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Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers

BACKGROUND: Robust evidence links sleep and circadian rhythm disturbances to alcohol use and alcohol-related problems, with a growing literature implicating reward-related mechanisms. However, the extant literature has been limited by cross-sectional designs, self-report or behavioral proxies for ci...

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Autores principales: Hasler, Brant P., Graves, Jessica L., Soehner, Adriane M., Wallace, Meredith L., Clark, Duncan B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8888521/
https://www.ncbi.nlm.nih.gov/pubmed/35250449
http://dx.doi.org/10.3389/fnins.2022.803349
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author Hasler, Brant P.
Graves, Jessica L.
Soehner, Adriane M.
Wallace, Meredith L.
Clark, Duncan B.
author_facet Hasler, Brant P.
Graves, Jessica L.
Soehner, Adriane M.
Wallace, Meredith L.
Clark, Duncan B.
author_sort Hasler, Brant P.
collection PubMed
description BACKGROUND: Robust evidence links sleep and circadian rhythm disturbances to alcohol use and alcohol-related problems, with a growing literature implicating reward-related mechanisms. However, the extant literature has been limited by cross-sectional designs, self-report or behavioral proxies for circadian timing, and samples without substantive alcohol use. Here, we employed objective measures of sleep and circadian rhythms, and an intensive prospective design, to assess whether circadian alignment predicts the neural response to reward in a sample of late adolescents reporting regular alcohol use. METHODS: Participants included 31 late adolescents (18–22 y/o; 19 female participants) reporting weekly alcohol use. Participants completed a 14-day protocol including pre- and post-weekend (Thursday and Sunday) circadian phase assessments via the dim light melatonin onset (DLMO), in counterbalanced order. Sleep-wake timing was assessed via actigraphy. Circadian alignment was operationalized as the DLMO-midsleep interval; secondary analyses considered social jet lag based on weekday-weekend differences in midsleep or DLMO. Neural response to reward (anticipation and outcome) was assessed via a monetary reward fMRI task (Friday and Monday scans). Alcohol use was assessed at baseline and via ecological momentary assessment. Mean BOLD signal was extracted from two regions-of-interest (striatum and medial prefrontal cortex, mPFC) for analyses in regression models, accounting for age, sex, racial identity, and scan order. RESULTS: In primary analyses, shorter DLMO-midsleep intervals (i.e., greater misalignment) on Thursday predicted lower striatal and mPFC responses to anticipated reward, but not reward outcome, on Friday. Lower neural (striatum and mPFC) responses to anticipated reward on Friday correlated with more binge-drinking episodes at baseline, but were not associated with alcohol use in the post-scan weekend. In secondary analyses, greater social jet lag (particularly larger weekend delays in midsleep or DLMO) was associated with lower neural responses to reward anticipation on Monday. CONCLUSION: Findings provide preliminary evidence of proximal associations between objectively determined circadian alignment and the neural response to anticipated monetary reward, which is linked in turn to patterns of problematic drinking. Replication in a larger sample and experimental designs will be important next steps to determining the extent to which circadian misalignment influences risk for alcohol involvement via alterations in reward function.
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spelling pubmed-88885212022-03-03 Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers Hasler, Brant P. Graves, Jessica L. Soehner, Adriane M. Wallace, Meredith L. Clark, Duncan B. Front Neurosci Neuroscience BACKGROUND: Robust evidence links sleep and circadian rhythm disturbances to alcohol use and alcohol-related problems, with a growing literature implicating reward-related mechanisms. However, the extant literature has been limited by cross-sectional designs, self-report or behavioral proxies for circadian timing, and samples without substantive alcohol use. Here, we employed objective measures of sleep and circadian rhythms, and an intensive prospective design, to assess whether circadian alignment predicts the neural response to reward in a sample of late adolescents reporting regular alcohol use. METHODS: Participants included 31 late adolescents (18–22 y/o; 19 female participants) reporting weekly alcohol use. Participants completed a 14-day protocol including pre- and post-weekend (Thursday and Sunday) circadian phase assessments via the dim light melatonin onset (DLMO), in counterbalanced order. Sleep-wake timing was assessed via actigraphy. Circadian alignment was operationalized as the DLMO-midsleep interval; secondary analyses considered social jet lag based on weekday-weekend differences in midsleep or DLMO. Neural response to reward (anticipation and outcome) was assessed via a monetary reward fMRI task (Friday and Monday scans). Alcohol use was assessed at baseline and via ecological momentary assessment. Mean BOLD signal was extracted from two regions-of-interest (striatum and medial prefrontal cortex, mPFC) for analyses in regression models, accounting for age, sex, racial identity, and scan order. RESULTS: In primary analyses, shorter DLMO-midsleep intervals (i.e., greater misalignment) on Thursday predicted lower striatal and mPFC responses to anticipated reward, but not reward outcome, on Friday. Lower neural (striatum and mPFC) responses to anticipated reward on Friday correlated with more binge-drinking episodes at baseline, but were not associated with alcohol use in the post-scan weekend. In secondary analyses, greater social jet lag (particularly larger weekend delays in midsleep or DLMO) was associated with lower neural responses to reward anticipation on Monday. CONCLUSION: Findings provide preliminary evidence of proximal associations between objectively determined circadian alignment and the neural response to anticipated monetary reward, which is linked in turn to patterns of problematic drinking. Replication in a larger sample and experimental designs will be important next steps to determining the extent to which circadian misalignment influences risk for alcohol involvement via alterations in reward function. Frontiers Media S.A. 2022-02-16 /pmc/articles/PMC8888521/ /pubmed/35250449 http://dx.doi.org/10.3389/fnins.2022.803349 Text en Copyright © 2022 Hasler, Graves, Soehner, Wallace and Clark. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Hasler, Brant P.
Graves, Jessica L.
Soehner, Adriane M.
Wallace, Meredith L.
Clark, Duncan B.
Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers
title Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers
title_full Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers
title_fullStr Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers
title_full_unstemmed Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers
title_short Preliminary Evidence That Circadian Alignment Predicts Neural Response to Monetary Reward in Late Adolescent Drinkers
title_sort preliminary evidence that circadian alignment predicts neural response to monetary reward in late adolescent drinkers
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8888521/
https://www.ncbi.nlm.nih.gov/pubmed/35250449
http://dx.doi.org/10.3389/fnins.2022.803349
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