Functional Structure of Spontaneous Sleep Slow Oscillation Activity in Humans

Danilo Menicucci,Andrea Piarulli,Paola D'Ascanio,Alberto Landi,Ursula Debarnot,Angelo Gemignani,Clayton T Dickson

doi:10.1371/journal.pone.0007601

Abstract

BackgroundDuring non-rapid eye movement (NREM) sleep synchronous neural oscillations between neural silence (down state) and neural activity (up state) occur. Sleep Slow Oscillations (SSOs) events are their EEG correlates. Each event has an origin site and propagates sweeping the scalp. While recent findings suggest a SSO key role in memory consolidation processes, the structure and the propagation of individual SSO events, as well as their modulation by sleep stages and cortical areas have not been well characterized so far.Methodology/Principal FindingsWe detected SSO events in EEG recordings and we defined and measured a set of features corresponding to both wave shapes and event propagations. We found that a typical SSO shape has a transition to down state, which is steeper than the following transition from down to up state. We show that during SWS SSOs are larger and more locally synchronized, but less likely to propagate across the cortex, compared to NREM stage 2. Also, the detection number of SSOs as well as their amplitudes and slopes, are greatest in the frontal regions. Although derived from a small sample, this characterization provides a preliminary reference about SSO activity in healthy subjects for 32-channel sleep recordings.Conclusions/SignificanceThis work gives a quantitative picture of spontaneous SSO activity during NREM sleep: we unveil how SSO features are modulated by sleep stage, site of origin and detection location of the waves. Our measures on SSOs shape indicate that, as in animal models, onsets of silent states are more synchronized than those of neural firing. The differences between sleep stages could be related to the reduction of arousal system activity and to the breakdown of functional connectivity. The frontal SSO prevalence could be related to a greater homeostatic need of the heteromodal association cortices.

Highlights

Sleep Slow Oscillations (SSOs) have been recently revealed and are increasingly attracting the attention of neurophysiologists as EEG characteristic signals during sleep [1,2,3,4]
In this paper we generalize the detection criteria of Massimini et al [5] (MDC): We still detect propagating SSO events looking for waves satisfying these detection criteria but we introduce a likeness rule to complete the identification of the events
SSOs were detected all over the scalp but with a prevalence over the frontocentral areas and, on average, SSOs travel at a mean speed of

Summary

Introduction

Sleep Slow Oscillations (SSOs) have been recently revealed and are increasingly attracting the attention of neurophysiologists as EEG characteristic signals during sleep [1,2,3,4]. It has been shown that individual events of SSO emerge from the background activity of the deepest stages of NREM sleep and spread over large areas of cortex [5]. This rhythmic activity, which originates in the cortex [6] and reverberates in subcortical structures [7,8], was detected during sleep in humans through electroencephalographical (EEG) and magnetoencephalographical recordings [2,3,5,9], and functional magnetic resonance imaging scans [10]. While recent findings suggest a SSO key role in memory consolidation processes, the structure and the propagation of individual SSO events, as well as their modulation by sleep stages and cortical areas have not been well characterized so far

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