Associations between brain structure and sleep patterns across adolescent development

Author:

Jalbrzikowski Maria1,Hayes Rebecca A1,Scully Kathleen E1,Franzen Peter L1,Hasler Brant P123ORCID,Siegle Greg J123,Buysse Daniel J13ORCID,Dahl Ronald E4ORCID,Forbes Erika E1235ORCID,Ladouceur Cecile D1,McMakin Dana L6,Ryan Neal D1,Silk Jennifer S2,Goldstein Tina R1,Soehner Adriane M1

Affiliation:

1. Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA

2. Department of Psychology, University of Pittsburgh, Pittsburgh, PA

3. Department of Clinical and Translational Science, University of Pittsburgh School of Medicine, Pittsburgh, PA

4. Department of Public Health, University of California, Berkeley, CA

5. Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, PA

6. Department of Psychology, Florida International University, Miami, FL

Abstract

Abstract Study Objectives Structural brain maturation and sleep are complex processes that exhibit significant changes over adolescence and are linked to many physical and mental health outcomes. We investigated whether sleep–gray matter relationships are developmentally invariant (i.e. stable across age) or developmentally specific (i.e. only present during discrete time windows) from late childhood through young adulthood. Methods We constructed the Neuroimaging and Pediatric Sleep Databank from eight research studies conducted at the University of Pittsburgh (2009–2020). Participants completed a T1-weighted structural MRI scan (sMRI) and 5–7 days of wrist actigraphy to assess naturalistic sleep. The final analytic sample consisted of 225 participants without current psychiatric diagnoses (9–25 years). We extracted cortical thickness and subcortical volumes from sMRI. Sleep patterns (duration, timing, continuity, regularity) were estimated from wrist actigraphy. Using regularized regression, we examined cross-sectional associations between sMRI measures and sleep patterns, as well as the effects of age, sex, and their interaction with sMRI measures on sleep. Results Shorter sleep duration, later sleep timing, and poorer sleep continuity were associated with thinner cortex and altered subcortical volumes in diverse brain regions across adolescence. In a discrete subset of regions (e.g. posterior cingulate), thinner cortex was associated with these sleep patterns from late childhood through early-to-mid adolescence but not in late adolescence and young adulthood. Conclusions In childhood and adolescence, developmentally invariant and developmentally specific associations exist between sleep patterns and gray matter structure, across brain regions linked to sensory, cognitive, and emotional processes. Sleep intervention during specific developmental periods could potentially promote healthier neurodevelopmental outcomes.

Funder

National Center for Advancing Translational Sciences

National Institute of Mental Health

National Institute on Drug Abuse

National Institute on Alcohol Abuse and Alcoholism

Pittsburgh Foundation

Publisher

Oxford University Press (OUP)

Subject

Physiology (medical),Clinical Neurology

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