Increased Aperiodic Neural Activity During Sleep in Major Depressive Disorder

Yevgenia Rosenblum; Leonore Bovy; Frederik D. Weber; Axel Steiger; Marcel Zeising; Martin Dresler

doi:10.1016/j.bpsgos.2022.10.001

Increased Aperiodic Neural Activity During Sleep in Major Depressive Disorder

Yevgenia Rosenblum^*, Leonore Bovy, Frederik D. Weber, Axel Steiger, Marcel Zeising, Martin Dresler

^*Corresponding author for this work

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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Abstract

Background: In major depressive disorder (MDD), patients often express subjective sleep complaints, while polysomnographic studies report only subtle alterations of the electroencephalographic signal. We hypothesize that differentiating the signal into its oscillatory and aperiodic components may bring new insights into our understanding of sleep abnormalities in MDD. Specifically, we investigated aperiodic neural activity during sleep and its relationships with sleep architecture, depression severity, and responsivity to antidepressant treatment. Methods: Polysomnography was recorded in 38 patients with MDD (in unmedicated and 7-day-medicated states) and 38 age-matched healthy control subjects (N = 76). The aperiodic power component was calculated using irregularly resampled auto-spectral analysis. Depression severity was assessed with the Hamilton Depression Rating Scale. We replicated the analysis using 2 independently collected datasets of medicated patients and control subjects (N = 60 and N = 80, respectively). Results: Unmedicated patients showed flatter aperiodic slopes compared with control subjects during non–rapid eye movement (non-REM) stage 2 sleep (p = .009). Medicated patients showed flatter aperiodic slopes compared with their earlier unmedicated state (p values < .001) and control subjects during all sleep stages (p values < .03). In medicated patients, flatter aperiodic slopes during non-REM sleep were linked to the higher proportion of N1, lower proportion of REM, delayed onset of N3 and REM, and shorter total sleep time. Conclusions: Flatter slopes of aperiodic electroencephalographic power may reflect noisier neural activity due to increased excitation-to-inhibition balance, representing a new disease-relevant feature of sleep in MDD.

Original language	English
Pages (from-to)	1021-1029
Journal	Biological Psychiatry Global Open Science
Volume	3
DOIs	https://doi.org/10.1016/j.bpsgos.2022.10.001
Publication status	Published - 2023

Keywords

Antidepressants
Aperiodic power
Excitation-to-inhibition ratio
Impaired sleep
Major depressive disorder
Neural noise

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10.1016/j.bpsgos.2022.10.001

Rosenblum2023Final published version, 657 KBLicence: CC BY

Cite this

@article{73264fb0d2cb41a89cb09b3f68f85830,

title = "Increased Aperiodic Neural Activity During Sleep in Major Depressive Disorder",

abstract = "Background: In major depressive disorder (MDD), patients often express subjective sleep complaints, while polysomnographic studies report only subtle alterations of the electroencephalographic signal. We hypothesize that differentiating the signal into its oscillatory and aperiodic components may bring new insights into our understanding of sleep abnormalities in MDD. Specifically, we investigated aperiodic neural activity during sleep and its relationships with sleep architecture, depression severity, and responsivity to antidepressant treatment. Methods: Polysomnography was recorded in 38 patients with MDD (in unmedicated and 7-day-medicated states) and 38 age-matched healthy control subjects (N = 76). The aperiodic power component was calculated using irregularly resampled auto-spectral analysis. Depression severity was assessed with the Hamilton Depression Rating Scale. We replicated the analysis using 2 independently collected datasets of medicated patients and control subjects (N = 60 and N = 80, respectively). Results: Unmedicated patients showed flatter aperiodic slopes compared with control subjects during non–rapid eye movement (non-REM) stage 2 sleep (p = .009). Medicated patients showed flatter aperiodic slopes compared with their earlier unmedicated state (p values < .001) and control subjects during all sleep stages (p values < .03). In medicated patients, flatter aperiodic slopes during non-REM sleep were linked to the higher proportion of N1, lower proportion of REM, delayed onset of N3 and REM, and shorter total sleep time. Conclusions: Flatter slopes of aperiodic electroencephalographic power may reflect noisier neural activity due to increased excitation-to-inhibition balance, representing a new disease-relevant feature of sleep in MDD.",

keywords = "Antidepressants, Aperiodic power, Excitation-to-inhibition ratio, Impaired sleep, Major depressive disorder, Neural noise",

author = "Yevgenia Rosenblum and Leonore Bovy and Weber, {Frederik D.} and Axel Steiger and Marcel Zeising and Martin Dresler",

note = "Funding Information: MD and MZ designed the study. YR analyzed the data and wrote the manuscript. All authors contributed to, reviewed, and approved the final draft of the paper. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication. We thank all the participants for participating in this study. We thank Sofia Tzioridou for her helpful suggestions. A previous version of this article was published as a preprint on medRxiv: https://doi.org/10.1101/2022.06.03.22275735. The authors report no biomedical financial interests or potential conflicts of interest. Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2023",

doi = "10.1016/j.bpsgos.2022.10.001",

language = "English",

volume = "3",

pages = "1021--1029",

}

TY - JOUR

T1 - Increased Aperiodic Neural Activity During Sleep in Major Depressive Disorder

AU - Rosenblum, Yevgenia

AU - Bovy, Leonore

AU - Weber, Frederik D.

AU - Steiger, Axel

AU - Zeising, Marcel

AU - Dresler, Martin

N1 - Funding Information: MD and MZ designed the study. YR analyzed the data and wrote the manuscript. All authors contributed to, reviewed, and approved the final draft of the paper. All authors had full access to all the data in the study and had final responsibility for the decision to submit for publication. We thank all the participants for participating in this study. We thank Sofia Tzioridou for her helpful suggestions. A previous version of this article was published as a preprint on medRxiv: https://doi.org/10.1101/2022.06.03.22275735. The authors report no biomedical financial interests or potential conflicts of interest. Publisher Copyright: © 2022 The Authors

PY - 2023

Y1 - 2023

N2 - Background: In major depressive disorder (MDD), patients often express subjective sleep complaints, while polysomnographic studies report only subtle alterations of the electroencephalographic signal. We hypothesize that differentiating the signal into its oscillatory and aperiodic components may bring new insights into our understanding of sleep abnormalities in MDD. Specifically, we investigated aperiodic neural activity during sleep and its relationships with sleep architecture, depression severity, and responsivity to antidepressant treatment. Methods: Polysomnography was recorded in 38 patients with MDD (in unmedicated and 7-day-medicated states) and 38 age-matched healthy control subjects (N = 76). The aperiodic power component was calculated using irregularly resampled auto-spectral analysis. Depression severity was assessed with the Hamilton Depression Rating Scale. We replicated the analysis using 2 independently collected datasets of medicated patients and control subjects (N = 60 and N = 80, respectively). Results: Unmedicated patients showed flatter aperiodic slopes compared with control subjects during non–rapid eye movement (non-REM) stage 2 sleep (p = .009). Medicated patients showed flatter aperiodic slopes compared with their earlier unmedicated state (p values < .001) and control subjects during all sleep stages (p values < .03). In medicated patients, flatter aperiodic slopes during non-REM sleep were linked to the higher proportion of N1, lower proportion of REM, delayed onset of N3 and REM, and shorter total sleep time. Conclusions: Flatter slopes of aperiodic electroencephalographic power may reflect noisier neural activity due to increased excitation-to-inhibition balance, representing a new disease-relevant feature of sleep in MDD.

AB - Background: In major depressive disorder (MDD), patients often express subjective sleep complaints, while polysomnographic studies report only subtle alterations of the electroencephalographic signal. We hypothesize that differentiating the signal into its oscillatory and aperiodic components may bring new insights into our understanding of sleep abnormalities in MDD. Specifically, we investigated aperiodic neural activity during sleep and its relationships with sleep architecture, depression severity, and responsivity to antidepressant treatment. Methods: Polysomnography was recorded in 38 patients with MDD (in unmedicated and 7-day-medicated states) and 38 age-matched healthy control subjects (N = 76). The aperiodic power component was calculated using irregularly resampled auto-spectral analysis. Depression severity was assessed with the Hamilton Depression Rating Scale. We replicated the analysis using 2 independently collected datasets of medicated patients and control subjects (N = 60 and N = 80, respectively). Results: Unmedicated patients showed flatter aperiodic slopes compared with control subjects during non–rapid eye movement (non-REM) stage 2 sleep (p = .009). Medicated patients showed flatter aperiodic slopes compared with their earlier unmedicated state (p values < .001) and control subjects during all sleep stages (p values < .03). In medicated patients, flatter aperiodic slopes during non-REM sleep were linked to the higher proportion of N1, lower proportion of REM, delayed onset of N3 and REM, and shorter total sleep time. Conclusions: Flatter slopes of aperiodic electroencephalographic power may reflect noisier neural activity due to increased excitation-to-inhibition balance, representing a new disease-relevant feature of sleep in MDD.

KW - Antidepressants

KW - Aperiodic power

KW - Excitation-to-inhibition ratio

KW - Impaired sleep

KW - Major depressive disorder

KW - Neural noise

U2 - 10.1016/j.bpsgos.2022.10.001

DO - 10.1016/j.bpsgos.2022.10.001

M3 - Article

AN - SCOPUS:85151889708

VL - 3

SP - 1021

EP - 1029

JO - Biological Psychiatry Global Open Science

JF - Biological Psychiatry Global Open Science

ER -

Increased Aperiodic Neural Activity During Sleep in Major Depressive Disorder

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