Spontaneous cortical dynamics from the first years to the golden years

Abstract

In the largest and most expansive lifespan magnetoencephalography (MEG) study to date (n = 434, 6 to 84 y), we provide critical data on the normative trajectory of resting-state spontaneous activity and its temporal dynamics. We perform cutting-edge analyses to examine age and sex effects on whole-brain, spatially-resolved relative and absolute power maps, and find significant age effects in all spectral bands in both types of maps. Specifically, lower frequencies showed a negative correlation with age, while higher frequencies positively correlated with age. These correlations were further probed with hierarchical regressions, which revealed significant nonlinear trajectories in key brain regions. Sex effects were found in absolute but not relative power maps, highlighting key differences between outcome indices that are generally used interchangeably. Our rigorous and innovative approach provides multispectral maps indicating the unique trajectory of spontaneous neural activity across the lifespan, and illuminates key methodological considerations with the widely used relative/absolute power maps of spontaneous cortical dynamics.

Keywords: aging; development; lifespan; magnetoencephalography; oscillations.

Fig. 1.

Neural power distribution schematic. (A) Participants sat upright in the MEG with their eyes closed for 5 to 8 min. Individual sensors capture raw temporal dynamics as shown through the time series in the square box above the MEG. These magnetic field strength measurements can be projected to the cortex using source reconstruction approaches. Each location in these maps can be further broken down into individual canonical frequency bands as shown in the line graph to the right. Each frequency band is denoted by a specific color: delta (2 to 4 Hz) purple, theta (5 to 7 Hz) blue, alpha (8 to 12 Hz) green, beta (15 to 29 Hz) orange, and gamma (3 to 59 Hz) red. (B) Distribution of relative power. The grand-averaged distribution for relative power across all participants (n = 434) is shown for each of the frequencies denoted in part (A) in percentage units. Compared with the lower frequencies, higher frequency bands are comprised of a smaller percentage of relative power. Additionally, each band has a unique power distribution: delta-anterior frontal, theta-posterior frontal, alpha-occipital, beta-sensorimotor cortices, and gamma-prefrontal regions. (C) Distribution of absolute power. The grand-averaged distribution for absolute power across all participants (n = 434) is shown for each of the canonical frequency bands denoted in part (A) using the pseudo neural activity index (PNAI) as units. Each frequency band has a unique power distribution: delta-anterior frontotemporal, theta-temporal, alpha-occipital, beta-sensorimotor, and gamma-posterior frontal.

Fig. 2.

The impact of age on relative power. (Middle) F-maps thresholded with TFCE are displayed for the main effect of age on relative power with the center of the black boxes denoting the peak for each respective hemisphere, although the box encompasses a much larger region than the peak vertex itself. The color bar beneath the brains shows the scale of F-values. Both the left and right clusters survived TFCE and FWE correction. (Left and Right) Scatterplots display the extracted values from the peak of the significant main effect of age on spontaneous relative power. Relative power (percent) is plotted on the Y-axis, and age (years) is plotted on the X-axis. The color distributions correspond to the canonical frequency band being shown (delta-purple, theta-blue, alpha-green, beta-orange, and gamma-red). The dots on the scatterplot represent each individual participant and the trendline represents the group’s linear trajectory. (A) Delta (2 to 4 Hz): Relative power decreased with age across the cortex with peaks in bilateral middle temporal gyri. (B) Theta (5 to 7 Hz): Relative power decreased with age across the parietal and temporal lobes with peaks in bilateral superior temporal gyri. (C) Alpha (8 to 12 Hz): Relative power increased with age across the cortex with peaks in bilateral inferior temporal gyri. (D) Beta (15 to 29 Hz): Relative power increased with age across the cortex with peaks in bilateral precentral gyri. (E) Gamma (30 to 59 Hz): Relative power increased with age across the cortex with peaks in superior frontal gyri.

Fig. 3.

The impact of age on absolute power. (Middle) F-maps thresholded with TFCE are displayed for the main effect of age on absolute power with the center of the black boxes denoting the peak for each respective hemisphere, although the box encompasses a much larger region than the peak vertex itself. The color bar beneath the brains shows the scale of F-values. Both the left and right clusters survived TFCE and FWE correction. (Left and Right) Scatterplots display the extracted values from the peak of the significant main effect of age on spontaneous absolute power. Absolute power, in units corresponding to the pseudo neural activity index (PNAI), is plotted on the Y-axis, and age (years) is plotted on the X-axis. The color distributions correspond to the canonical frequency band being shown (delta-purple, theta-blue, alpha-green, beta-orange, and gamma-red). The dots on the scatterplot represent each individual participant and the trendline represents the group’s linear trajectory. (A) Delta (2 to 4 Hz). Absolute power decreased with age across the cortex with peaks in bilateral temporoparietal junction. (B) Theta (5 to 7 Hz). Absolute power decreased with age across the cortex with peaks in the left superior temporal gyrus and right supramarginal gyrus. (C) Alpha (8 to 12 Hz). Absolute power increased with age in frontal and temporal regions with peaks in bilateral inferior temporal gyri. (D) Beta (15 to 29 Hz). Absolute power increased with age across the cortex with peaks in bilateral precentral gyri. (E) Gamma (30 to 59 Hz). Absolute power increased with age across the cortex with peaks in superior frontal gyri.

Fig. 4.

Quadratic analysis of age effects. Scatterplots displaying the peak values of the significant main effect of age and power with linear (gray) and quadratic (color) fits for each significant age effect. Asterisks indicate that the quadratic fit is significantly better than the linear. The box on each brain represents the peak of each cluster from which data were extracted. The dots on the scatterplots represent each individual participant with the corresponding colored line showing the quadratic fit, with the shaded portion representing SE. The color distributions correspond to the canonical frequency band being shown (delta-purple, theta-blue, alpha-green, beta-orange, and gamma-red). (Left) Relative power (%) is plotted on the Y-axis, and age is plotted on the X-axis. Left hemispheric clusters are in the left column, and right hemispheric clusters are in the right column. (Right) Absolute power in pseudo neural activity index (PNAI) units is plotted on the Y-axis, and age is plotted on the X-axis. Left hemispheric clusters are in the left column and right hemispheric clusters are in the right column. (A) Delta (2 to 4 Hz): Relative delta power had a significant quadratic relationship with age in both right and left hemispheres. (B) Theta (5 to 7 Hz): Relative theta power did not have a significant quadratic relationship with age in either right or left hemisphere. (C) Alpha (8 to 12 Hz): Relative alpha power had a significant quadratic relationship with age in both right and left hemispheres. (D) Beta (15 to 29 Hz): Relative beta power had a significant quadratic relationship with age in the right but not the left hemisphere. (E) Gamma (30 to 59 Hz): Relative gamma power had a significant quadratic relationship with age in both right and left hemispheres. (F) Delta (2 to 4 Hz): Absolute delta power had a significant quadratic relationship with age in both right and left hemispheres. (G) Theta (5 to 7 Hz): Absolute theta power had a significant quadratic relationship with age in the left but not the right hemisphere. (H) Alpha (8 to 12 Hz): Absolute alpha power did not have a significant quadratic relationship with age in either right or left hemisphere. (I) Beta (15 to 29 Hz): Absolute beta power had a significant quadratic relationship with age in the right but not the left hemisphere. (J) Gamma (30 to 59 Hz): Absolute gamma power had a significant quadratic relationship with age in both right and left hemispheres.

Fig. 5.

The effect of sex on absolute power. (Middle) F-maps thresholded with TFCE are displayed for the main effect of sex on absolute power with the center of the black boxes denoting the peak for each respective hemisphere, although the box encompasses a much larger region than the peak vertex itself. The color bar beneath the brains shows the scale of F-values. Both the left and right clusters survived TFCE and FWE correction. (Left and Right) Scatterplots display the extracted values from the peak of the significant main effect of sex on spontaneous absolute power. Absolute power, in pseudo neural activity index (PNAI) units, is plotted on the X-axis, and sex is plotted on the Y-axis. The color distributions correspond to the canonical frequency band (delta-purple, theta-blue, alpha-green). The dots on the boxplots represent each individual participant with the raincloud representing the distribution. (A) Delta (2 to 4 Hz): Absolute power was increased in males relative to females across an extended area of the frontal lobe, with peaks at the frontal poles. (B) Theta (5 to 7 Hz): Absolute power was increased in males relative to females in a more restricted area of the anterior frontal lobe, with peaks at the frontal poles. (C) Alpha (8 to 12 Hz): Absolute power increased in males compared to females with peaks in lateral occipital lobes.