Restless REM Sleep Impedes Overnight Amygdala Adaptation

Rick Wassing; Oti Lakbila-Kamal; Jennifer R. Ramautar; Diederick Stoffers; F. Schalkwijk; Eus J.W. Van Someren

doi:10.1016/j.cub.2019.06.034

Restless REM Sleep Impedes Overnight Amygdala Adaptation

Rick Wassing, Oti Lakbila-Kamal, Jennifer R. Ramautar, Diederick Stoffers, F. Schalkwijk, Eus J.W. Van Someren^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

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Abstract

Animal studies show that insufficient silencing of the locus coeruleus (LC) during REM sleep impairs sleep-related brain plasticity. Restless REM sleep, a characteristic of several psychiatric disorders, likely reflects insufficient LC silencing. We investigated whether endogenous REM sleep interruptions interfere with overnight reorganization of limbic circuits in human volunteers with a wide range of insomnia severity, from no insomnia complaints to fulfilling community-sample criteria for insomnia disorder. We induced a self-conscious emotion during two functional MRI sessions and recorded sleep EEG in between. Amygdala reactivity decreased overnight in proportion to the total duration of consolidated REM sleep. Restless REM sleep, in contrast, impeded overnight amygdala adaptation. Using targeted memory reactivation with odors tagged to the self-conscious emotional stimulus, we could experimentally enhance both the favorable effect of consolidated REM sleep and the unfavorable effect of restless REM sleep. The findings reveal a maladaptive type of sleep, providing a target for interventions in mental disorders characterized by restless REM sleep.

Original language	English
Pages (from-to)	2351-2358.e4
Number of pages	13
Journal	Current Biology
Volume	29
Issue number	14
Early online date	11 Jul 2019
DOIs	https://doi.org/10.1016/j.cub.2019.06.034
Publication status	Published - 22 Jul 2019

Funding

The authors would like to thank all the volunteers involved in this study, as well as the undergraduate students that helped with the acquisition of the data: C. Dekker, V. Hohn, M. Korpelshoek, K. Müller, L. Nijboer, C. Oosterwijk, S. Riemsma, M. Spaander, G. Thijsma, and N. Veerman. This work was supported by ZONMW Neuropsychoanalysis Fund grant 16.561.0001 of the Netherlands Organization of Scientific Research (NWO), by grant 253/2012 of the Bial Foundation , and by the European Research Council grants ERC-2014-AdG-671084 INSOMNIA and ERC-2016-PoC-737634 INSOMNIA BEAT IT .

Funders	Funder number
Horizon 2020 Framework Programme	671084, 737634
European Research Council
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	253/2012
Fundação Bial

Keywords

amygdala
memory reactivation
REM sleep fragmentation
self-conscious emotions
spindles
transition to REM sleep

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Restless REM Sleep Impedes Overnight Amygdala AdaptationFinal published version, 1.77 MBLicence: Article 25fa Dutch Copyright Act

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title = "Restless REM Sleep Impedes Overnight Amygdala Adaptation",

abstract = "Animal studies show that insufficient silencing of the locus coeruleus (LC) during REM sleep impairs sleep-related brain plasticity. Restless REM sleep, a characteristic of several psychiatric disorders, likely reflects insufficient LC silencing. We investigated whether endogenous REM sleep interruptions interfere with overnight reorganization of limbic circuits in human volunteers with a wide range of insomnia severity, from no insomnia complaints to fulfilling community-sample criteria for insomnia disorder. We induced a self-conscious emotion during two functional MRI sessions and recorded sleep EEG in between. Amygdala reactivity decreased overnight in proportion to the total duration of consolidated REM sleep. Restless REM sleep, in contrast, impeded overnight amygdala adaptation. Using targeted memory reactivation with odors tagged to the self-conscious emotional stimulus, we could experimentally enhance both the favorable effect of consolidated REM sleep and the unfavorable effect of restless REM sleep. The findings reveal a maladaptive type of sleep, providing a target for interventions in mental disorders characterized by restless REM sleep.",

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AU - Van Someren, Eus J.W.

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N2 - Animal studies show that insufficient silencing of the locus coeruleus (LC) during REM sleep impairs sleep-related brain plasticity. Restless REM sleep, a characteristic of several psychiatric disorders, likely reflects insufficient LC silencing. We investigated whether endogenous REM sleep interruptions interfere with overnight reorganization of limbic circuits in human volunteers with a wide range of insomnia severity, from no insomnia complaints to fulfilling community-sample criteria for insomnia disorder. We induced a self-conscious emotion during two functional MRI sessions and recorded sleep EEG in between. Amygdala reactivity decreased overnight in proportion to the total duration of consolidated REM sleep. Restless REM sleep, in contrast, impeded overnight amygdala adaptation. Using targeted memory reactivation with odors tagged to the self-conscious emotional stimulus, we could experimentally enhance both the favorable effect of consolidated REM sleep and the unfavorable effect of restless REM sleep. The findings reveal a maladaptive type of sleep, providing a target for interventions in mental disorders characterized by restless REM sleep.

AB - Animal studies show that insufficient silencing of the locus coeruleus (LC) during REM sleep impairs sleep-related brain plasticity. Restless REM sleep, a characteristic of several psychiatric disorders, likely reflects insufficient LC silencing. We investigated whether endogenous REM sleep interruptions interfere with overnight reorganization of limbic circuits in human volunteers with a wide range of insomnia severity, from no insomnia complaints to fulfilling community-sample criteria for insomnia disorder. We induced a self-conscious emotion during two functional MRI sessions and recorded sleep EEG in between. Amygdala reactivity decreased overnight in proportion to the total duration of consolidated REM sleep. Restless REM sleep, in contrast, impeded overnight amygdala adaptation. Using targeted memory reactivation with odors tagged to the self-conscious emotional stimulus, we could experimentally enhance both the favorable effect of consolidated REM sleep and the unfavorable effect of restless REM sleep. The findings reveal a maladaptive type of sleep, providing a target for interventions in mental disorders characterized by restless REM sleep.

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Restless REM Sleep Impedes Overnight Amygdala Adaptation

Abstract

Funding

Keywords

UN SDGs

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