Longitudinal sleep EEG trajectories indicate complex patterns of adolescent brain maturation

Abstract

New longitudinal sleep data spanning ages 6-10 yr are presented and combined with previous data to analyze maturational trajectories of delta and theta EEG across ages 6-18 yr in non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. NREM delta power (DP) increased from age 6 to age 8 yr and then declined. Its highest rate of decline occurred between ages 12 and 16.5 yr. We attribute the delta EEG trajectories to changes in synaptic density. Whatever their neuronal underpinnings, these age curves can guide research into the molecular-genetic mechanisms that underlie adolescent brain development. The DP trajectories in NREM and REM sleep differed strikingly. DP in REM did not initially increase but declined steadily from age 6 to age 16 yr. We hypothesize that the DP decline in REM reflects maturation of the same brain arousal systems that eliminate delta waves in waking EEG. Whereas the DP age curves differed in NREM and REM sleep, theta age curves were similar in both, roughly paralleling the age trajectory of REM DP. The different maturational curves for NREM delta and theta indicate that they serve different brain functions despite having similar within-sleep dynamics and responses to sleep loss. Period-amplitude analysis of NREM and REM delta waveforms revealed that the age trends in DP were driven more by changes in wave amplitude rather than incidence. These data further document the powerful and complex link between sleep and brain maturation. Understanding this relationship would shed light on both brain development and the function of sleep.

Fig. 1.

Comparison of the maturational trajectories for average delta (1–4 Hz) EEG power in non-rapid eye movement (NREM) and rapid eye movement (REM) sleep. Average (± SE) delta power is plotted against age for the C6 (●), C9 (▲), and C12 (■) cohorts. Note the different scales for the NREM delta power (black) and REM delta power (gray) axes. NREM delta power showed a complex maturational trend with an initial increase to a peak at about age 8 yr and a very steep decline between ages 12 and 16.5 yr. In contrast, REM delta power declined steadily until its decline decelerated at about age 16 yr.

Fig. 2.

Period-amplitude measures of delta (1–4 Hz) EEG during NREM sleep. A: maturational trend for NREM delta integrated amplitude (IA) closely resembled that for NREM delta power. IA is the product of average sample amplitude (ASA) and time in band (TIB). The maturational change in ASA (B) largely determined the trend in IA. TIB (C) remained constant between ages 6 and 11 before declining. We could not find a basis for the C9 C12 cohort difference in TIB in late adolescence. It was not due to a few outlying observations and probably represents sampling variation.

Fig. 3.

Period-amplitude measures of delta (1–4 Hz) EEG during REM sleep (format as in Fig. 2). In contrast to NREM, delta ASA and delta TIB showed similar maturational trajectories in REM sleep.

Fig. 4.

Maturation of delta (1–4 Hz) mean frequency during NREM sleep (A) and REM sleep (B). In NREM sleep, delta mean frequency was unchanged between ages 6 and 10 yr and then increased steadily. In REM sleep, delta mean frequency increased across ages 6 to 18 yr.

Fig. 5.

Comparison of the maturational trajectories for theta (4–8 Hz) FFT power in NREM sleep and REM sleep. The format is the same as in Fig. 1. In contrast to the different age trajectories for delta power in NREM and REM sleep, theta power showed similar maturational trends in NREM and REM sleep.