Dissipation of sleep pressure is stable across adolescence

Abstract

The sleep electroencephalogram (EEG) undergoes many changes during adolescence. We assessed whether sleep homeostasis is altered across adolescent development using two measures: the dissipation of slow-wave activity (SWA, 0.6-4.6Hz) across the night and the rate of build-up of SWA in the first non-rapid eye movement (NREM) sleep episode. Furthermore, we examined the association between homeostatic and circadian measures, by correlating the build-up of SWA in the first non-rapid eye movement (NREM) sleep episode with circadian phase. Finally, we compared the dissipation of SWA in individuals with (PH+) and without (PH-) a parental history of alcohol abuse/dependence. Twenty children (8 PH+) and 25 teens (10 PH+) underwent two consecutive polysomnographic recordings at ages 9/10 and 15/16 years and again 1.5-3 years later. Thirteen young adults (ages 20-23 years; no PH+) were assessed one time. The decay of Process S was modeled for each individual at each assessment using data from both recordings. Four parameters of Process S were derived for EEG derivation C3/A2: time constant of the decay, lower asymptote (LA), the level of S at sleep onset (S(SO)), and S(SO) minus LA. We found no change in these parameters between assessments for the children and teen cohorts. Between-subject analysis of the follow-up assessment for children (ages 11-13 years) and the initial assessment for teens (ages 15/16 years) showed no difference in these parameters, nor did follow-up assessment of teens (ages 17-19 years) compared to the single assessment of young adults (ages 20-23 years). Similarly, we observed no developmental changes in the rate of the build-up of SWA in the first NREM sleep episode for our within- and between-subject analyses, or a correlation between this measure and circadian phase for either cohort. With regard to parental alcohol history, we found no difference in the dissipation of sleep pressure between PH+ and PH- children and teens. These results indicate that the dissipation of sleep pressure does not change across adolescent development, is not correlated with circadian phase, and does not differ between PH+ and PH- children and teens.

Figure 1

Illustration of methodology. Data are from the initial assessment of a boy in the children cohort. The data in green correspond to the adaptation night (Panels A and B), blue the baseline (panels D and E) night data. For each night, a hypnogram (Panels A and D), SWA (0.6 to 4.6 Hz; Panels B and E), and smoothed normalized SWA are shown (Panels C and F). The first REM sleep episode is skipped on the adaptation night (Panel A) and indicated with a black arrow. In the normalized SWA plots (Panels C and F), the maximum value in the first NREM sleep episode is depicted with a magenta dot and the fit to the first peak from which the rise-rate is derived are shown in black. Panel G shows the exponential decay fit using mean normalized SWA plotted at NREM sleep episode midpoint from both adaptation (green triangles) and baseline (blue circles) nights.

Figure 2

Data and exponential declined fitted to the data for one exemplary child, teen and young adult at derivation C3/A2. Normalized mean SWA at episode midpoint is plotted as a black dot for the initial session and as a diamond for the follow-up session. The exponential fit to the decay is shown as a solid line for the initial session and a dashed line at the follow-up session. We observed no change between assessments for any derivation in the children and teen cohorts.

Figure 3

Individual parameters of Process S for all cohorts. Each color represents an individual within a cohort. Black circles and bars show the mean value across participants and standard deviations.

Figure 4

Parameters obtained from the rise of SWA in the first NREM sleep episode. Each individual is shown in one color. The top plot shows the slope of the rise to the peak in the first NREM sleep episode. The bottom plots shows the time in minutes to the first peak. IA = Initial adaptation; IB = Initial baseline; FA = Final Adaptation; FB = Final Baseline. Mean values at each time point are shown in black diamonds.