Ma¹, Qi An¹, Yutong Bai¹, Baotian Zhao¹, Yichen Xu¹, Houyou Fan¹, Quan Zhang¹, Guofan Qin¹, Ning Zhang⁴, Jun Ma⁴, Hua Zhang¹, Huanguang Liu¹, Lin Shi¹, Anchao Yang¹, Fangang Meng¹, Guanyu Zhu⁵, Jianguo Zhang⁶

Affiliations

¹ Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China.
² Department of Functional Neurosurgery, Beijing Neurosurgical Institute, Capital Medical University, Beijing, China; Beijing Key Laboratory of Neurostimulation, Beijing, China.
³ Movement Disorder and Neuromodulation Unit, Department of Neurology, Charité - Campus Mitte, Charite - Universitatsmedizin Berlin, Chariteplatz 1, 10117 Berlin, Germany.
⁴ Department of Neurology, Beijing Tiantan Hospital, Capital Medical University, Beijing, China; Department of Neuropsychiatry, Behavioral Neurology and Sleep Center, Beijing Tiantan Hospital, Capital Medical University, Beijing, China.
⁵ Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China. Electronic address: zhuguanyu1991@foxmail.com.
⁶ Department of Neurosurgery, Beijing Tiantan Hospital, Capital Medical University, Beijing, China; Department of Functional Neurosurgery, Beijing Neurosurgical Institute, Capital Medical University, Beijing, China; Beijing Key Laboratory of Neurostimulation, Beijing, China. Electronic address: zjguo73@126.com.

PMID: 37146835
DOI: 10.1016/j.nbd.2023.106143

Abstract

Background: Sleep disturbances are highly prevalent in movement disorders, potentially due to the malfunctioning of basal ganglia structures. Pallidal deep brain stimulation (DBS) has been widely used for multiple movement disorders and been reported to improve sleep. We aimed to investigate the oscillatory pattern of pallidum during sleep and explore whether pallidal activities can be utilized to differentiate sleep stages, which could pave the way for sleep-aware adaptive DBS.

Methods: We directly recorded over 500 h of pallidal local field potentials during sleep from 39 subjects with movement disorders (20 dystonia, 8 Huntington's disease, and 11 Parkinson's disease). Pallidal spectrum and cortical-pallidal coherence were computed and compared across sleep stages. Machine learning approaches were utilized to build sleep decoders for different diseases to classify sleep stages through pallidal oscillatory features. Decoding accuracy was further associated with the spatial localization of the pallidum.

Results: Pallidal power spectra and cortical-pallidal coherence were significantly modulated by sleep-stage transitions in three movement disorders. Differences in sleep-related activities between diseases were identified in non-rapid eye movement (NREM) and REM sleep. Machine learning models using pallidal oscillatory features can decode sleep-wake states with over 90% accuracy. Decoding accuracies were higher in recording sites within the internus-pallidum than the external-pallidum, and can be precited using structural (P < 0.0001) and functional (P < 0.0001) whole-brain neuroimaging connectomics.

Conclusion: Our findings revealed strong sleep-stage dependent distinctions in pallidal oscillations in multiple movement disorders. Pallidal oscillatory features were sufficient for sleep stage decoding. These data may facilitate the development of adaptive DBS systems targeting sleep problems that have broad translational prospects.

Keywords: Basal ganglia, local field potential; Deep brain stimulation; Movement disorders; Sleep disorders.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Deep Brain Stimulation* / methods
Dystonia*
Dystonic Disorders*
Globus Pallidus
Humans
Parkinson Disease* / complications
Parkinson Disease* / therapy
Sleep