Slow dissolving of emotional distress contributes to hyperarousal

Rick Wassing; Jeroen S Benjamins; Kim Dekker; Sarah Moens; Kai Spiegelhalder; Bernd Feige; Dieter Riemann; Sophie van der Sluis; Ysbrand D Van Der Werf; Lucia M Talamini; Matthew P Walker; Frans Schalkwijk; Eus J W Van Someren

doi:10.1073/pnas.1522520113

Slow dissolving of emotional distress contributes to hyperarousal

Rick Wassing, Jeroen S Benjamins, Kim Dekker, Sarah Moens, Kai Spiegelhalder, Bernd Feige, Dieter Riemann, Sophie van der Sluis, Ysbrand D Van Der Werf, Lucia M Talamini, Matthew P Walker, Frans Schalkwijk, Eus J W Van Someren

Netherlands Institute for Neuroscience (NIN)

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

125 Citations (Scopus)

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Abstract

The mechanisms underlying hyperarousal, the key symptom of insomnia, have remained elusive, hampering cause-targeted treatment. Recently, restless rapid-eye-movement (REM) sleep emerged as a robust signature of sleep in insomnia. Given the role of REM sleep in emotion regulation, we hypothesized that restless REM sleep could interfere with the overnight resolution of emotional distress, thus contributing to accumulation of arousal. Participants (n = 1,199) completed questionnaires on insomnia severity, hyperarousal, self-conscious emotional distress, and thought-like nocturnal mentation that was validated to be a specific proxy for restless REM sleep (selective fragmentation: R = 0.57, P < 0.001; eye movement density: R = 0.46, P < 0.01) in 32 polysomnographically assessed participants. The experience of distress lasting overnight increased with insomnia severity (β = 0.29, P < 10(-23)), whereas short-lasting distress did not (β = -0.02, P = 0.41). Insomnia severity was associated with hyperarousal (β = 0.47, P < 10(-63)) and with the thought-like nocturnal mentation that is specifically associated with restless REM sleep (β = 0.31, P < 10(-26)). Structural equation modeling showed that 62.4% of the association between these key characteristics of insomnia was mediated specifically by reduced overnight resolution of emotional distress. The model outperformed all alternative mediation pathways. The findings suggest that restless REM sleep reflects a process that interferes with the overnight resolution of distress. Its accumulation may promote the development of chronic hyperarousal, giving clinical relevance to the role of REM sleep in emotion regulation in insomnia, depression, and posttraumatic stress disorder.

Original language	English
Pages (from-to)	2538-43
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	113
Issue number	9
DOIs	https://doi.org/10.1073/pnas.1522520113
Publication status	Published - 01 Mar 2016

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Wassing, R., Benjamins, J. S., Dekker, K., Moens, S., Spiegelhalder, K., Feige, B., Riemann, D., van der Sluis, S., Van Der Werf, Y. D., Talamini, L. M., Walker, M. P., Schalkwijk, F., & Van Someren, E. J. W. (2016). Slow dissolving of emotional distress contributes to hyperarousal. Proceedings of the National Academy of Sciences of the United States of America, 113(9), 2538-43. https://doi.org/10.1073/pnas.1522520113

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title = "Slow dissolving of emotional distress contributes to hyperarousal",

abstract = "The mechanisms underlying hyperarousal, the key symptom of insomnia, have remained elusive, hampering cause-targeted treatment. Recently, restless rapid-eye-movement (REM) sleep emerged as a robust signature of sleep in insomnia. Given the role of REM sleep in emotion regulation, we hypothesized that restless REM sleep could interfere with the overnight resolution of emotional distress, thus contributing to accumulation of arousal. Participants (n = 1,199) completed questionnaires on insomnia severity, hyperarousal, self-conscious emotional distress, and thought-like nocturnal mentation that was validated to be a specific proxy for restless REM sleep (selective fragmentation: R = 0.57, P < 0.001; eye movement density: R = 0.46, P < 0.01) in 32 polysomnographically assessed participants. The experience of distress lasting overnight increased with insomnia severity (β = 0.29, P < 10(-23)), whereas short-lasting distress did not (β = -0.02, P = 0.41). Insomnia severity was associated with hyperarousal (β = 0.47, P < 10(-63)) and with the thought-like nocturnal mentation that is specifically associated with restless REM sleep (β = 0.31, P < 10(-26)). Structural equation modeling showed that 62.4% of the association between these key characteristics of insomnia was mediated specifically by reduced overnight resolution of emotional distress. The model outperformed all alternative mediation pathways. The findings suggest that restless REM sleep reflects a process that interferes with the overnight resolution of distress. Its accumulation may promote the development of chronic hyperarousal, giving clinical relevance to the role of REM sleep in emotion regulation in insomnia, depression, and posttraumatic stress disorder.",

author = "Rick Wassing and Benjamins, {Jeroen S} and Kim Dekker and Sarah Moens and Kai Spiegelhalder and Bernd Feige and Dieter Riemann and {van der Sluis}, Sophie and {Van Der Werf}, {Ysbrand D} and Talamini, {Lucia M} and Walker, {Matthew P} and Frans Schalkwijk and {Van Someren}, {Eus J W}",

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doi = "10.1073/pnas.1522520113",

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Wassing, R, Benjamins, JS, Dekker, K, Moens, S, Spiegelhalder, K, Feige, B, Riemann, D, van der Sluis, S, Van Der Werf, YD, Talamini, LM, Walker, MP, Schalkwijk, F & Van Someren, EJW 2016, 'Slow dissolving of emotional distress contributes to hyperarousal', Proceedings of the National Academy of Sciences of the United States of America, vol. 113, no. 9, pp. 2538-43. https://doi.org/10.1073/pnas.1522520113

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T1 - Slow dissolving of emotional distress contributes to hyperarousal

AU - Wassing, Rick

AU - Benjamins, Jeroen S

AU - Dekker, Kim

AU - Moens, Sarah

AU - Spiegelhalder, Kai

AU - Feige, Bernd

AU - Riemann, Dieter

AU - van der Sluis, Sophie

AU - Van Der Werf, Ysbrand D

AU - Talamini, Lucia M

AU - Walker, Matthew P

AU - Schalkwijk, Frans

AU - Van Someren, Eus J W

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N2 - The mechanisms underlying hyperarousal, the key symptom of insomnia, have remained elusive, hampering cause-targeted treatment. Recently, restless rapid-eye-movement (REM) sleep emerged as a robust signature of sleep in insomnia. Given the role of REM sleep in emotion regulation, we hypothesized that restless REM sleep could interfere with the overnight resolution of emotional distress, thus contributing to accumulation of arousal. Participants (n = 1,199) completed questionnaires on insomnia severity, hyperarousal, self-conscious emotional distress, and thought-like nocturnal mentation that was validated to be a specific proxy for restless REM sleep (selective fragmentation: R = 0.57, P < 0.001; eye movement density: R = 0.46, P < 0.01) in 32 polysomnographically assessed participants. The experience of distress lasting overnight increased with insomnia severity (β = 0.29, P < 10(-23)), whereas short-lasting distress did not (β = -0.02, P = 0.41). Insomnia severity was associated with hyperarousal (β = 0.47, P < 10(-63)) and with the thought-like nocturnal mentation that is specifically associated with restless REM sleep (β = 0.31, P < 10(-26)). Structural equation modeling showed that 62.4% of the association between these key characteristics of insomnia was mediated specifically by reduced overnight resolution of emotional distress. The model outperformed all alternative mediation pathways. The findings suggest that restless REM sleep reflects a process that interferes with the overnight resolution of distress. Its accumulation may promote the development of chronic hyperarousal, giving clinical relevance to the role of REM sleep in emotion regulation in insomnia, depression, and posttraumatic stress disorder.

AB - The mechanisms underlying hyperarousal, the key symptom of insomnia, have remained elusive, hampering cause-targeted treatment. Recently, restless rapid-eye-movement (REM) sleep emerged as a robust signature of sleep in insomnia. Given the role of REM sleep in emotion regulation, we hypothesized that restless REM sleep could interfere with the overnight resolution of emotional distress, thus contributing to accumulation of arousal. Participants (n = 1,199) completed questionnaires on insomnia severity, hyperarousal, self-conscious emotional distress, and thought-like nocturnal mentation that was validated to be a specific proxy for restless REM sleep (selective fragmentation: R = 0.57, P < 0.001; eye movement density: R = 0.46, P < 0.01) in 32 polysomnographically assessed participants. The experience of distress lasting overnight increased with insomnia severity (β = 0.29, P < 10(-23)), whereas short-lasting distress did not (β = -0.02, P = 0.41). Insomnia severity was associated with hyperarousal (β = 0.47, P < 10(-63)) and with the thought-like nocturnal mentation that is specifically associated with restless REM sleep (β = 0.31, P < 10(-26)). Structural equation modeling showed that 62.4% of the association between these key characteristics of insomnia was mediated specifically by reduced overnight resolution of emotional distress. The model outperformed all alternative mediation pathways. The findings suggest that restless REM sleep reflects a process that interferes with the overnight resolution of distress. Its accumulation may promote the development of chronic hyperarousal, giving clinical relevance to the role of REM sleep in emotion regulation in insomnia, depression, and posttraumatic stress disorder.

U2 - 10.1073/pnas.1522520113

DO - 10.1073/pnas.1522520113

M3 - Article

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SN - 0027-8424

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SP - 2538

EP - 2543

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 9

ER -

Slow dissolving of emotional distress contributes to hyperarousal

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