Sex, puberty, and the timing of sleep EEG measured adolescent brain maturation

Abstract

The steep adolescent decline in the slow wave (delta, 1-4 Hz) electroencephalogram (EEG) of nonrapid eye movement (NREM) sleep is a dramatic maturational change in brain electrophysiology thought to be driven by cortical synaptic pruning. A perennial question is whether this change in brain electrophysiology is related to sexual maturation. Applying Gompertz growth models to longitudinal data spanning ages 9-18 y, we found that the timing of the delta decline was significantly (P < 0.0001) linked to timing of pubertal maturation. This timing relation remained significant when sex differences in the timing of the delta decline were statistically controlled. Sex differences and the relation to the timing of puberty jointly explained 67% of the between-subject variance in the timing of the delta decline. These data provide a demonstration of a temporal relation between puberty and an electrophysiological marker of adolescent brain development. They can guide research into whether the neuroendocrine events of puberty are mechanistically linked to cortical maturation or whether, instead, the two maturational processes are parallel but independent programs of human ontogenesis.

Fig. 1.

(A) Delta power at each semiannual recording is plotted against age for each male (faint blue) and each female (faint pink) subject. The delta power decline across adolescence was fit with a Gompertz equation, . The age of steepest decline, M, differed significantly (P < 0.0001) between individual subjects and, on average, occurred earlier in girls (heavy pink) than in boys (heavy blue). (B) Theta power at each semiannual recording is plotted against age using the same format as in Fig. 1A. The age of steepest decline for theta differed significantly (P < 0.0001) between individual subjects, occurred earlier in girls than in boys, and occurred earlier than the age of steepest decline for delta.

Fig. 2.

Tanner_ph stage Gompertz growth curves for each boy (faint blue) and each girl (faint pink) were estimated with nonlinear mixed effect analysis. The age of most rapid increase for each subject was used in subsequent analyses as a marker of the timing of pubertal maturation. The validity of this estimate is demonstrated by the earlier average maturation in girls (heavy pink) than in boys (heavy blue) and by the significant P < 0.0001 relation between the age of most rapid Tanner stage increase and the age of menarche in female subjects (see text).