The Topology of Pediatric Structural Asymmetries in Language-Related Cortex

Abstract

Structural asymmetries in language-related brain regions have long been hypothesized to underlie hemispheric language laterality and variability in language functions. These structural asymmetries have been examined using voxel-level, gross volumetric, and surface area measures of gray matter and white matter. Here we used deformation-based and persistent homology approaches to characterize the three-dimensional topology of brain structure asymmetries within language-related areas that were defined in functional neuroimaging experiments. Persistence diagrams representing the range of values for each spatially unique structural asymmetry were collected within language-related regions of interest across 212 children (mean age (years) = 10.56, range 6.39–16.92; 39% female). These topological data exhibited both leftward and rightward asymmetries within the same language-related regions. Permutation testing demonstrated that age and sex effects were most consistent and pronounced in the superior temporal sulcus, where older children and males had more rightward asymmetries. While, consistent with previous findings, these associations exhibited small effect sizes that were observable because of the relatively large sample. In addition, the density of rightward asymmetry structures in nearly all language-related regions was consistently higher than the density of leftward asymmetric structures. These findings guide the prediction that the topological pattern of structural asymmetries in language-related regions underlies the organization of language.

Cortical asymmetries at different spatial hierarchies relate to phonological processing ability

“…Moreover, we statistically controlled for age in the regression analyses to ensure that effects would be replicable across pediatric and adult samples. This approach would have limited sensitivity to effects in specific brain regions, perhaps including the superior temporal sulcus where we previously observed a rightward topological asymmetry that increased with age in a pediatric sample [ 61 ]. It is possible that there are developmental periods where asymmetries in specific cortical regions are predictive of phonological processing (or vice versa) because of age and experience-related changes in brain asymmetries or behavior, although structural asymmetries and socioeconomic status can exhibit independent additive effects in predicting phonological processing measures in children [ 33 ].…”

“…Instead, the persistent homology results appeared to depend on qualitatively distinct asymmetries that appeared to be due to hemispheric differences in sulcal/gyral variability, as in the case of the dorsal cingulate results, and perhaps increased cortical surface area given the consistency in asymmetry results from surface area and deformation-based approaches (e.g., results shown in [ 25 ] and Fig F in S1 Appendix ). That is, the persistent homology approach appeared to characterize hemispheric differences in sulcal/gyral features (Fig J in S1 Appendix ) and volume [ 61 ] across the persistence diagram. It may have been feasible to select participants with the same sulcal/gyral features to examine spatially specific volumetric effects with the deformation-based approach, but this would likely have missed effects from the current study that appeared to be influenced by differences in sulcal patterning.…”

“…Data sharing for these research data was approved by the contributing institutions and the Medical University of South Carolina Institutional Review Board (protocol # 20606), and the research was performed according to the principles of the Declaration of Helsinki. A subset of this data has been studied previously to show the application of methods for multisite retrospective data and persistent homology analysis of structural asymmetry data [ 10 , 61 , 99 – 101 ].…”

“…For example, a leftward asymmetry would be observed when the left motor cortex is reduced in volume to fit to the symmetrical template and the right motor cortex is increased in volume to fit to the symmetrical template. Cortical regions that are leftward or rightward asymmetric in these images exhibit hyperintense voxel values (e.g., motor/somatosensory cortex, planum temporale, and frontal and occipital petalias), which can be quantified using persistent homology within functionally distinct cortical parcellations or regions of interest (ROIs; Fig 1D ) [ 60 , 61 ].…”

“…Different objects in a scene will appear (birth) and then blend with the background (death) across exposure times. Although the number of asymmetric structures within ROI can vary, the data can be analyzed across participants by transforming the persistence diagram into a persistence landscape that represents the most asymmetric object across the range of lower intensity boundary (birth) values ( Fig 1F ) [ 61 ]. Thus, the persistent homology data can be considered a form of data reduction, as shown in Fig A in S1 Appendix where the persistent homology measure of dorsal cingulate/paracingulate asymmetry was significantly related to voxel-level data in the same region.…”