A surface-based analysis of hemispheric asymmetries and folding of cerebral cortex in term-born human infants

Abstract

We have established a population average surface-based atlas of human cerebral cortex at term gestation and used it to compare infant and adult cortical shape characteristics. Accurate cortical surface reconstructions for each hemisphere of 12 healthy term gestation infants were generated from structural magnetic resonance imaging data using a novel segmentation algorithm. Each surface was inflated, flattened, mapped to a standard spherical configuration, and registered to a target atlas sphere that reflected shape characteristics of all 24 contributing hemispheres using landmark constrained surface registration. Population average maps of sulcal depth, depth variability, three-dimensional positional variability, and hemispheric depth asymmetry were generated and compared with previously established maps of adult cortex. We found that cortical structure in term infants is similar to the adult in many respects, including the pattern of individual variability and the presence of statistically significant structural asymmetries in lateral temporal cortex, including the planum temporale and superior temporal sulcus. These results indicate that several features of cortical shape are minimally influenced by the postnatal environment.

Figure 1.

Example term infant segmentation volumes. The top row displays cropped T2-weighted MRI volumes for the right hemisphere viewed in the coronal plane for two term infants. The bottom row shows the final segmentation result created using the LIGASE method overlaid in red on the anatomic MRI. Note that the medial wall region (from the fundus of the parahippocampal sulcus inferiorly to callosal sulcus superiorly) was manually delineated and smoothed.

Figure 2.

Key steps in term infant surface generation and regional shape analysis. A, Example right hemisphere cortical segmentation volume (red) overlaid on anatomic T2-weighted MRI volume. B, Cerebral hull segmentation volume used for calculating sulcal depth. C, Lateral view of a fiducial surface reconstruction generated by a tessellation running along the boundary of the cortical segmentation volume and slight smoothing. D, Lateral view of the cerebral hull surface generated by a tessellation that runs along the boundary of the cerebral hull segmentation volume. E, Lateral view of an inflated surface displaying a map of cortical folding. The inflated surface was generated by applying 300 iterations of inflation to the fiducial surface. F, Lateral view of an inflated surface displaying a map of sulcal depth.

Figure 3.

Registration landmarks and creation of PALS-term12 registration target. Individual, population, and population-average landmarks are shown on several surfaces. Lateral views are displayed in the top row and medial views in the bottom row. A, Native-mesh inflated surface configuration for one term infant overlaid with a map of sulcal depth. The six landmarks (Core 6) used for registration are displayed on the surface. On the lateral surface, these consisted of the fundus of the central sulcus (yellow), Sylvian fissure (blue), and anterior half of the superior temporal gyrus (pink). Medial landmarks are the calcarine sulcus (orange) and the cortical margin of the medial wall divided into dorsal (purple) and ventral (magenta) portions. B, Core 6 landmarks displayed on the native-mesh spherical surface map for the same individual overlaid with a map of sulcal depth. C, Core 6 landmarks from both hemispheres (right and mirror-flipped left) of all 12 term infants projected to the standard-mesh (73,730 node) PALS-term12 spherical map. D, Average trajectory of each landmark for the 12 term infants displayed on the standard-mesh sphere. These average landmarks served as the target for surface-based registration.

Figure 4.

Standard-mesh fiducial surfaces for two term infants (left) and two adults (right), lateral views (top row) and the medial views (bottom row). Note the different scale bars. The particular individuals displayed have native-mesh surface areas closest to the age-specific population mean. Regions that hint at age differences in folding complexity include the anterior temporal region (blue arrow) and anterior cingulate region (black arrow).

Figure 5.

Right hemisphere population-average maps for the term infant and adult populations. Rows 1 and 2 show lateral views for a population of 12 term infants and 12 adults, respectively. Rows 3 and 4 show corresponding medial views for term infants and adults, respectively. All maps were generated after surface-based scale normalization. A, Average fiducial and average sulcal depth maps. The average fiducial surface was created by calculating the average spatial coordinate from all 12 individuals after surface-based scale normalization. The average sulcal depth maps were created by calculating the average sulcal depth across individuals for each node. Note scale differences for each age group. B, Maps of sulcal depth and 3D positional variability. Sulcal depth variability maps display the SD in sulcal depth for all individuals. 3D positional variability maps display the SD in 3D fiducial coordinate position for all individuals. Note scale differences for each age group. Average sulcal depth variability and 3D positional variability maps for the term infants and adults are displayed on the PALS-term12 and PALS-B12 standard-mesh average inflated surfaces, respectively.

Figure 6.

Analysis of hemispheric depth asymmetries. Rows 1 and 2 show lateral views for a population of 12 term infants and 12 adults, respectively. Rows 3 and 4 show corresponding medial views for term infants and adults, respectively. All maps are displayed on the age-specific standard-mesh average inflated surface. A, Maps of mean sulcal depth difference between hemispheres. Blue and green regions are deeper on the left; red and yellow regions are deeper on the right. B, Paired t statistic map for hemispheric depth difference. The paired t statistic was computed as the mean depth difference (left depth minus right depth) divided by the SEM. C, TFCE statistic map. This map was generated by applying the TFCE transform to the t statistic at each surface node. D, Location of significant depth difference clusters revealed by TFCE and permutation testing. Blue clusters are deeper on the left, and red clusters are deeper on the right.