Intracerebral Dynamics of Sleep Arousals: A Combined Scalp–Intracranial EEG Study
- Yingqi Laetitia Wang1,*,
- Tamir Avigdor1,*,
- Sana Hannan2,
- Chifaou Abdallah1,
- François Dubeau3,
- Laure Peter-Derex4, and
- Birgit Frauscher1,5
- 1Analytical Neurophysiology Lab, Montreal Neurological Institute, McGill University, Montreal, Quebec H3A 2B4, Canada
- 2Department of Biomedical and Life Sciences, Lancaster University, Lancaster LA1 4YW, United Kingdom
- 3Montreal Neurological Institute, McGill University, Montreal, Quebec H3A 2B4, Canada
- 4Centre de Médecine du Sommeil et des Maladies respiratoires, University Hospital of Lyon, Lyon 1 University, Lyon 69004, France
- 5Analytical Neurophysiology Lab, Departments of Neurology & Biomedical Engineering, Duke University, Durham, North Carolina 27705
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Author contributions: Y.L.W., T.A., S.H., L.P.-D., and B.F. designed research; Y.L.W., T.A., C.A., L.P.-D., and B.F. performed research; F.D., L.P.-D., and B.F. contributed unpublished reagents/analytic tools; Y.L.W., T.A., and B.F. analyzed data; Y.L.W. and B.F. wrote the paper.
Abstract
As an intrinsic component of sleep architecture, sleep arousals represent an intermediate state between sleep and wakefulness and are important for sleep–wake regulation. They are defined in an all-or-none manner, whereas they actually present a wide range of scalp-electroencephalography (EEG) activity patterns. It is poorly understood how these arousals differ in their mechanisms. Stereo-EEG (SEEG) provides the unique opportunity to record intracranial activities in superficial and deep structures in humans. Using combined polysomnography and SEEG, we quantitatively categorized arousals during nonrapid eye movement sleep into slow wave (SW) and non-SW arousals based on whether they co-occurred with a scalp-EEG SW event. We then investigated their intracranial correlates in up to 26 brain regions from 26 patients (12 females). Across both arousal types, intracranial theta, alpha, sigma, and beta activities increased in up to 25 regions (p < 0.05; d = 0.06–0.63), while gamma and high-frequency (HF) activities decreased in up to 18 regions across the five brain lobes (p < 0.05; d = 0.06–0.44). Intracranial delta power widely increased across five lobes during SW arousals (p < 0.05 in 22 regions; d = 0.10–0.39), while it widely decreased during non-SW arousals (p < 0.05 in 19 regions; d = 0.10–0.30). Despite these main patterns, unique activities were observed locally in some regions such as the hippocampus and middle cingulate cortex, indicating spatial heterogeneity of arousal responses. Our results suggest that non-SW arousals correspond to a higher level of brain activation than SW arousals. The decrease in HF activities could potentially explain the absence of awareness and recollection during arousals.
- Received April 10, 2023.
- Revision received February 5, 2024.
- Accepted February 12, 2024.
- Copyright © 2024 the authors





