Spontaneous cortical MEG activity undergoes unique age- and sex-related changes during the transition to adolescence

Abstract

Background: While numerous studies have examined the developmental trajectory of task-based neural oscillations during childhood and adolescence, far less is known about the evolution of spontaneous cortical activity during this time period. Likewise, many studies have shown robust sex differences in task-based oscillations during this developmental period, but whether such sex differences extend to spontaneous activity is not understood.

Methods: Herein, we examined spontaneous cortical activity in 111 typically-developing youth (ages 9-15 years; 55 male). Participants completed a resting state magnetoencephalographic (MEG) recording and a structural MRI. MEG data were source imaged and the power within five canonical frequency bands (delta, theta, alpha, beta, gamma) was computed. The resulting power spectral density maps were analyzed via vertex-wise ANCOVAs to identify spatially-specific effects of age, sex, and their interaction.

Results: We found robust increases in power with age in all frequencies except delta, which decreased over time, with findings largely confined to frontal cortices. Sex effects were distributed across frontal and temporal regions; females tended to have greater delta and beta power, whereas males had greater alpha. Importantly, there was a significant age-by-sex interaction in theta power, such that males exhibited decreasing power with age while females showed increasing power with age in the bilateral superior temporal cortices.

Discussion: These data suggest that the strength of spontaneous activity undergoes robust change during the transition from childhood to adolescence (i.e., puberty onset), with intriguing sex differences in some cortical areas. Future developmental studies should probe task-related oscillations and spontaneous activity in parallel.

Keywords: Development; Frequency; Magnetoencephalography (MEG); Power; Resting state.

Fig. 1.

Main Effect of Sex: Box and whisker plots display significant sex effects by frequency band and cluster. Collapsing across age, plots show relative power on the y-axis and sex on the x-axis. F-maps thresholded with TFCE are superimposed on the corresponding plots, with a black box indicating the peak. The color bar to the right of each F-map displays the scale of respective F values. Delta power was higher in females than males in bilateral right (A) and left inferior temporal (B) clusters. Beta power in the right superior parietal was higher in females relative to males (C). Alpha power was higher in males than in females in the left dorsal prefrontal cluster (D).

Fig. 2.

Main Effects of Age: Each participant’s relative power from the overall peak (maximum F value) is graphed in a scatterplot by frequency band and cluster. Relative power is shown on the y-axis and age on the x-axis. Trendlines are included on each graph indicating an increase or decrease in relative power with age. F-maps thresholded with TFCE are displayed with a black box indicating the peak. The color scale bar of F values is shown under each map. Delta power decreases with age in the right dorsal prefrontal cortex (A). Alpha power in the anterior cingulate cortex (B) and right middle temporal gyrus (C) increases with age. Beta power in the left superior occipital cortex (D) increases with age. Gamma (E) power increases with age in the left frontal pole.

Fig. 3.

Interaction Effects of Sex and Age: Scatterplots display relative theta power on the y-axis and age on the x-axis in bilateral left (A) and right (B) superior temporal cortices. The blue circles and trendline in each plot represent males, while the orange circles and trendline represent females. In both regions, relative theta power decreased with age in males and increased with age in females. F-maps thresholded with TFCE are displayed with a black box indicating the peak. The color bar next to each map shows the scale of F values. Extracted values from the peak are plotted for each participant in the graph.