Sleep electroencephalogram evidence of delayed brain maturation in attention deficit hyperactivity disorder: a longitudinal study

Abstract

Abstract Study Objectives This study investigates whether longitudinally measured changes in adolescent brain electrophysiology corroborate the maturational lag associated with attention deficit hyperactivity disorder (ADHD) reported in magnetic resonance imaging (MRI) studies and cross-sectional sleep electroencephalogram (EEG) data. Methods Semiannually nine adolescents diagnosed with ADHD (combined presentation, DSM-V criteria, mean age 12.39 ± 0.61 years at first time-point, two females) and nine typically developing controls (12.08 ± 0.35 years, four females) underwent all-night laboratory polysomnography, yielding four recordings. Results Sleep macrostructure was similar between groups. A quadratic model of the age change in non-rapid eye movement (NREM) delta (1.07–4 Hz) power, with sex effects accounted for, found that delta power peaked 0.92 ± 0.37 years later in the ADHD group. A Gompertz function fit to the same data showed that the age of most rapid delta power decline occurred 0.93 ± 0.41 years later in the ADHD group (p = 0.037), but this group difference was not significant (p = 0.38) with sex effects accounted for. For very low frequency (0.29–1.07 Hz) EEG, the ADHD lag (1.07 ± 0.42 years later, p = 0.019) was significant for a Gompertz model with sex effects accounted for (p = 0.044). Theta (4–7.91 Hz) showed a trend (p = 0.064) toward higher power in the ADHD group. Analysis of the EEG decline across the night found that standardized delta and theta power in NREMP1 were significantly (p < 0.05 for both) lower in adolescents with ADHD. Conclusions This is the first longitudinal study to reveal electrophysiological evidence of a maturational lag associated with ADHD. In addition, our findings revealed basically unaltered sleep macrostructure but altered sleep homeostasis associated with ADHD.