The Concurrence of Cortical Surface Area Expansion and White Matter Myelination in Human Brain Development

Abstract

The human brain undergoes dramatic structural changes during childhood that co-occur with behavioral development. These age-related changes are documented for the brain's gray matter and white matter. However, their interrelation is largely unknown. In this study, we investigated age-related effects in cortical thickness (CT) and in cortical surface area (SA) as parts of the gray matter volume as well as age effects in T1 relaxation times in the white matter. Data from N = 170 children between the ages of 3 and 7 years contributed to the sample. We found a high spatial overlap of age-related correlations between SA and T1 relaxation times of the corresponding white matter connections, but no such relation between SA and CT. These results indicate that during childhood the developmental expansion of the cortical surface goes hand-in-hand with age-related increase of white matter fiber connections terminating in the cortical surface.

Figure 1.

Maps (Z scores) showing areas of significant correlation between surface area and age. The values are displayed on the inflated surface. Large regions of cortical surface area, particularly in frontal and temporal lobes, increase with age. Results are FDR corrected (α = 0.01).

Figure 2.

White matter T-map of voxels displaying a significant negative correlation between T₁ values and age. Results are masked using a P value image thresholded using α = 0.001 (FDR corrected). Results are shown on the group template created from the T₁ weighted images aligned to the MNI coordinate system.

Figure 3.

Normalized average distribution map of the start- and endpoints of connections traveling through the white matter clusters displaying significant negative correlation between T₁ values and age. Results are FDR corrected (P < 0.001).

Figure 4.

A: Visualization of significant effects of age on cortical surface area (blue) and on myelin content (T₁ values) (yellow) on the same map. A substantial overlap between these two maps is apparent (green). B: Z scores of the per-vertex relationship between Surface Area expansion and the distribution of myelinating fibers’ termination points.

Figure 5.

Spider plot showing the average visitation probability for clusters with significant correlation between age and T₁ values of white matter (in green), and complementary for the regionally corresponding correlation between age and cortical surface area (in red).

Figure 6.

Average streamline length distribution of the fibers originating or terminating from portions of the cortex displaying significant T1/SA relationship with Age (Fig. 3B).