Association of sleep spindle activity with executive functioning and intellectual ability in children and adolescents

Sleep spindles have been studied as an underlying mechanism of cognition. Prior research primarily relied on experimental studies of selective samples of healthy youth. We tested the relationship between spindle activity and cognition in youth from the general population.

Eight hundred and ninety-two sleep electroencephalographies (EEGs) from 9-hour polysomnography were leveraged from 456 typically developing children (median 8 years), and 258 typically developing adolescents (median 16 years) and youth with unmedicated psychiatric/behavioral disorders (89 children; 89 adolescents). Multivariable-adjusted linear regression models examined associations between sleep spindle density (SSD; number/minute) and peak spindle frequency (PSF; 10-16 Hz range) during N2 with Wechsler indices of processing speed, working memory, verbal intelligence, and nonverbal intelligence. We first analyzed typically developing and unmedicated psychiatric/behavioral youth, followed by an analysis of the 47 unmedicated attention deficit/hyperactivity disorder (ADHD) subgroup.

In typically developing children, higher SSD and PSF were associated with better working memory and verbal intelligence. In adolescents, higher SSD was associated with better working memory and nonverbal intelligence, while slower PSF was associated with better nonverbal intelligence. Longitudinally, higher childhood SSD was associated with better adolescent nonverbal intelligence among typically developing youth. In youth with unmedicated psychiatric/behavioral disorders, spindle-cognition associations were lost, except in ADHD, where higher childhood SSD and slower adolescent PSF supported working memory.

Sleep spindles may serve as a biomarker for neural and cognitive maturation, with developmental differences reflecting key brain maturational changes from childhood to adolescence. While altered in unmedicated psychiatric/behavioral disorders, lower-frequency spindles may provide a protective mechanism for working memory in adolescents with ADHD. Statement of Significance Sleep spindles occur as bursts of activity in the sigma-frequency range during non-rapid eye movement sleep. Due to their thalamocortical origin, spindles have been linked to cognitive functioning. We examined spindle activity in typically developing youth and unmedicated youth with psychiatric/behavioral disorders. In typically developing children, higher spindle density was associated with better verbal intelligence and, as they transitioned to adolescence, with better nonverbal intelligence. In unmedicated children with attention deficit/hyperactivity disorder (ADHD), lower-frequency spindles were associated with better working memory in adolescence. Sleep spindles promote neural plasticity for cognitive growth, with reduced impact in later developmental stages reflecting matured neural pathways. In youth with ADHD, sleep spindles may serve a protective role in mitigating cognitive deficits over time.