Neurophysiological features of STN LFP underlying sleep fragmentation in Parkinson's disease

Guokun Zhang; Huiling Yu; Yue Chen; Chen Gong; Hongwei Hao; Yi Guo; Shujun Xu; Yuhuan Zhang; Xuemei Yuan; Guoping Yin; Jian-Guo Zhang; Huiling Tan; Luming Li

doi:10.1136/jnnp-2023-331979

Neurophysiological features of STN LFP underlying sleep fragmentation in Parkinson's disease

J Neurol Neurosurg Psychiatry. 2024 Nov 18;95(12):1112-1122. doi: 10.1136/jnnp-2023-331979.

Authors

Guokun Zhang^#¹, Huiling Yu^#¹, Yue Chen¹, Chen Gong¹, Hongwei Hao¹, Yi Guo², Shujun Xu³, Yuhuan Zhang⁴, Xuemei Yuan⁴, Guoping Yin⁴, Jian-Guo Zhang⁵, Huiling Tan⁶, Luming Li^{7

8}

Affiliations

¹ National Engineering Research Center of Neuromodulation, Tsinghua University School of Aerospace Engineering, Beijing, China.
² Peking Union Medical College Hospital, Beijing, China.
³ Department of Neurosurgery, Qilu Hospital of Shandong University Qingdao, Qingdao, Shandong, China.
⁴ Department of Otolaryngology Head and Neck Surgery, Beijing Tsinghua Changgung Hospital, Beijing, China.
⁵ Beijing Tiantan Hospital, Beijing, China.
⁶ Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK [email protected] [email protected].
⁷ National Engineering Research Center of Neuromodulation, Tsinghua University School of Aerospace Engineering, Beijing, China [email protected] [email protected].
⁸ IDG/McGovern Institute for Brain Research at Tsinghua University, Beijing, China.

^# Contributed equally.

Abstract

Background: Sleep fragmentation is a persistent problem throughout the course of Parkinson's disease (PD). However, the related neurophysiological patterns and the underlying mechanisms remained unclear.

Method: We recorded subthalamic nucleus (STN) local field potentials (LFPs) using deep brain stimulation (DBS) with real-time wireless recording capacity from 13 patients with PD undergoing a one-night polysomnography recording, 1 month after DBS surgery before initial programming and when the patients were off-medication. The STN LFP features that characterised different sleep stages, correlated with arousal and sleep fragmentation index, and preceded stage transitions during N2 and REM sleep were analysed.

Results: Both beta and low gamma oscillations in non-rapid eye movement (NREM) sleep increased with the severity of sleep disturbance (arousal index (ArI)-beta_NREM: r=0.9, p=0.0001, sleep fragmentation index (SFI)-beta_NREM: r=0.6, p=0.0301; SFI-gamma_NREM: r=0.6, p=0.0324). We next examined the low-to-high power ratio (LHPR), which was the power ratio of theta oscillations to beta and low gamma oscillations, and found it to be an indicator of sleep fragmentation (ArI-LHPR_NREM: r=-0.8, p=0.0053; ArI-LHPR_REM: r=-0.6, p=0.0373; SFI-LHPR_NREM: r=-0.7, p=0.0204; SFI-LHPR_REM: r=-0.6, p=0.0428). In addition, long beta bursts (>0.25 s) during NREM stage 2 were found preceding the completion of transition to stages with more cortical activities (towards Wake/N1/REM compared with towards N3 (p<0.01)) and negatively correlated with STN spindles, which were detected in STN LFPs with peak frequency distinguishable from long beta bursts (STN spindle: 11.5 Hz, STN long beta bursts: 23.8 Hz), in occupation during NREM sleep (β=-0.24, p<0.001).

Conclusion: Features of STN LFPs help explain neurophysiological mechanisms underlying sleep fragmentations in PD, which can inform new intervention for sleep dysfunction.

Trial registration number: NCT02937727.

Keywords: PARKINSON'S DISEASE; SLEEP.

MeSH terms

Aged
Beta Rhythm / physiology
Deep Brain Stimulation*
Female
Humans
Male
Middle Aged
Parkinson Disease* / complications
Parkinson Disease* / physiopathology
Parkinson Disease* / therapy
Polysomnography*
Sleep Deprivation / physiopathology
Sleep Stages / physiology
Subthalamic Nucleus* / physiopathology

Associated data

ClinicalTrials.gov/NCT02937727