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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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Autores principales: Christensen, Julie Anja Engelhard, Wassing, Rick, Wei, Yishul, Ramautar, Jennifer R., Lakbila-Kamal, Oti, Jennum, Poul Jørgen, Van Someren, Eus J. W.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6629891/
https://www.ncbi.nlm.nih.gov/pubmed/31338014
http://dx.doi.org/10.3389/fnins.2019.00598
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author Christensen, Julie Anja Engelhard
Wassing, Rick
Wei, Yishul
Ramautar, Jennifer R.
Lakbila-Kamal, Oti
Jennum, Poul Jørgen
Van Someren, Eus J. W.
author_facet Christensen, Julie Anja Engelhard
Wassing, Rick
Wei, Yishul
Ramautar, Jennifer R.
Lakbila-Kamal, Oti
Jennum, Poul Jørgen
Van Someren, Eus J. W.
author_sort Christensen, Julie Anja Engelhard
collection PubMed
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.
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spelling pubmed-66298912019-07-23 Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder Christensen, Julie Anja Engelhard Wassing, Rick Wei, Yishul Ramautar, Jennifer R. Lakbila-Kamal, Oti Jennum, Poul Jørgen Van Someren, Eus J. W. Front Neurosci Neuroscience 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. Frontiers Media S.A. 2019-07-09 /pmc/articles/PMC6629891/ /pubmed/31338014 http://dx.doi.org/10.3389/fnins.2019.00598 Text en Copyright © 2019 Christensen, Wassing, Wei, Ramautar, Lakbila-Kamal, Jennum and Van Someren. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Christensen, Julie Anja Engelhard
Wassing, Rick
Wei, Yishul
Ramautar, Jennifer R.
Lakbila-Kamal, Oti
Jennum, Poul Jørgen
Van Someren, Eus J. W.
Data-Driven Analysis of EEG Reveals Concomitant Superficial Sleep During Deep Sleep in Insomnia Disorder
title 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_short 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
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6629891/
https://www.ncbi.nlm.nih.gov/pubmed/31338014
http://dx.doi.org/10.3389/fnins.2019.00598
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