Abstract

ObjectiveThe stage of sleep is a known modulator of high-frequency oscillations (HFOs). For instance, high amplitude slow waves during NREM sleep and the subtypes of REM sleep were shown to contribute to a better separation between physiological and pathological HFOs. This study investigated rates and spatial spread of the different HFO types (physiological and pathological ripples in the 80–250 Hz frequency band, and fast ripples above 250 Hz) depending on time spent in sleep across the different sleep cycles.MethodsFifteen patients with focal pharmaco-resistant epilepsy underwent one night of video-polysomnography during chronic intracranial EEG recording for presurgical epilepsy evaluation. The HFO rate and spread across the different sleep cycles were determined with an automatic HFO detector. We built models to explain the observed rate and spread based on time in sleep and other variables i.e. sleep stage, delta band and sigma band activity, and slow wave amplitude. Statistical significance of the different variables was determined by a model comparison using the Akaike information criterion.ResultsThe rate of HFOs depends significantly on the accumulated time of sleep. As the night advanced, the rate of pathological ripples and fast ripples decreased during NREM sleep (up to 15% per hour spent in the respective sleep stages), while the rate of physiological ripples increased during REM sleep (8% per hour spent in REM sleep). Interestingly, the stage of sleep but not the sleep cycle determined the extent of spread of HFOs, showing a larger field during NREM sleep and a more restricted field during REM sleep.ConclusionThe different dependence with sleep time for physiological and pathological ripples is in keeping with their distinct underlying generating mechanisms. From a practical point of view, the first sleep cycle seems to be best suitable for studying HFOs in epilepsy, given that the contrast between physiological and pathological ripple rates is largest during this time.

Highlights

  • High-frequency oscillations N80 Hz (HFOs), which can be divided into ripples (80–250 Hz) and fast ripples (N250 Hz), are a new biomarker of epilepsy

  • The major findings of this work are (i) the presence of a sleep-homeostatic variation of the rate of high-frequency oscillations (HFOs) across the different sleep cycles, (ii) a difference in the behavior of physiological versus pathological HFOs with sleep time, with the highest difference in rates of physiological and pathological HFOs occurring during the first sleep cycle, and (iii) a modulation of the spread of HFOs by the different sleep stages, but not the different sleep cycles

  • We showed that physiological HFOs are closely linked to phasic REM sleep (Frauscher et al, 2016), which is suggested to play an important role in learning and memory (Buzsáki et al, 1992; Datta, 2000, Datta et al, 2004; Diekelmann et al, 2009)

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Summary

Introduction

High-frequency oscillations N80 Hz (HFOs), which can be divided into ripples (80–250 Hz) and fast ripples (N250 Hz), are a new biomarker of epilepsy (see review of Frauscher et al, 2017, submitted). N. von Ellenrieder et al / NeuroImage: Clinical 14 (2017) 566–573 phasic compared to tonic REM sleep (Frauscher et al, 2016). These studies suggest that the coupling to sleep transients might be useful to separate physiological from pathological HFOs. For instance, adding the coupling to slow waves increases the discrimination between physiological and pathological HFOs (von Ellenrieder et al, 2016)

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