Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder

Study Objectives: The subjective suffering of people with Insomnia Disorder (ID) is insufficiently accounted for by traditional sleep classification, which presumes a strict sequential occurrence of global brain states. Recent studies challenged this presumption by showing concurrent sleep- and wake...

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Main Authors: Julie Anja Engelhard Christensen, Rick Wassing, Yishul Wei, Jennifer R. Ramautar, Oti Lakbila-Kamal, Poul Jørgen Jennum, Eus J. W. Van Someren
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-07-01
Series:Frontiers in Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnins.2019.00598/full
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spelling doaj-7ac00b8fae744e5bb10e317a093597c42020-11-25T01:49:38ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-07-011310.3389/fnins.2019.00598445494Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia DisorderJulie Anja Engelhard Christensen0Julie Anja Engelhard Christensen1Rick Wassing2Yishul Wei3Jennifer R. Ramautar4Oti Lakbila-Kamal5Poul Jørgen Jennum6Eus J. W. Van Someren7Eus J. W. Van Someren8Eus J. W. Van Someren9Danish Center for Sleep Medicine, Department of Clinical Neurophysiology, Rigshospitalet Glostrup, Glostrup, DenmarkDepartment of Health Technology, Technical University of Denmark, Kongens Lyngby, DenmarkDepartment of Sleep and Cognition, Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, NetherlandsDepartment of Sleep and Cognition, Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, NetherlandsDepartment of Sleep and Cognition, Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, NetherlandsDepartment of Sleep and Cognition, Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, NetherlandsDanish Center for Sleep Medicine, Department of Clinical Neurophysiology, Rigshospitalet Glostrup, Glostrup, DenmarkDepartment of Sleep and Cognition, Netherlands Institute for Neuroscience, an Institute of the Royal Netherlands Academy of Arts and Sciences, Amsterdam, NetherlandsDepartment of Integrative Neurophysiology, Center for Neurogenomics and Cognitive Research (CNCR), Amsterdam Neuroscience, VU University Amsterdam, Amsterdam, NetherlandsAmsterdam UMC, Vrije Universiteit, Psychiatry, Amsterdam Neuroscience, Amsterdam, NetherlandsStudy Objectives: The subjective suffering of people with Insomnia Disorder (ID) is insufficiently accounted for by traditional sleep classification, which presumes a strict sequential occurrence of global brain states. Recent studies challenged this presumption by showing concurrent sleep- and wake-type neuronal activity. We hypothesized enhanced co-occurrence of diverging EEG vigilance signatures during sleep in ID.Methods: Electroencephalography (EEG) in 55 cases with ID and 64 controls without sleep complaints was subjected to a Latent Dirichlet Allocation topic model describing each 30 s epoch as a mixture of six vigilance states called Topics (T), ranked from N3-related T1 and T2 to wakefulness-related T6. For each stable epoch we determined topic dominance (the probability of the most likely topic), topic co-occurrence (the probability of the remaining topics), and epoch-to-epoch transition probabilities.Results: In stable epochs where the N1-related T4 was dominant, T4 was more dominant in ID than in controls, and patients showed an almost doubled co-occurrence of T4 during epochs where the N3-related T1 was dominant. Furthermore, patients had a higher probability of switching from T1- to T4-dominated epochs, at the cost of switching to N3-related T2-dominated epochs, and a higher probability of switching from N2-related T3- to wakefulness-related T6-dominated epochs.Conclusion: Even during their deepest sleep, the EEG of people with ID express more N1-related vigilance signatures than good sleepers do. People with ID are moreover more likely to switch from deep to light sleep and from N2 sleep to wakefulness. The findings suggest that hyperarousal never rests in ID.https://www.frontiersin.org/article/10.3389/fnins.2019.00598/fullinsomniaindiscrete labeling of sleepvigilance statestopic modelingdata-driven analysispolysomnography
collection DOAJ
language English
format Article
sources DOAJ
author Julie Anja Engelhard Christensen
Julie Anja Engelhard Christensen
Rick Wassing
Yishul Wei
Jennifer R. Ramautar
Oti Lakbila-Kamal
Poul Jørgen Jennum
Eus J. W. Van Someren
Eus J. W. Van Someren
Eus J. W. Van Someren
spellingShingle Julie Anja Engelhard Christensen
Julie Anja Engelhard Christensen
Rick Wassing
Yishul Wei
Jennifer R. Ramautar
Oti Lakbila-Kamal
Poul Jørgen Jennum
Eus J. W. Van Someren
Eus J. W. Van Someren
Eus J. W. Van Someren
Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder
Frontiers in Neuroscience
insomnia
indiscrete labeling of sleep
vigilance states
topic modeling
data-driven analysis
polysomnography
author_facet Julie Anja Engelhard Christensen
Julie Anja Engelhard Christensen
Rick Wassing
Yishul Wei
Jennifer R. Ramautar
Oti Lakbila-Kamal
Poul Jørgen Jennum
Eus J. W. Van Someren
Eus J. W. Van Someren
Eus J. W. Van Someren
author_sort Julie Anja Engelhard Christensen
title Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder
title_short Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder
title_full Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder
title_fullStr Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder
title_full_unstemmed Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder
title_sort data-driven analysis of eeg reveals concomitant superficial sleep during deep sleep in insomnia disorder
publisher Frontiers Media S.A.
series Frontiers in Neuroscience
issn 1662-453X
publishDate 2019-07-01
description Study Objectives: The subjective suffering of people with Insomnia Disorder (ID) is insufficiently accounted for by traditional sleep classification, which presumes a strict sequential occurrence of global brain states. Recent studies challenged this presumption by showing concurrent sleep- and wake-type neuronal activity. We hypothesized enhanced co-occurrence of diverging EEG vigilance signatures during sleep in ID.Methods: Electroencephalography (EEG) in 55 cases with ID and 64 controls without sleep complaints was subjected to a Latent Dirichlet Allocation topic model describing each 30 s epoch as a mixture of six vigilance states called Topics (T), ranked from N3-related T1 and T2 to wakefulness-related T6. For each stable epoch we determined topic dominance (the probability of the most likely topic), topic co-occurrence (the probability of the remaining topics), and epoch-to-epoch transition probabilities.Results: In stable epochs where the N1-related T4 was dominant, T4 was more dominant in ID than in controls, and patients showed an almost doubled co-occurrence of T4 during epochs where the N3-related T1 was dominant. Furthermore, patients had a higher probability of switching from T1- to T4-dominated epochs, at the cost of switching to N3-related T2-dominated epochs, and a higher probability of switching from N2-related T3- to wakefulness-related T6-dominated epochs.Conclusion: Even during their deepest sleep, the EEG of people with ID express more N1-related vigilance signatures than good sleepers do. People with ID are moreover more likely to switch from deep to light sleep and from N2 sleep to wakefulness. The findings suggest that hyperarousal never rests in ID.
topic insomnia
indiscrete labeling of sleep
vigilance states
topic modeling
data-driven analysis
polysomnography
url https://www.frontiersin.org/article/10.3389/fnins.2019.00598/full
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