Abstract

During the sleep onset (SO) process, the human electroencephalogram (EEG) is characterized by an orchestrated pattern of spatiotemporal changes. Sleep deprivation (SD) strongly affects both wake and sleep EEG, but a description of the topographical EEG power spectra and oscillatory activity during the wake-sleep transition after a period of prolonged wakefulness is still missing. The increased homeostatic sleep pressure should induce an earlier onset of sleep-related EEG oscillations. The aim of the present study was to assess the spatiotemporal EEG pattern at SO following SD. A dataset of a previous study was analyzed. We assessed the spatiotemporal EEG changes (19 cortical derivations) during the SO (5 min before vs. 5 min after the first epoch of Stage 2) of a recovery night after 40 h of SD in 39 healthy subjects, analyzing the EEG power spectra (fast Fourier transform) and the oscillatory activity [better oscillation (BOSC) detection method]. The spatiotemporal pattern of the EEG power spectra mostly confirmed the changes previously observed during the wake-sleep transition at baseline. The comparison between baseline and recovery showed a wide increase of the post- vs. pre-SO ratio during the recovery night in the frequency bins ≤10 Hz. We found a predominant alpha oscillatory rhythm in the pre-SO period, while after SO the theta oscillatory activity was prevalent. The oscillatory peaks showed a generalized increase in all frequency bands from delta to sigma with different predominance, while beta activity increased only in the fronto-central midline derivations. Overall, the analysis of the EEG power replicated the topographical pattern observed during a baseline night of sleep but with a stronger intensity of the SO-induced changes in the frequencies ≤10 Hz, and the detection of the rhythmic activity showed the rise of several oscillations at SO after SD that was not observed during the wake-sleep transition at baseline (e.g., alpha and frontal theta in correspondence of their frequency peaks). Beyond confirming the local nature of the EEG pattern at SO, our results show that SD has an impact on the spatiotemporal modulation of cortical activity during the falling-asleep process, inducing the earlier emergence of sleep-related EEG oscillations.

Highlights

  • Sleep is widely considered as a local and use-dependent process, since regional patterns of activation and deactivation coexist in the brain during sleep, and recent evidence suggests that large regional heterogeneities occur during specific transitional states

  • We found a significant (p ≤ 0.0005 corresponding to t ≥ 3.79 after the Bonferroni correction) differences between pre- and post-sleep onset (SO) in all cortical derivations in the ≤8 Hz frequency range, in the direction of a power increase after SO

  • The interest for the characterization of the local brain activity during the SO process is growing, and our findings appear complementary to recent observations on the effect of Sleep deprivation (SD) on the wake-sleep transition assessed with EEG source localization and effective connectivity (Fernandez Guerrero and Achermann, 2018, 2019)

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Summary

Introduction

Sleep is widely considered as a local and use-dependent process, since regional patterns of activation and deactivation coexist in the brain during sleep, and recent evidence suggests that large regional heterogeneities occur during specific transitional states (for review see Ferrara and De Gennaro, 2011; Siclari and Tononi, 2017). The sleep onset (SO) period represents a complex phenomenon of transition between two different functional states (i.e., wakefulness and sleep) of the brain in which the fluctuation of consciousness seems to result from topographically heterogeneous cortical activities (Gorgoni et al, 2019). We cannot exclude that these unexpected findings were due to the short window considered for the SO period (i.e., the two 5-min intervals before and after the first epoch of stage 2), which could make not viable the observation of specific EEG oscillatory activities with a more delayed build-up

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