A high-density electroencephalography study reveals abnormal sleep homeostasis in patients with rapid eye movement sleep behavior disorder

David T Plante,Giulio Tononi,Melanie Boly,Keith P Nakamura,Amandine Valomon,Brady A Riedner,Ruth M Benca,Stephanie G Jones

doi:10.1038/s41598-021-83980-w

Abstract

Rapid eye movement (REM) sleep behavior disorder (RBD) is characterized by disrupting motor enactments during REM sleep, but also cognitive impairments across several domains. In addition to REM sleep abnormalities, we hypothesized that RBD patients may also display EEG abnormalities during NREM sleep. We collected all-night recordings with 256-channel high-density EEG in nine RBD patients, predominantly early-onset medicated individuals, nine sex- and age- matched healthy controls, and nine additional controls with matched medications and comorbidities. Power spectra in delta to gamma frequency bands were compared during both REM and NREM sleep, between phasic and tonic REM sleep, and between the first versus last cycle of NREM sleep. Controls, but not RBD patients, displayed a decrease in beta power during phasic compared to tonic REM sleep. Compared to controls, RBD patients displayed a reduced decline in SWA from early to late NREM sleep. Overnight changes in the distribution of the amplitude of slow waves were also reduced in RBD patients. Without suppression of beta rhythms during phasic REM sleep, RBD patients might demonstrate heightened cortical arousal, favoring the emergence of behavioral episodes. A blunted difference between REM sleep sub-stages may constitute a sensitive biomarker for RBD. Moreover, reduced overnight decline in SWA suggests a reduced capacity for synaptic plasticity in RBD patients, which may favor progression towards neurodegenerative diseases.

Highlights

Rapid eye movement (REM) sleep behavior disorder (RBD) is characterized by disrupting motor enactments during rapid eye movements (REMs) sleep, and cognitive impairments across several domains
In line with the synaptic homeostasis h ypothesis[42,43], a wealth of data have shown that cortical circuits undergo net synaptic potentiation during wake, and a subsequent renormalization of synaptic strength during sleep at night, which can both be tracked by assessing changes in EEG slow-wave activity (SWA) during NREM sleep[44,45]
Relative to non-medicated healthy controls (NMC), RBD patients and medicated controls (MC) had increased time spent in N1 sleep and decreased time spent in N3 sleep (% N1: p = 0.017, 8.2 to 12.8% in MC and RBD vs 4.5% in NMC, % N3: p = 0.043, 4.8 to 8.6% in MC and RBD vs 14.9% in NMC)

Summary

Introduction

Rapid eye movement (REM) sleep behavior disorder (RBD) is characterized by disrupting motor enactments during REM sleep, and cognitive impairments across several domains. In addition to REM sleep abnormalities, we hypothesized that RBD patients may display EEG abnormalities during NREM sleep. But not RBD patients, displayed a decrease in beta power during phasic compared to tonic REM sleep. RBD patients displayed a reduced decline in SWA from early to late NREM sleep. Reduced overnight decline in SWA suggests a reduced capacity for synaptic plasticity in RBD patients, which may favor progression towards neurodegenerative diseases. If the regulation of phasic vs tonic REM sleep was altered in motor, visual and limbic cortex in RBD patients, it may predispose them to behavioral enactment during REM s leep[26]. We hypothesized that RBD patients may display REM sleep abnormalities, and abnormal sleep SWA homeostasis during NREM sleep

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Discussion

Conclusion