Wake EEG oscillation dynamics reflect both sleep pressure and brain maturation across childhood and adolescence.

Abstract

An objective measure of brain maturation is highly insightful for monitoring both typical and atypical development. Slow wave activity, recorded in the sleep electroencephalogram (EEG), reliably indexes age-related changes in sleep pressure as well as deficits related to developmental disorders such as attention-deficit hyperactivity disorder (ADHD). We aimed to determine whether wake EEG measured before and after sleep could index the same developmental changes in sleep pressure, using data collected from 163 participants 3-25 years old. We analyzed age- and sleep-dependent changes in two measures of oscillatory activity, amplitudes and density, as well as two measures of aperiodic activity, offsets and exponents. We then compared these wake measures to sleep slow wave amplitudes and slopes. Finally, we compared wake EEG in children with ADHD (N=58) to neurotypical controls. Of the four wake measures, only oscillation amplitudes consistently exhibited the same changes as sleep slow waves. Wake amplitudes decreased with age, decreased after sleep, and this overnight decrease decreased with age. Furthermore, wake amplitudes were significantly related to both sleep slow wave amplitudes and slopes. Wake oscillation densities decreased overnight in children but increased overnight in adolescents and adults. Aperiodic offsets decreased linearly with age, decreased after sleep, and were significantly related to sleep slow wave amplitudes. Aperiodic exponents also decreased with age, but increased after sleep. No wake measure showed significant effects of ADHD. Overall, our results indicate that wake oscillation amplitudes, and to some extent aperiodic offsets, behave like sleep slow waves across sleep and development. At the same time, overnight changes in oscillation densities independently reflect some yet-unknown shift in neural activity around puberty.