Temporal progression of sleep electroencephalography features in isolated rapid eye movement sleep behaviour disorder

Abstract

Previous studies indicated that patients with isolated rapid eye movement (REM) sleep behaviour disorder (iRBD) exhibit alterations in spectral electroencephalographic (EEG), spindle, and slow-wave features. As it is currently unknown how these EEG features evolve over time, this study aimed to evaluate their temporal progression in patients with iRBD in comparison to controls. We included 23 patients with iRBD and 23 controls. Two polysomnographies (baseline and follow-up) were recorded with a mean (standard deviation) interval of 4.0 (2.5) years and were automatically analysed for sleep stages, spectral bandpower, spindles, and slow waves. We used linear models to evaluate differences at each time point, and linear mixed-effects models to analyse differences in temporal progression between the groups. At baseline, patients with iRBD presented EEG slowing both in REM (expressed as significantly reduced α-bandpower and increased δ-bandpower in frontal channels) and in non-REM (NREM) sleep (significantly increased slow-to-fast ratio in central channels). These differences vanished at follow-up. In both REM and NREM sleep, γ-bandpower was increased at follow-up in patients with iRBD, resulting in significantly different temporal progression between groups (in occipital channels during REM sleep and frontal channels during NREM sleep). Relative power of sleep spindles was significantly higher at baseline in patients with iRBD in frontal channels, but we observed a significant reduction over time in central channels. Finally, slow waves were significantly shorter in patients with iRBD at both time-points. Our results underscore the need of considering longitudinal data when analysing sleep EEG features in patients with iRBD. The observed temporal changes as markers of progression of neurodegeneration require further investigations.

Keywords: computerised methods; electrophysiology; prodromal alpha‐synucleinopathy.

FIGURE 1

Electroencephalogram features in rapid eye movement (REM) sleep. The figure reports bandpower values measured during REM sleep for which a significant difference at baseline, follow‐up or in the temporal progression between groups was observed: (a) δ‐bandpower, (b) α‐bandpower, and (c) γ‐bandpower. For each graph, the brain region where the difference was observed is specified on top of the graph. Translucent points represent the values of each individual subject, while error bars showing the standard error are centred at the mean. Stars denote significant differences at baseline or follow‐up. Stars in between baseline and follow‐up denote significant difference in change over time. iRBD, isolated REM sleep behaviour disorder; Rel., relative.

FIGURE 2

Electroencephalogram features in non‐rapid eye movement (NREM) sleep. The figure reports bandpower values measured during NREM sleep for which a significant difference at baseline, follow‐up or in the temporal progression between groups was observed: (a,b) γ‐bandpower and (c) slow‐to‐fast ratio. For each graph, the brain region where the difference was observed is specified on top of the graph. Translucent points represent the values of each individual subject, while error bars showing the standard error are centred at the mean. Stars denote significant differences at baseline or follow‐up. Stars in between baseline and follow‐up denote significant difference in change over time. iRBD, isolated REM sleep behaviour disorder; Rel., relative.

FIGURE 3

Spindle features. The figure reports relative spindle power, the only feature for which a significant difference at baseline, or in the temporal progression between groups was observed. For each graph, the brain region where the difference was observed is specified on top of the graph. Translucent points represent the values of each individual subject, while error bars showing the standard error are centred at the mean. Stars denote significant differences at baseline. Stars in between baseline and follow‐up denote significant difference in change over time. iRBD, isolated rapid eye movement sleep behaviour disorder; Rel., relative.

FIGURE 4

Slow wave features. The figure reports relative slow wave duration, the only feature for which a significant difference at baseline or follow‐up between groups was observed. For each graph, the brain region where the difference was observed is specified on top of the graph. Translucent points represent the values of each individual subject, while error bars showing the standard error are centred at the mean. Stars denote significant differences at baseline or follow‐up. iRBD, isolated rapid eye movement sleep behaviour disorder.