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

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 sti...

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Main Authors: Zhang, G, Yu, H, Chen, Y, Gong, C, Hao, H, Guo, Y, Xu, S, Zhang, Y, Yuan, X, Yin, G, Zhang, J, Tan, H, Li, L
Format: Journal article
Language:English
Published: BMJ Publishing Group 2024
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author Zhang, G
Yu, H
Chen, Y
Gong, C
Hao, H
Guo, Y
Xu, S
Zhang, Y
Yuan, X
Yin, G
Zhang, J
Tan, H
Li, L
author_facet Zhang, G
Yu, H
Chen, Y
Gong, C
Hao, H
Guo, Y
Xu, S
Zhang, Y
Yuan, X
Yin, G
Zhang, J
Tan, H
Li, L
author_sort Zhang, G
collection OXFORD
description 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)-betaNREM: r=0.9, p=0.0001, 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 (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-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 (>0.25 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.
first_indexed 2024-09-25T04:16:43Z
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spelling oxford-uuid:34d1d425-8a6c-487b-b001-4f5a5512f1572024-10-16T09:40:48ZNeurophysiological features of STN LFP underlying sleep fragmentation in Parkinson’s diseaseJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:34d1d425-8a6c-487b-b001-4f5a5512f157EnglishJisc Publications RouterBMJ Publishing Group2024Zhang, GYu, HChen, YGong, CHao, HGuo, YXu, SZhang, YYuan, XYin, GZhang, JTan, HLi, LBackground: 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)-betaNREM: r=0.9, p=0.0001, 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 (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-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 (>0.25 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.
spellingShingle Zhang, G
Yu, H
Chen, Y
Gong, C
Hao, H
Guo, Y
Xu, S
Zhang, Y
Yuan, X
Yin, G
Zhang, J
Tan, H
Li, L
Neurophysiological features of STN LFP underlying sleep fragmentation in Parkinson’s disease
title Neurophysiological features of STN LFP underlying sleep fragmentation in Parkinson’s disease
title_full Neurophysiological features of STN LFP underlying sleep fragmentation in Parkinson’s disease
title_fullStr Neurophysiological features of STN LFP underlying sleep fragmentation in Parkinson’s disease
title_full_unstemmed Neurophysiological features of STN LFP underlying sleep fragmentation in Parkinson’s disease
title_short Neurophysiological features of STN LFP underlying sleep fragmentation in Parkinson’s disease
title_sort neurophysiological features of stn lfp underlying sleep fragmentation in parkinson s disease
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