Neurophysiological Features of STN LFP underlying Sleep Fragmentation in Parkinson’s Disease

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 DBS with real-time wireless recording capacity from thirteen PD patients undergoing a one-night polysomnography recording, one month after DBS surgery before initial programming and when the patients were Off-Medication. The STN LFP features that characterized different sleep stages, correlated with arousal and sleep fragmentation index, and preceded stage transitions during N2 and REM sleep were analyzed.Results Both beta and low gamma oscillations in NREM sleep increased with the severity of sleep disturbance (arousal index (ArI)-betaNREM: r=0.9,p=0.0001) and sleep fragmentation index (SFI)-betaNREM: r=0.6,p=0.0301; SFI-gammaNREM: r=0.6,p=0.0324). We next examined the low-to-high power ratio, 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-LHPRNREM: r=-0.8,p=0.0053; ArI-LHPRREM: r=-0.6,p=0.0373; SFI-LHPRNREM: r=-0.7,p=0.0204; SFI-LHPRREM: r=-0.6,p=0.0428). In addition, long beta bursts (>0.25s) 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: 11.5Hz, STN long beta bursts: 23.8Hz), 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.What is already known on this topic Beta oscillation, which is a biomarker for rigidity and bradykinesia during awake, significantly reduced during NREM sleep compared to REM or awake. Researches from MPTP non-human primate model suggested increased beta oscillation in basal ganglia contributed to insomnia in PD, however evidence in human patients is still lacking.What this study adds Beta and low gamma band activities in STN LFPs during sleep recorded from human PD patients correlated with severity of sleep impairment. The low-high power ratio can serve as a biomarker for sleep fragmentation. Besides, pathological beta bursts and physiological sleep spindles can be detected in STN LFP during NREM sleep and distinguishable from each other.How this study might affect research, practice or policy These findings enhance our understanding of the electrophysiological mechanisms that underlie sleep fragmentation in Parkinson’s disease. The study also has implications on the design of closed-loop DBS: we may need to take multiple frequency band activities into consideration and differentiate pathological beta oscillation from the sleep spindles..

Medienart:

Preprint

Erscheinungsjahr:

2023

Erschienen:

2023

Enthalten in:

bioRxiv.org - (2023) vom: 27. Okt. Zur Gesamtaufnahme - year:2023

Sprache:

Englisch

Beteiligte Personen:

Zhang, Guokun [VerfasserIn]
Yu, Huiling [VerfasserIn]
Chen, Yue [VerfasserIn]
Gong, Chen [VerfasserIn]
Hao, Hongwei [VerfasserIn]
Guo, Yi [VerfasserIn]
Xu, Shujun [VerfasserIn]
Zhang, Yuhuan [VerfasserIn]
Yuan, Xuemei [VerfasserIn]
Yin, Guoping [VerfasserIn]
Zhang, Jianguo [VerfasserIn]
Tan, Huiling [VerfasserIn]
Li, Luming [VerfasserIn]

Links:

Volltext [kostenfrei]

Themen:

570
Biology

doi:

10.1101/2023.10.19.563075

funding:

Förderinstitution / Projekttitel:

PPN (Katalog-ID):

XBI04128884X