Abstract

Specific patterns of brain activity during sleep and waking are recorded in the electroencephalogram (EEG). Time-frequency analysis methods have been widely used to analyse the EEG and identified characteristic oscillations for each vigilance state (VS), i.e., wakefulness, rapid-eye movement (REM) and non-rapid-eye movement (NREM) sleep. However, other aspects such as change of patterns associated with brain dynamics may not be captured unless a non-linear-based analysis method is used. In this pilot study, Permutation Lempel–Ziv complexity (PLZC), a novel symbolic dynamics analysis method, was used to characterise the changes in the EEG in sleep and wakefulness during baseline and recovery from sleep deprivation (SD). The results obtained with PLZC were contrasted with a related non-linear method, Lempel–Ziv complexity (LZC). Both measure the emergence of new patterns. However, LZC is dependent on the absolute amplitude of the EEG, while PLZC is only dependent on the relative amplitude due to symbolisation procedure and thus, more resistant to noise. We showed that PLZC discriminates activated brain states associated with wakefulness and REM sleep, which both displayed higher complexity, compared to NREM sleep. Additionally, significantly lower PLZC values were measured in NREM sleep during the recovery period following SD compared to baseline, suggesting a reduced emergence of new activity patterns in the EEG. These findings were validated using PLZC on surrogate data. By contrast, LZC was merely reflecting changes in the spectral composition of the EEG. Overall, this study implies that PLZC is a robust non-linear complexity measure, which is not dependent on amplitude variations in the signal, and which may be useful to further assess EEG alterations induced by environmental or pharmacological manipulations.

Highlights

  • Sleep is an essential part of everyday life

  • Significantly lower Permutation Lempel–Ziv complexity (PLZC) values were measured in non-rapid-eye movement (NREM) sleep during the recovery period following sleep deprivation (SD) compared to baseline, suggesting a reduced emergence of new activity patterns in the EEG

  • Cortical and subcortical brain structures contribute to the generation of oscillatory dynamic activities that are reflected in the electroencephalogram (EEG)

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Summary

Introduction

Sleep is an essential part of everyday life. It affects a wide range of processes from cognitive performance and learning capabilities [1] to physical and emotional well-being that are thought to be related to neuronal plasticity [2,3]. Cortical and subcortical brain structures contribute to the generation of oscillatory dynamic activities that are reflected in the electroencephalogram (EEG). The characterisation of these oscillatory dynamics has received a lot of interest in sleep medicine for the past 50 years in the context of mental health, including neurodegeneration [4,5]. Maintenance and transitions between vigilances states (VS) are regulated by changes in neural networks resulting in the cortical activity recorded by the EEG [7]. These dynamic changes in the EEG display various amplitudes (i.e., low amplitude in wakefulness and REM sleep and high amplitude in NREM sleep) and specific spectral features. Analysis of the EEG is based on the visual and/or automated scoring of vigilance states on epochs of various durations using defined criteria both in humans [8,9] and rodents [10,11]

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