Maturational Patterns of Sigma Frequency Power Across Childhood and Adolescence: A Longitudinal Study

Abstract

Study objectives: To further evaluate adolescent brain maturation by determining the longitudinal trajectories of nonrapid eye movement (NREM) sigma (11-15 Hz) power across childhood-adolescence.

Methods: The maturational trend for sigma (11-15 Hz) power was evaluated in an accelerated longitudinal study of three overlapping age cohorts (n = 92) covering ages 6 to 18 y. Semiannually, sleep electroencephalography (EEG) was recorded from participants sleeping at home in their normal sleep environment while keeping their current school night schedules.

Results: Sigma frequencies became faster with age. The frequency of the 11-15 Hz spectral peak increased linearly. Sigma frequency power (SFP) declined with age, but its trajectory was complex (cubic). Power in a group of low sigma subfrequencies declined with age. Power in a group of high sigma frequencies increased with age. Power in subfrequencies within 11-15 Hz also showed different trends across the night, with lower frequencies increasing across NREM periods and higher frequencies decreasing across NREM periods. The upper and lower boundaries for the sigma frequencies that changed across NREMPs shifted upward with age.

Conclusions: We hypothesize that these maturational brain changes result from synaptic elimination which decreases sleep depth and streamlines circuits. SFP displays a maturational trajectory different from both delta and theta power. Theories on the function of sigma must be reconciled with its maturational trajectory. These findings further demonstrate the value of sleep EEG for studying noninvasively the complex developmental brain changes of adolescence.

Keywords: EEG; NREM; adolescence; brain maturation; sleep spindle; trajectory.

Figure 1

Power spectra at age 12 y for electroencephalogram recorded during the first 5 h of nonrapid eye movement (NREM) sleep (black line) or during the second and third rapid eye movement (REM) periods (gray line). Mean (n = 65) power density is plotted against the midpoint of the frequency band. A peak occurs in the sigma frequency band (11–15 Hz) in NREM but not in REM sleep in each age group.

Figure 2

Maturational trajectory of the frequency of peak sigma power. The average (± standard error) peak frequency at each semiannual recording is plotted against age for each of the three cohorts, C6 (circles), C9 (squares), and C12 (triangles). The linear increase is highly significant (F1,865 = 128, P < 0.0001).

Figure 3

Maturational trajectory of sigma power shows a power increase at younger ages followed by a steep decrease across adolescence. Average (± standard error) power at each semiannual recording is plotted against age for the three cohorts. The trend line is a cubic function fit with mixed-effect analysis.

Figure 4

Statistical analysis demonstrates significantly different maturational trajectories for the subfrequencies within sigma. For each 0.195 Hz subfrequency band between 10.8 and 15.3 Hz, the t-value for the slope of the age-related change in power is plotted against frequency band midpoint. Results are for the first 5 h of nonrapid eye movement (NREM) sleep (solid line, circles) and the second and third rapid eye movement (REM) periods (dashed line, triangles). Horizontal gray lines indicate significance level. Power in frequencies below 12.8 Hz and above 14.9 Hz declined significantly with age, and power in frequencies between 13.4 and 14.4 Hz increased significantly with age. In REM sleep, power in all sigma subfrequencies declined with age.

Figure 5

Maturational trajectory of power in (A) 11.0–12.8 Hz, the frequency range that significantly decreases in power with age and (B) 13.4–14.4 Hz, the frequency range that significantly increases in power with age. Also shown for comparison are the maturational trends for (C) delta (1–4 Hz) and (D) theta (4–8 Hz) in these subjects. The trajectory for low frequency sigma power (A) strongly resembles that for delta power (C). Format as in Figure 3.

Figure 6

The trend in power across the night differs by frequency band. Mean power (± standard error) for nonrapid eye movement (NREM) periods 1–4 for the seventh recording of the C9 cohort (mean age = 12.4 y) is plotted against NREM period for (A) a subfrequency, 12.6–12.8 Hz, which increases in power across the night and for (B) a subfrequency, 14.6–14.7 Hz, which decreases in power across the night. The trends across the night change as children mature. Thus, Figure 6C shows for each recording period for each cohort, the lowest 0.195 Hz frequency band for which power increases significantly across the night (solid line), the highest 0.195 Hz frequency band for which power increases significantly across the night (dotted line), and the lowest 0.195 Hz frequency band at which the trend reverses and power decreases significantly across the night (dashed line).