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Effects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth

INTRODUCTION: Adequate sleep is essential for cognitive and emotion-related functioning, and 9 to 12 hr of sleep is recommended for children ages 6 to 12 years and 8 to 10 hr for children ages 13 to 18 years. However, national survey data indicate that older youth sleep for fewer hours and fall asle...

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Autores principales: Hehr, Aneesh, Marusak, Hilary A., Huntley, Edward D., Rabinak, Christine A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: SAGE Publications 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6739076/
https://www.ncbi.nlm.nih.gov/pubmed/31511841
http://dx.doi.org/10.1177/2470547019856332
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author Hehr, Aneesh
Marusak, Hilary A.
Huntley, Edward D.
Rabinak, Christine A.
author_facet Hehr, Aneesh
Marusak, Hilary A.
Huntley, Edward D.
Rabinak, Christine A.
author_sort Hehr, Aneesh
collection PubMed
description INTRODUCTION: Adequate sleep is essential for cognitive and emotion-related functioning, and 9 to 12 hr of sleep is recommended for children ages 6 to 12 years and 8 to 10 hr for children ages 13 to 18 years. However, national survey data indicate that older youth sleep for fewer hours and fall asleep later than younger youth. This shift in sleep duration and timing corresponds with a sharp increase in onset of emotion-related problems (e.g., anxiety, depression) during adolescence. Given that both sleep duration and timing have been linked to emotion-related outcomes, the present study tests the effects of sleep duration and timing, and their interaction, on resting-state functional connectivity (RS-FC) of corticolimbic emotion-related neural circuitry in children and adolescents. METHODS: A total of 63 children and adolescents (6–17 years, 34 females) completed a weekend overnight sleep journal and a 10-min resting-state functional magnetic resonance imaging scan the next day (Sunday). Whole-brain RS-FC of the amygdala was computed, and the effects of sleep duration, timing (i.e., midpoint of sleep), and their interaction were explored using regression analyses. RESULTS: Overall, we found that older youth tended to sleep later and for fewer hours than younger youth. Controlling for age, shorter sleep duration was associated with lower RS-FC between the amygdala and regions implicated in emotion regulation, including ventral anterior cingulate cortex, precentral gyrus, and superior temporal gyrus. Interestingly, midpoint of sleep was associated with altered connectivity in a distinct set of brain regions involved in interoception and sensory processing, including insula, supramarginal gyrus, and postcentral gyrus. Our data also indicate widespread interactive effects of sleep duration and midpoint on brain regions implicated in emotion regulation, sensory processing, and motor control. CONCLUSION: These results suggest that both sleep duration and midpoint of sleep are associated with next-day RS-FC within corticolimbic emotion-related neural circuitry in children and adolescents. The observed interactive effects of sleep duration and timing on RS-FC may reflect how homeostatic and circadian process interact in the brain and explain the complex patterns observed with respect to emotional health when considering sleep duration and timing. Sleep-related changes in corticolimbic circuitry may contribute to the onset of emotion-related problems during adolescence.
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spelling pubmed-67390762019-09-11 Effects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth Hehr, Aneesh Marusak, Hilary A. Huntley, Edward D. Rabinak, Christine A. Chronic Stress (Thousand Oaks) Original Article INTRODUCTION: Adequate sleep is essential for cognitive and emotion-related functioning, and 9 to 12 hr of sleep is recommended for children ages 6 to 12 years and 8 to 10 hr for children ages 13 to 18 years. However, national survey data indicate that older youth sleep for fewer hours and fall asleep later than younger youth. This shift in sleep duration and timing corresponds with a sharp increase in onset of emotion-related problems (e.g., anxiety, depression) during adolescence. Given that both sleep duration and timing have been linked to emotion-related outcomes, the present study tests the effects of sleep duration and timing, and their interaction, on resting-state functional connectivity (RS-FC) of corticolimbic emotion-related neural circuitry in children and adolescents. METHODS: A total of 63 children and adolescents (6–17 years, 34 females) completed a weekend overnight sleep journal and a 10-min resting-state functional magnetic resonance imaging scan the next day (Sunday). Whole-brain RS-FC of the amygdala was computed, and the effects of sleep duration, timing (i.e., midpoint of sleep), and their interaction were explored using regression analyses. RESULTS: Overall, we found that older youth tended to sleep later and for fewer hours than younger youth. Controlling for age, shorter sleep duration was associated with lower RS-FC between the amygdala and regions implicated in emotion regulation, including ventral anterior cingulate cortex, precentral gyrus, and superior temporal gyrus. Interestingly, midpoint of sleep was associated with altered connectivity in a distinct set of brain regions involved in interoception and sensory processing, including insula, supramarginal gyrus, and postcentral gyrus. Our data also indicate widespread interactive effects of sleep duration and midpoint on brain regions implicated in emotion regulation, sensory processing, and motor control. CONCLUSION: These results suggest that both sleep duration and midpoint of sleep are associated with next-day RS-FC within corticolimbic emotion-related neural circuitry in children and adolescents. The observed interactive effects of sleep duration and timing on RS-FC may reflect how homeostatic and circadian process interact in the brain and explain the complex patterns observed with respect to emotional health when considering sleep duration and timing. Sleep-related changes in corticolimbic circuitry may contribute to the onset of emotion-related problems during adolescence. SAGE Publications 2019-06-19 /pmc/articles/PMC6739076/ /pubmed/31511841 http://dx.doi.org/10.1177/2470547019856332 Text en © The Author(s) 2019 http://creativecommons.org/licenses/by-nc/4.0/ Creative Commons Non Commercial CC BY-NC: This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
spellingShingle Original Article
Hehr, Aneesh
Marusak, Hilary A.
Huntley, Edward D.
Rabinak, Christine A.
Effects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth
title Effects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth
title_full Effects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth
title_fullStr Effects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth
title_full_unstemmed Effects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth
title_short Effects of Duration and Midpoint of Sleep on Corticolimbic Circuitry in Youth
title_sort effects of duration and midpoint of sleep on corticolimbic circuitry in youth
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6739076/
https://www.ncbi.nlm.nih.gov/pubmed/31511841
http://dx.doi.org/10.1177/2470547019856332
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