Associations between brain structure and sleep patterns across adolescent development

Abstract

Importance Structural brain maturation and sleep are complex processes that exhibit significant changes over adolescence and are linked to healthy physical and mental development. The precise timing and magnitude of these changes influence function throughout the lifespan. However, the relationships between gray matter structure and sleep patterns during adolescence are not fully understood. A detailed characterization of brain-sleep associations during this sensitive period is crucial for understanding factors contributing to optimal neurodevelopmental trajectories in adolescence. Objective To investigate 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. Setting The Neuroimaging and Pediatric Sleep Databank was constructed from 8 research studies conducted at the University of Pittsburgh between 2009 and 2020. Participants The final sample consisted of 240 participants without current psychiatric diagnoses (9-25 years), and with good quality sleep tracking and structural MRI (sMRI) data. Design Participants completed a sMRI scan and 5-7 days of wrist actigraphy to assess naturalistic sleep. 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. Main Outcome(s) and Measure(s) Using Freesurfer software, we extracted cortical thickness and subcortical volumes from T1-weighted MRI. Sleep patterns (duration, timing, continuity, regularity) were estimated from wrist actigraphy. Results Shorter sleep duration, later sleep timing, and poorer sleep continuity were associated with a stable pattern of 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 and Relevance In childhood and adolescence, developmentally-invariant and developmentally-specific associations exist between sleep patterns and gray matter structure, in a wide array of brain regions linked to many sensory, cognitive, and emotional processes. Sleep intervention during specific developmental periods could potentially promote healthier neurodevelopmental outcomes. KEY POINTS Question Does age modulate associations between gray matter structure and actigraphic sleep patterns across adolescent development? Findings This cross-sectional study reports stable associations between regional gray matter structure and shorter duration, later timing, and poorer continuity of sleep from ages 9 to 25 years-old, as well as developmentally-specific associations that are present only from late childhood to early-to-mid adolescence. Meaning Stronger coupling of gray matter and sleep patterns from late childhood to early-to-mid adolescence potentially implicates this discrete developmental window as a period of vulnerability to adverse sleep-brain interactions. Sleep intervention during this developmental stage may support healthier neurodevelopmental trajectories.