Brain-wide properties of slow waves across vigilance states

Abstract

Until recently, slow waves (SWs) were considered to be highly specific, if not exclusive, to sleep and non-rapid eye movement (NREM) sleep in particular. During NREM sleep, they are proposed to track and contribute to normalization of homeostatic sleep pressure. However, recent evidence has identified typical SWs during wakefulness and rapid-eye movement (REM) sleep. SWs during wakefulness have been regarded as intrusions of sleep, supported by the finding of an associated down-state of neural activity. Although this suggests that the underlying neurobiology of SWs might be shared across vigilance states, i.e., the activity of neurons is comparable, it does not address the question as to whether SWs display state-dependent differences that could reflect a homeostatic regulation. To address this question, we utilized an intracranial dataset of 106 adult patients with drug-resistant epilepsy and computed specific features of SWs – their incidence, slope, transition frequency, associated high gamma (HG) activity, multipeak morphology and overlap across brain regions. Overall, we found that changes in these features reflect a state-dependent modulation, potentially in line with expected changes in homeostatic pressure. The multipeak morphology displayed the greatest changes across states. SW differences were sufficiently specific to vigilance state that we could successfully classify these states using SW properties. Our work provides further evidence that SWs during wakefulness and REM sleep are consistent with intrusion of NREM-SW and establish normative values for future studies on SWs across vigilance states and brain regions.