Longitudinal trajectories of non-rapid eye movement delta and theta EEG as indicators of adolescent brain maturation

Abstract

It is now recognized that extensive maturational changes take place in the human brain during adolescence, and that the trajectories of these changes are best studied longitudinally. We report the first longitudinal study of the adolescent decline in non-rapid eye movement (NREM) delta (1-4 Hz) and theta (4-8 Hz) EEG. Delta and theta are the homeostatic frequencies of human sleep. We recorded sleep EEG in 9- and 12-year-old cohorts twice yearly over a 5-year period. Delta power density (PD) was unchanged between age 9 and 11 years and then fell precipitously, decreasing by 66% between age 11 and 16.5 years (P < .000001). The decline in theta PD began significantly earlier than that in delta PD and also was very steep (by 60%) between age 11 and 16.5 years (P < .000001). These data suggest that age 11-16.5 years is a critically important maturational period for the brain processes that underlie homeostatic NREM EEG, a finding not suggested in previous cross-sectional data. We hypothesize that these EEG changes reflect synaptic pruning. Comparing our data with published longitudinal declines in MRI-estimated cortical thickness suggests the theta age curve parallels the earlier maturational thinning in 3-layer cortex, whereas the delta curve tracks the later changes in 5-layer cortex. This comparison also reveals that adolescent declines in NREM delta and theta are substantially larger than decreases in cortical thickness (>60% vs. <20%). The magnitude, interindividual difference, and tight link to age of these EEG changes indicate that they provide excellent noninvasive tools for investigating neurobehavioral correlates of adolescent brain maturation.

Fig. 1.

PD (mean ± SE) of C9 (filled circles) and C12 (triangles) plotted against mean cohort age for each semiannual recording period. Mean delta and theta data from the first recording of a new 6-year-old cohort (C6) are plotted as open circles. (A) In the longitudinal data, NREM delta (1–4 Hz) PD did not change between age 9.3 and 10.9 years but declined steeply to age 16.4 years, after which the decline slowed. A cross-sectional comparison revealed no significant difference in delta PD between age 6 and 9.3 years. (B) In the longitudinal data, NREM theta (4–8 Hz) PD declined significantly between age 9.3 and 10.9 years, then decreased steadily to age 16.4 years, after which the decline slowed. A cross-sectional comparison with C6 showed a significant theta decline between age 6 and 9 years. The data indicate that delta PD remained at a plateau level until it began to decline between age 11 and 12 years. In contrast, theta PD declined from early childhood. Both delta and theta PD dropped by >60% between age 10.9 and 16.4 years. Both curves show highly significant curvature (see text). PD values were virtually identical in the 2 cohorts where they overlapped in age.

Fig. 2.

NREM EEG PD in delta (Top) and theta (Bottom) for each of the 59 subjects in C9 and C12, plotted against age at each recording (gray lines). Black lines represent the cubic (Left) and Gompertz (Right) curves fit to the longitudinal data. Both functions show an earlier decline for theta compared with delta. The cubic function for theta peaks at a younger age. Also, the age of peak rate of decline estimated by the Gompertz function is significantly younger for theta. Mixed effects analysis shows that the individual differences in starting level and slope are highly significant for both delta and theta. In addition, higher initial values are correlated with steeper slopes.