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Sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study

Sleep restriction has been proposed to cause impaired emotional processing and emotional regulation by inhibiting top-down control from prefrontal cortex to amygdala. Intentional emotional regulation after sleep restriction has, however, never been studied using brain imaging. We aimed here to inves...

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Autores principales: Tamm, Sandra, Nilsonne, Gustav, Schwarz, Johanna, Golkar, Armita, Kecklund, Göran, Petrovic, Predrag, Fischer, Håkan, Åkerstedt, Torbjörn, Lekander, Mats
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6458356/
https://www.ncbi.nlm.nih.gov/pubmed/31032025
http://dx.doi.org/10.1098/rsos.181704
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author Tamm, Sandra
Nilsonne, Gustav
Schwarz, Johanna
Golkar, Armita
Kecklund, Göran
Petrovic, Predrag
Fischer, Håkan
Åkerstedt, Torbjörn
Lekander, Mats
author_facet Tamm, Sandra
Nilsonne, Gustav
Schwarz, Johanna
Golkar, Armita
Kecklund, Göran
Petrovic, Predrag
Fischer, Håkan
Åkerstedt, Torbjörn
Lekander, Mats
author_sort Tamm, Sandra
collection PubMed
description Sleep restriction has been proposed to cause impaired emotional processing and emotional regulation by inhibiting top-down control from prefrontal cortex to amygdala. Intentional emotional regulation after sleep restriction has, however, never been studied using brain imaging. We aimed here to investigate the effect of partial sleep restriction on emotional regulation through cognitive reappraisal. Forty-seven young (age 20–30) and 33 older (age 65–75) participants (38/23 with complete data and successful sleep intervention) performed a cognitive reappraisal task during fMRI after a night of normal sleep and after restricted sleep (3 h). Emotional downregulation was associated with significantly increased activity in the dorsolateral prefrontal cortex (p(FWE) < 0.05) and lateral orbital cortex (p(FWE) < 0.05) in young, but not in older subjects. Sleep restriction was associated with a decrease in self-reported regulation success to negative stimuli (p < 0.01) and a trend towards perceiving all stimuli as less negative (p = 0.07) in young participants. No effects of sleep restriction on brain activity nor connectivity were found in either age group. In conclusion, our data do not support the idea of a prefrontal-amygdala disconnect after sleep restriction, and neural mechanisms underlying behavioural effects on emotional regulation after insufficient sleep require further investigation.
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spelling pubmed-64583562019-04-26 Sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study Tamm, Sandra Nilsonne, Gustav Schwarz, Johanna Golkar, Armita Kecklund, Göran Petrovic, Predrag Fischer, Håkan Åkerstedt, Torbjörn Lekander, Mats R Soc Open Sci Psychology and Cognitive Neuroscience Sleep restriction has been proposed to cause impaired emotional processing and emotional regulation by inhibiting top-down control from prefrontal cortex to amygdala. Intentional emotional regulation after sleep restriction has, however, never been studied using brain imaging. We aimed here to investigate the effect of partial sleep restriction on emotional regulation through cognitive reappraisal. Forty-seven young (age 20–30) and 33 older (age 65–75) participants (38/23 with complete data and successful sleep intervention) performed a cognitive reappraisal task during fMRI after a night of normal sleep and after restricted sleep (3 h). Emotional downregulation was associated with significantly increased activity in the dorsolateral prefrontal cortex (p(FWE) < 0.05) and lateral orbital cortex (p(FWE) < 0.05) in young, but not in older subjects. Sleep restriction was associated with a decrease in self-reported regulation success to negative stimuli (p < 0.01) and a trend towards perceiving all stimuli as less negative (p = 0.07) in young participants. No effects of sleep restriction on brain activity nor connectivity were found in either age group. In conclusion, our data do not support the idea of a prefrontal-amygdala disconnect after sleep restriction, and neural mechanisms underlying behavioural effects on emotional regulation after insufficient sleep require further investigation. The Royal Society 2019-03-27 /pmc/articles/PMC6458356/ /pubmed/31032025 http://dx.doi.org/10.1098/rsos.181704 Text en © 2019 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Psychology and Cognitive Neuroscience
Tamm, Sandra
Nilsonne, Gustav
Schwarz, Johanna
Golkar, Armita
Kecklund, Göran
Petrovic, Predrag
Fischer, Håkan
Åkerstedt, Torbjörn
Lekander, Mats
Sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study
title Sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study
title_full Sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study
title_fullStr Sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study
title_full_unstemmed Sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study
title_short Sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study
title_sort sleep restriction caused impaired emotional regulation without detectable brain activation changes—a functional magnetic resonance imaging study
topic Psychology and Cognitive Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6458356/
https://www.ncbi.nlm.nih.gov/pubmed/31032025
http://dx.doi.org/10.1098/rsos.181704
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