The increase in longitudinally measured sleepiness across adolescence is related to the maturational decline in low-frequency EEG power

Abstract

Objectives: A changing sleep schedule that reduces sleep duration is thought to produce the increasing daytime sleepiness of adolescents. We tested the hypothesis that adolescent daytime sleepiness also results from adolescent brain maturational processes indexed by declining delta electroencephalographic (EEG) activity.

Design: Data are from the first 3 years of a semilongitudinal study of EEG changes in adolescence. All-night EEG was recorded semiannually.

Setting: EEG was recorded with ambulatory recorders in the subjects' homes.

Participants: Thirty-one subjects were 9 years old (cohort C9), and 38 subjects were 12 years old (cohort C12) at the start of the study.

Measurements: EEG power density (power/minute) was calculated for the first 5 hours of non-rapid eye movement sleep. Subjects rated sleepiness on a modified Epworth Sleepiness Scale. Habitual sleep schedules were assessed with self-reports and actigraphy.

Results: In C9 subjects, sleepiness increased slightly and was related only to age. In C12 subjects, the increase in subjective sleepiness was related to changes in age, bedtime, time in bed, and a wide frequency range of EEG power density. Sleepiness was not related to rise time, non-rapid eye movement sleep duration, rapid eye movement sleep duration, or total sleep time. With sleep schedule measures statistically controlled, the increase in sleepiness in the C12 group was strongly related to declining delta power density and, unexpectedly, even more strongly related to declining theta power density.

Conclusions: The data support our hypothesis that, independent of sleep schedule changes, increasing adolescent daytime sleepiness is related to brain maturational changes indexed by declining EEG power. Our working hypothesis is that the declines in delta and theta power are correlates of an adolescent synaptic pruning that reduces waking arousal levels.

Figure 1

Mean (± SEM) subjective daytime sleepiness rating plotted against subject age at each of 6 recordings for the C9 cohort (●) and the C12 cohort (▲). After an initial dip, sleepiness increased significantly with age in cohort C12. The increase with age in the C9 cohort was due to a large increase from the fourth to fifth recording.

Figure 2

Mean (± SEM) self-reported and actigraphy determined sleep-schedule measurements are plotted against age with format similar to Figure 1. With bedtime becoming later with age and rise time changing little, time in bed declined significantly with age in both the C9 and C12 cohorts.

Figure 3

Mean (± SEM) sleep durations are plotted against age with format as in Figure 1. Total sleep time declined significantly with age in both cohorts. Non-rapid eye movement sleep duration declined significantly in C12 but did not in C9. Despite a large increase in rapid eye movement duration at the sixth recording in C12, rapid eye movement sleep duration declined with age in both cohorts.

Figure 4

Mean (± SEM) electroencephalogram (EEG) power density in (A) 1- to 4-Hz and (B) 4- to 8-Hz frequency band is plotted against age with same format as in Figure 1. Delta (1–4 Hz) power density declined linearly across the 6 recordings in cohort C12, from age 12 to age 15 years. In cohort C9, the decline in delta power density with age was due to a decrease from the fourth to fifth recording. The 4- to 8-Hz power density declined linearly in both cohorts. (C) All-night total non-rapid eye movement sleep delta power showed the same relationship to age as did the delta power density.