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Event-related potentials in insomnia reflect altered perception of sleep

Abstract Study Objectives Insomnia is defined by the subjective complaint of poor sleep as well as daytime impairments. Since polysomnography (PSG) typically shows only modest sleep impairment, some still unidentified property of sleep, not mirrored in PSG, may be modified in insomnia. One possible...

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Published in:Sleep (New York, N.Y.) N.Y.), 2021-10, Vol.44 (10), p.1
Main Authors: Feige, Bernd, Baglioni, Chiara, Boehm, Philipp, Heinrich, Anna, Trumm, Samuel, Benz, Fee, Nissen, Christoph, Domschke, Katharina, Frase, Lukas, Riemann, Dieter
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container_issue 10
container_start_page 1
container_title Sleep (New York, N.Y.)
container_volume 44
creator Feige, Bernd
Baglioni, Chiara
Boehm, Philipp
Heinrich, Anna
Trumm, Samuel
Benz, Fee
Nissen, Christoph
Domschke, Katharina
Frase, Lukas
Riemann, Dieter
description Abstract Study Objectives Insomnia is defined by the subjective complaint of poor sleep as well as daytime impairments. Since polysomnography (PSG) typically shows only modest sleep impairment, some still unidentified property of sleep, not mirrored in PSG, may be modified in insomnia. One possible mechanistic hypothesis is that insomnia patients may be more sensitive to inevitably occurring internal or external stimuli during the night, causing brief sleep disruptions then perceived as wake time. Methods Auditory event-related potentials (ERP) to low intensity (50 dB SPL) synthesized guitar tones played continuously throughout two nights of polysomnographically registered sleep were obtained in fifty patients with insomnia disorder (ID, without comorbidities) and 50 age- and sex-matched good sleeper controls (GSC) for each sleep stage and NREM/REM cycle. Phasic and tonic REM were treated as separate stages. Latencies and amplitudes of components P1, N1 and P2 were measured and analyzed by multivariate repeated-measures ANCOVA including effects of group, night, cycle, and age. Results ID showed reduced P2 amplitudes relative to GSC specifically in phasic REM sleep. The same reduction also correlated with the amount of sleep misperception across groups. Independent component analysis showed a frontal negativity to contribute most to this group difference. Conclusions The present finding can be interpreted as increased mismatch negativity (MMN) in ID, reflecting automated detection of change in the auditory system and a concomitant orienting response. Specifically phasic REM sleep appears to be vulnerable to sensory afferences in ID patients, possibly contributing to the perception of being awake. Clinical Trial Information Short name “PERSLEEP 2,” URL https://www.drks.de/drks_web/navigate.do?navigationId=trial.HTML&TRIAL_ID=DRKS00008965, Registration DRKS00008965.
doi_str_mv 10.1093/sleep/zsab137
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Since polysomnography (PSG) typically shows only modest sleep impairment, some still unidentified property of sleep, not mirrored in PSG, may be modified in insomnia. One possible mechanistic hypothesis is that insomnia patients may be more sensitive to inevitably occurring internal or external stimuli during the night, causing brief sleep disruptions then perceived as wake time. Methods Auditory event-related potentials (ERP) to low intensity (50 dB SPL) synthesized guitar tones played continuously throughout two nights of polysomnographically registered sleep were obtained in fifty patients with insomnia disorder (ID, without comorbidities) and 50 age- and sex-matched good sleeper controls (GSC) for each sleep stage and NREM/REM cycle. Phasic and tonic REM were treated as separate stages. Latencies and amplitudes of components P1, N1 and P2 were measured and analyzed by multivariate repeated-measures ANCOVA including effects of group, night, cycle, and age. Results ID showed reduced P2 amplitudes relative to GSC specifically in phasic REM sleep. The same reduction also correlated with the amount of sleep misperception across groups. Independent component analysis showed a frontal negativity to contribute most to this group difference. Conclusions The present finding can be interpreted as increased mismatch negativity (MMN) in ID, reflecting automated detection of change in the auditory system and a concomitant orienting response. Specifically phasic REM sleep appears to be vulnerable to sensory afferences in ID patients, possibly contributing to the perception of being awake. Clinical Trial Information Short name “PERSLEEP 2,” URL https://www.drks.de/drks_web/navigate.do?navigationId=trial.HTML&amp;TRIAL_ID=DRKS00008965, Registration DRKS00008965.</description><identifier>ISSN: 0161-8105</identifier><identifier>EISSN: 1550-9109</identifier><identifier>DOI: 10.1093/sleep/zsab137</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Analysis ; Enterprise resource planning ; Insomnia ; REM sleep ; Sleep</subject><ispartof>Sleep (New York, N.Y.), 2021-10, Vol.44 (10), p.1</ispartof><rights>The Author(s) 2021. Published by Oxford University Press on behalf of Sleep Research Society. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com 2021</rights><rights>COPYRIGHT 2021 Oxford University Press</rights><rights>Sleep Research Society 2021. Published by Oxford University Press on behalf of the Sleep Research Society. All rights reserved. For permissions, please email: journals.permissions@oup.com</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c557t-d1285c2b11a9156c55b6cd7f516e63154347f0ccccb9300f138abb8190cf0ab83</citedby><cites>FETCH-LOGICAL-c557t-d1285c2b11a9156c55b6cd7f516e63154347f0ccccb9300f138abb8190cf0ab83</cites><orcidid>0000-0002-8394-9179 ; 0000-0002-9436-1258 ; 0000-0002-0841-3630</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27923,27924</link.rule.ids></links><search><creatorcontrib>Feige, Bernd</creatorcontrib><creatorcontrib>Baglioni, Chiara</creatorcontrib><creatorcontrib>Boehm, Philipp</creatorcontrib><creatorcontrib>Heinrich, Anna</creatorcontrib><creatorcontrib>Trumm, Samuel</creatorcontrib><creatorcontrib>Benz, Fee</creatorcontrib><creatorcontrib>Nissen, Christoph</creatorcontrib><creatorcontrib>Domschke, Katharina</creatorcontrib><creatorcontrib>Frase, Lukas</creatorcontrib><creatorcontrib>Riemann, Dieter</creatorcontrib><title>Event-related potentials in insomnia reflect altered perception of sleep</title><title>Sleep (New York, N.Y.)</title><description>Abstract Study Objectives Insomnia is defined by the subjective complaint of poor sleep as well as daytime impairments. Since polysomnography (PSG) typically shows only modest sleep impairment, some still unidentified property of sleep, not mirrored in PSG, may be modified in insomnia. One possible mechanistic hypothesis is that insomnia patients may be more sensitive to inevitably occurring internal or external stimuli during the night, causing brief sleep disruptions then perceived as wake time. Methods Auditory event-related potentials (ERP) to low intensity (50 dB SPL) synthesized guitar tones played continuously throughout two nights of polysomnographically registered sleep were obtained in fifty patients with insomnia disorder (ID, without comorbidities) and 50 age- and sex-matched good sleeper controls (GSC) for each sleep stage and NREM/REM cycle. Phasic and tonic REM were treated as separate stages. Latencies and amplitudes of components P1, N1 and P2 were measured and analyzed by multivariate repeated-measures ANCOVA including effects of group, night, cycle, and age. 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Since polysomnography (PSG) typically shows only modest sleep impairment, some still unidentified property of sleep, not mirrored in PSG, may be modified in insomnia. One possible mechanistic hypothesis is that insomnia patients may be more sensitive to inevitably occurring internal or external stimuli during the night, causing brief sleep disruptions then perceived as wake time. Methods Auditory event-related potentials (ERP) to low intensity (50 dB SPL) synthesized guitar tones played continuously throughout two nights of polysomnographically registered sleep were obtained in fifty patients with insomnia disorder (ID, without comorbidities) and 50 age- and sex-matched good sleeper controls (GSC) for each sleep stage and NREM/REM cycle. Phasic and tonic REM were treated as separate stages. Latencies and amplitudes of components P1, N1 and P2 were measured and analyzed by multivariate repeated-measures ANCOVA including effects of group, night, cycle, and age. Results ID showed reduced P2 amplitudes relative to GSC specifically in phasic REM sleep. The same reduction also correlated with the amount of sleep misperception across groups. Independent component analysis showed a frontal negativity to contribute most to this group difference. Conclusions The present finding can be interpreted as increased mismatch negativity (MMN) in ID, reflecting automated detection of change in the auditory system and a concomitant orienting response. Specifically phasic REM sleep appears to be vulnerable to sensory afferences in ID patients, possibly contributing to the perception of being awake. 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subjects Analysis
Enterprise resource planning
Insomnia
REM sleep
Sleep
title Event-related potentials in insomnia reflect altered perception of sleep
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