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 - 2019/7/9
Y1 - 2019/7/9
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 - data-driven analysis
KW - indiscrete labeling of sleep
KW - insomnia
KW - latent Dirichlet allocation
KW - polysomnography
KW - topic modeling
KW - vigilance states
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UR - https://www.ncbi.nlm.nih.gov/pubmed/31338014
U2 - https://doi.org/10.3389/fnins.2019.00598
DO - https://doi.org/10.3389/fnins.2019.00598
M3 - Article
C2 - 31338014
SN - 1662-4548
VL - 13
SP - 1
EP - 12
JO - Frontiers in neuroscience
JF - Frontiers in neuroscience
IS - JULY
M1 - 598
ER -