Evidence of a maturational disruption in non-rapid eye movement sleep slow wave activity in youth with attention-deficit/hyperactivity, learning and internalizing disorders

Background: Sleep slow wave activity (SWA) peaks during childhood and declines in the transition to adolescence during typical development (TD). It remains unknown whether this trajectory differs in youth with neuropsychiatric disorders. Methods: We analyzed sleep EEGs of 664 subjects 6 to 21 y (449 TD, 123 unmedicated, 92 medicated) and 114 subjects 7-12 y (median 10.5 y) followed-up at 18-22 y (median 19 y). SWA (0.4-4 Hz) power was calculated during non-rapid eye movement sleep. Results: TD and unmedicated youth showed cubic central and frontal SWA trajectories from 6 to 21 y (p-cubic<0.05), with TD youth showing peaks in central SWA at 6.8 y and frontal at 8.2 y. Unmedicated attention-deficit/hyperactivity (ADHD) and/or learning disorders (LD) showed peak central SWA 2 y later (at 9.6 y, coinciding with peak frontal SWA) than TD, followed by a 67% steeper slope by 19 y. Frontal SWA peak and slope in unmedicated ADHD/LD, and that of central and frontal in internalizing disorders (ID), were similar to TD. Unmedicated ADHD/LD did not differ in the longitudinal SWA percent change by 18-22 y; unmedicated ID showed a lower longitudinal change in frontal SWA than TD. Medicated youth showed a linear decline in central and frontal SWA from 6 to 21 y (p-linear<0.05). Conclusions: ADHD/LD youth show a maturational delay and potential topographical disruption in SWA during childhood and steeper decline throughout adolescence, suggesting faster synaptic pruning. Youth with ID experience less changes in frontal SWA by late adolescence. Psychotropic medications may impact the maturational trajectory of SWA, but not the magnitude of developmental decline by late adolescence. (C) 2022 Elsevier B.V. All rights reserved.