Aperiodic neural activity distinguishes between phasic and tonic REM sleep

Abstract Introduction Traditionally categorized as a uniform sleep phase, rapid eye movement (REM) sleep exhibits substantial heterogeneity with its phasic and tonic constituents showing marked differences regarding neuronal network activity, environmental alertness and information processing. Here, we investigate how tonic and phasic states differ with respect to aperiodic neural activity, a marker of arousal levels, sleep stages, depth of sleep and sleep intensity. We also attempt to challenge the binary categorisation of REM sleep states by introducing graduality into their definition. Specifically, we quantify the intensity of phasic oculomotor events and investigate their temporal relationships with aperiodic activity. Method We analyzed 57 polysomnographic recordings from three open-access datasets of healthy young volunteers aged 21.7±1.4 years. REM sleep heterogeneity was assessed using either binary phasic-tonic categorization or quantification of eye movement (EM) amplitudes detected by electrooculography with the YASA algorithm. Slopes of the aperiodic power component measured by electroencephalography in the low (2–30Hz) and high (30–48Hz) frequency bands were calculated using the Irregularly Resampled Auto-Spectral Analysis. For statistical analyses, we used ANOVA, Spearman correlations and cross-correlations. Results The binary approach revealed that the phasic state is characterized by steeper low-band aperiodic slopes compared to the tonic state with the strongest effect observed over the frontal area. The phasic state also showed flatter high-band slopes with the strongest effect over central and parietal areas. The gradual approach confirmed this result further showing that higher EM amplitudes are linked to steeper low-band and flatter high-band aperiodic slopes. The temporal analysis within REM episodes revealed that aperiodic activity preceding or following EM events did not cross-correlate with EM amplitudes. Conclusion This study demonstrates that aperiodic slopes can serve as a reliable objective marker able to differentiate between phasic and tonic constituents of REM sleep and reflect the intensity of phasic oculomotor events for instantaneous measurements. However, EM events could not be predicted by preceding aperiodic activity and vice versa, at least not with scalp electroencephalography.