The maturational trajectories of NREM and REM sleep durations differ across adolescence on both school-night and extended sleep

Abstract

We recorded sleep electroencephalogram longitudinally across ages 9-18 yr in subjects sleeping at home. Recordings were made twice yearly on 4 consecutive nights: 2 nights with the subjects maintaining their ongoing school-night schedules, and 2 nights with time in bed extended to 12 h. As expected, school-night total sleep time declined with age. This decline was entirely produced by decreasing non-rapid eye movement (NREM) sleep. Rapid eye movement (REM) sleep durations increased slightly but significantly. NREM and REM sleep durations also exhibited different age trajectories when sleep was extended. Both durations exceeded those on school-night schedules. However, the elevated NREM duration did not change with age, whereas REM durations increased significantly. We interpret the adolescent decline in school-night NREM duration in relation to our hypothesis that NREM sleep reverses changes produced in plastic brain systems during waking. The "substrate" produced during waking declines across adolescence, because synaptic elimination decreases the intensity (metabolic rate) of waking brain activity. Declining substrate reduces both NREM intensity (i.e., delta power) and NREM duration. The absence of a decline in REM sleep duration on school-night sleep and its age-dependent increase in extended sleep pose new challenges to understanding its physiological role. Whatever their ultimate explanation, these robust findings demonstrate that the two physiological states of human sleep respond differently to the maturational brain changes of adolescence. Understanding these differences should shed new light on both brain development and the functions of sleep.

Fig. 1.

Average ± SE time in bed (A), bedtime (B), and rise time (C) at each semiannual recording for the C9 cohort (subjects who entered the experiment at ∼9 yr of age; ▴) and C12 cohort (subjects who entered the experiment at ∼12 yr of age; ●). Results of mixed-effect analysis of age effects (F and P values) are shown on each plot. Linear trend lines (dashed lines) computed by mixed-effect analysis are shown for variables that changed significantly with age. Time in bed decreased across adolescence because bed times became later and rise times did not change.

Fig. 2.

Average ± SE school-night total sleep time (TST; A), non-rapid eye movement (NREM) sleep duration (B), and rapid eye movement (REM) sleep duration (C) plotted against age. Format is the same as in Fig 1. The adolescent decline in TST was entirely due to a significant decrease in NREM sleep duration. REM sleep duration increased slightly but significantly. ▴, C9 cohort; ●, C12 cohort.

Fig. 3.

Average ± SE school-night NREM sleep duration (open symbols) plotted with average delta power (solid symbols). The developmental curves for these two variables are similar. Both curves show a period of rapid decline between ages 11.5 and 16.5 yr of age. However, statistical analysis did not show a significant covariance in the parameters of the equations describing the declines. Note the different scaling for the two measures. While the shapes of the curves are similar, the decline in delta power is steeper than that of NREM duration. Triangles, C9 cohort; circles, C12 cohort.

Fig. 4.

Average ± SE TST (A), NREM sleep duration (B), and REM sleep duration (C) on the first extended night (solid symbols) and school-nights (open symbols). Format is the same as in Fig 1. TST on extended nights increased with age, as did the difference between TST on extended nights and school-nights. NREM duration on the extended night did not change with age. Differences between NREM duration on extended nights vs. school-nights increased across adolescence, because school-night NREM durations declined. The age-related increase in TST on extended nights was produced by significant age-related increases in REM sleep duration. Triangles, C9 cohort; circles, C12 cohort.