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Experimentally imposed circadian misalignment alters the neural response to monetary rewards and response inhibition in healthy adolescents

Published online by Cambridge University Press:  17 March 2021

Brant P. Hasler Open the ORCID record for Brant P. Hasler [Opens in a new window] ,
Adriane M. Soehner ,
Meredith L. Wallace ,
Ryan W. Logan ,
Wambui Ngari ,
Erika E. Forbes ,
Daniel J. Buysse  and
Duncan B. Clark
Brant P. Hasler*
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Adriane M. Soehner
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Meredith L. Wallace
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Ryan W. Logan
Affiliation:
Department of Pharmacology and Experimental Therapeutics, Boston University School of Medicine, Boston, MA, USA
Wambui Ngari
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Erika E. Forbes
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Daniel J. Buysse
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
Duncan B. Clark
Affiliation:
Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
*
Author for correspondence: Brant P. Hasler, E-mail: [email protected]
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Abstract

Background

Sleep and circadian timing shifts later during adolescence, conflicting with early school start times, and resulting in circadian misalignment. Although circadian misalignment has been linked to depression, substance use, and altered reward function, a paucity of experimental studies precludes the determination of causality. Here we tested, for the first time, whether experimentally-imposed circadian misalignment alters the neural response to monetary reward and/or response inhibition.

Methods

Healthy adolescents (n = 25, ages 13–17) completed two in-lab sleep schedules in counterbalanced order: An ‘aligned’ condition based on typical summer sleep-wake times (0000–0930) and a ‘misaligned’ condition mimicking earlier school year sleep-wake times (2000–0530). Participants completed morning and afternoon functional magnetic resonance imaging scans during each condition, including monetary reward (morning only) and response inhibition (morning and afternoon) tasks. Total sleep time and circadian phase were assessed via actigraphy and salivary melatonin, respectively.

Results

Bilateral ventral striatal (VS) activation during reward outcome was lower during the Misaligned condition after accounting for the prior night's total sleep time. Bilateral VS activation during reward anticipation was lower during the Misaligned condition, including after accounting for covariates, but did not survive correction for multiple comparisons. Right inferior frontal gyrus activation during response inhibition was lower during the Misaligned condition, before and after accounting for total sleep time and vigilant attention, but only during the morning scan.

Conclusions

Our findings provide novel experimental evidence that circadian misalignment analogous to that resulting from school schedules may have measurable impacts on healthy adolescents' reward processing and inhibition of prepotent responses.

Keywords

Adolescentscircadian rhythmsfMRIrewardimpulse controlsleep
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 16 , December 2022 , pp. 3939 - 3947
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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