Theta waves in children\u2019s waking electroencephalogram resemble local aspects of sleep during wakefulness

Sara Fattinger,Salome Kurth,Oskar G Jenni,Reto Huber,Maya Ringli

doi:10.1038/s41598-017-11577-3

Abstract

Vyazovskiy and colleagues found in rats’ multi-unit recordings brief periods of silence (off-states) in local populations of cortical neurons during wakefulness which closely resembled the characteristic off-states during sleep. These off-states became more global and frequent with increasing sleep pressure and were associated with the well-known increase of theta activity under sleep deprivation in the surface EEG. Moreover, the occurrence of such off-states was related to impaired performance. While these animal experiments were based on intracranial recordings, we aimed to explore whether the human surface EEG may also provide evidence for such a local sleep-like intrusion during wakefulness. Thus, we analysed high-density wake EEG recordings during an auditory attention task in the morning and evening in 12 children. We found that, theta waves became more widespread in the evening and the occurrence of widespread theta waves was associated with slower reaction times in the attention task. These results indicate that widespread theta events measured on the scalp might be markers of local sleep in humans. Moreover, such markers of local sleep, seem to be related to the well described performance decline under high sleep pressure.

Highlights

Sleep and wakefulness are clearly separable brain states, but are yet critically dependent on each other
Intracranial recordings of brain activity in patients suffering from drug resistant epilepsy show clear signs of wakefulness-like activity typically observed over sensorimotor areas[9]
We investigated whether the surface EEG likewise provides evidence for such local intrusion of one brain state into the other that is local sleep during wakefulness

Summary

Introduction

Sleep and wakefulness are clearly separable brain states, but are yet critically dependent on each other. The question arises whether local sleep (off-states) of cortical neurons during wakefulness, which seem to reflect waking theta activity, can account for the performance impairment. To address this question, Vyazovskiy et al.[10] trained rats on a sugar pellet reaching task. The results showed significantly more off-states (300–800 ms) prior to an unsuccessful reaching attempt as compared to successful trials These data indicate that local populations of cortical neurons that “fall asleep” may be responsible for the impaired performance following sleep deprivation. We analysed high-density (hd, 128 channels) wake EEG recordings which provide a good spatial resolution and examined children because they generally show a pronounced increase in sleep need and a high signal to noise ratio

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