Aperiodic neural activity distinguishes between phasic and tonic <scp>REM</scp> sleep

Traditionally categorized as a uniform sleep phase, rapid eye movement sleep exhibits substantial heterogeneity with its phasic and tonic constituents showing marked differences regarding many characteristics. Here, we investigate how tonic and phasic states differ with respect to aperiodic neural activity, a marker of arousal and sleep. Rapid eye movement sleep heterogeneity was assessed using either binary phasic-tonic (n = 97) or continuous (in 60/97 participants) approach. Slopes of the aperiodic power component were measured in the low (2-30 Hz, n = 97) and high (30-48 Hz, n = 60/97) frequency bands with the Irregularly Resampled Auto-Spectral Analysis applied on electroencephalography. Rapid eye movement amplitudes were quantified with the YASA applied on electrooculography (n = 60/97). The binary approach revealed that the phasic state is characterized by steeper low-band slopes with small effect sizes and some topographical heterogeneity over datasets. High-band aperiodic slopes were flatter in the phasic versus tonic state with medium-to-large effect sizes over all areas in both datasets. The continuous approach confirmed these findings. The temporal analysis within rapid eye movement episodes revealed that aperiodic activity preceding or following EM events did not cross-correlate with eye movement amplitudes. This study demonstrates that aperiodic slopes can serve as a reliable marker able to differentiate between phasic and tonic constituents of rapid eye movement sleep and reflect phasic rapid eye movement event intensity. However, rapid eye movement events could not be predicted by preceding aperiodic activity and vice versa, at least not with scalp electroencephalography.

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Publication Details

Journal
Journal of Sleep Research
Published
2024-12-26
DOI
https://doi.org/10.1111/jsr.14439
Citations
7
Primary Topic
Sleep and Wakefulness Research
Type
article
Field-Weighted Citation Impact
2.40

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article en
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Abstract

Traditionally categorized as a uniform sleep phase, rapid eye movement sleep exhibits substantial heterogeneity with its phasic and tonic constituents showing marked differences regarding many characteristics. Here, we investigate how tonic and phasic states differ with respect to aperiodic neural activity, a marker of arousal and sleep. Rapid eye movement sleep heterogeneity was assessed using either binary phasic-tonic (n = 97) or continuous (in 60/97 participants) approach. Slopes of the aperiodic power component were measured in the low (2-30 Hz, n = 97) and high (30-48 Hz, n = 60/97) frequency bands with the Irregularly Resampled Auto-Spectral Analysis applied on electroencephalography. Rapid eye movement amplitudes were quantified with the YASA applied on electrooculography (n = 60/97). The binary approach revealed that the phasic state is characterized by steeper low-band slopes with small effect sizes and some topographical heterogeneity over datasets. High-band aperiodic slopes were flatter in the phasic versus tonic state with medium-to-large effect sizes over all areas in both datasets. The continuous approach confirmed these findings. The temporal analysis within rapid eye movement episodes revealed that aperiodic activity preceding or following EM events did not cross-correlate with eye movement amplitudes. This study demonstrates that aperiodic slopes can serve as a reliable marker able to differentiate between phasic and tonic constituents of rapid eye movement sleep and reflect phasic rapid eye movement event intensity. However, rapid eye movement events could not be predicted by preceding aperiodic activity and vice versa, at least not with scalp electroencephalography.

Journal of Sleep ResearchVol. 34(4)
Semmelweis University (HU), Eötvös Loránd University (HU), Radboud University Nijmegen (NL), Radboud University Medical Center (NL), Pázmány Péter Catholic University (HU)
Nederlandse Organisatie voor Wetenschappelijk Onderzoek
Openalex Percentile: Top 11%
Sleep and Wakefulness Research
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