Data-driven analysis of EEG reveals concomitant superficial sleep during deep sleep in insomnia disorder

Julie Anja Engelhard Christensen, Rick Wassing, Yishul Wei, Jennifer R. Ramautar, Oti Lakbila-Kamal, Poul Jørgen Jennum, Eus J.W. Van Someren*

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

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Abstract

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.
Original languageEnglish
Article number598
JournalFrontiers in Neuroscience
Volume13
Number of pages12
ISSN1662-4548
DOIs
Publication statusPublished - 2019

Keywords

  • Insomnia
  • Indiscrete labeling of sleep
  • Vigilance states
  • Topic modeling
  • Data-driven analysis
  • Polysomnography
  • Latent Dirichlet allocation

Cite this

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. In: Frontiers in Neuroscience. 2019 ; Vol. 13.
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title = "Data-driven analysis of EEG reveals concomitant superficial sleep during deep sleep in insomnia disorder",
abstract = "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.",
keywords = "Insomnia, Indiscrete labeling of sleep, Vigilance states, Topic modeling, Data-driven analysis, Polysomnography, Latent Dirichlet allocation",
author = "Christensen, {Julie Anja Engelhard} and Rick Wassing and Yishul Wei and Ramautar, {Jennifer R.} and Oti Lakbila-Kamal and Jennum, {Poul J{\o}rgen} and {Van Someren}, {Eus J.W.}",
year = "2019",
doi = "10.3389/fnins.2019.00598",
language = "English",
volume = "13",
journal = "Frontiers in Neuroscience",
issn = "1662-4548",
publisher = "Frontiers Research Foundation",

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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.

In: Frontiers in Neuroscience, Vol. 13, 598, 2019.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Data-driven analysis of EEG reveals concomitant superficial sleep during deep sleep in insomnia disorder

AU - Christensen, Julie Anja Engelhard

AU - Wassing, Rick

AU - Wei, Yishul

AU - Ramautar, Jennifer R.

AU - Lakbila-Kamal, Oti

AU - Jennum, Poul Jørgen

AU - Van Someren, Eus J.W.

PY - 2019

Y1 - 2019

N2 - 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.

AB - 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.

KW - Insomnia

KW - Indiscrete labeling of sleep

KW - Vigilance states

KW - Topic modeling

KW - Data-driven analysis

KW - Polysomnography

KW - Latent Dirichlet allocation

U2 - 10.3389/fnins.2019.00598

DO - 10.3389/fnins.2019.00598

M3 - Journal article

VL - 13

JO - Frontiers in Neuroscience

JF - Frontiers in Neuroscience

SN - 1662-4548

M1 - 598

ER -