Age-Related Differences in Sleep Architecture and Electroencephalogram in Adolescents in the National Consortium on Alcohol and Neurodevelopment in Adolescence Sample

Abstract

Study objectives: To investigate age-related differences in polysomnographic and sleep electroencephalographic (EEG) measures, considering sex, pubertal stage, ethnicity, and scalp topography in a large group of adolescents in the National Consortium on Alcohol and NeuroDevelopment in Adolescence (NCANDA).

Methods: Following an adaptation/clinical screening night, 141 healthy adolescents (12-21 y, 64 girls) had polysomnographic recordings, from which sleep staging and EEG measures were derived. The setting was the SRI International Human Sleep Laboratory and University of Pittsburgh Pediatric Sleep Laboratory.

Results: Older age was associated with a lower percentage of N3 sleep, accompanied by higher percentages of N2, N1, and rapid eye movement (REM) sleep. Older boys compared with younger boys had more frequent awakenings and wakefulness after sleep onset, effects that were absent in girls. Delta (0.3-4 Hz) EEG power in nonrapid eye movement NREM sleep was lower in older than younger adolescents at all electrode sites, with steeper slopes of decline over the occipital scalp. EEG power in higher frequency bands was also lower in older adolescents than younger adolescents, with equal effects across electrodes. Percent delta power in the first NREM period was similar across age. African Americans had lower EEG power across frequency bands (delta to sigma) compared with Caucasians. Finally, replacing age with pubertal status in the models showed similar relationships.

Conclusions: Substantial differences in sleep architecture and EEG were evident across adolescence in this large group, with sex modifying some relationships. Establishment and follow-up of this cohort allows the investigation of sleep EEG-brain structural relationships and the effect of behaviors, such as alcohol and substance use, on sleep EEG maturation.

Keywords: adolescence; alcohol; delta; electroencephalogram; nonrapid eye movement sleep; sex differences; sleep cycles; slow wave activity.

Figure 1

Univariate relationships between age and (A) wakefulness after sleep onset (WASO) and (B) Awakening Index calculated from polysomnographic recordings in 141 adolescent boys (blue triangles, blue regression lines) and girls (red circles, red regression lines). Older age was associated with higher amounts of WASO (R² = 0.07, P = 0.02) and more awakenings (R² = 0.08, P = 0.01) in boys but not in girls.

Figure 2

Relationships between age and percentage time spent in each sleep stage for 77 male (blue triangles) and 64 female (red circles) adolescents. Percentages of N1, N2, and rapid eye movement (REM) sleep were higher in older than in younger adolescents, regardless of sex. There was a significant age*sex interaction effect for %N3 sleep, with the age-related difference in %N3 sleep being greater in boys than in girls.

Figure 3

Univariate relationships between age and Ln delta power during nonrapid eye movement (NREM) sleep at five topographic electrode positions across the scalp (F3, FC3, C3, P3, O1) in 77 male (blue triangles) and 64 female (red circles) adolescents. Older boys and girls had less delta power across all positions compared with younger adolescents, controlling for BMI percentile, sex, ethnicity, site, and exceed alcohol criteria. There was a significant sex*age interaction effect at O1, where the slope of the age-delta power relationship was slightly steeper in boys (see text for details).

Figure 4

Ln delta, theta, and alpha power at C3 in nonrapid eye movement (NREM) sleep (mean ± SEM) according to ethnicity. African American adolescents had significantly lower power in delta, theta, and alpha frequency bands compared with Caucasian adolescents, controlling for age, sex, body mass index (BMI) percentile, exceeded alcohol criteria, and site (see text for details).

Figure 5

Univariate relationship between scores on the pubertal development scale and Ln delta power in nonrapid eye movement (NREM) sleep at C3 in 77 male (blue triangles) and 64 female (red circles) adolescents. More pubertally advanced adolescents had less delta power than less pubertally advanced adolescents.

Figure 6

(A) Average delta power ± standard deviation plotted across the first four nonrapid eye movement (NREM) periods of the night in 139 adolescents, showing the decline in delta power across the night. Regression analysis with age showed that delta power was lower in older adolescents at each NREM period compared with younger adolescents, but the decline in delta power was similar across the NREM sleep periods regardless of age. (B) Delta power in NREM1 as a percentage of all-night NREM delta power plotted against age, showing no age-related difference in the percentage of delta power in the first NREM period.