Age-Related Differences and Heritability of the Perisylvian Language Networks

Abstract

Acquisition of language skills depends on the progressive maturation of specialized brain networks that are usually lateralized in adult population. However, how genetic and environmental factors relate to the age-related differences in lateralization of these language pathways is still not known. We recruited 101 healthy right-handed subjects aged 9-40 years to investigate age-related differences in the anatomy of perisylvian language pathways and 86 adult twins (52 monozygotic and 34 dizygotic) to understand how heritability factors influence language anatomy. Diffusion tractography was used to dissect and extract indirect volume measures from the three segments of the arcuate fasciculus connecting Wernicke's to Broca's region (i.e., long segment), Broca's to Geschwind's region (i.e., anterior segment), and Wernicke's to Geschwind's region (i.e., posterior segment). We found that the long and anterior arcuate segments are lateralized before adolescence and their lateralization remains stable throughout adolescence and early adulthood. Conversely, the posterior segment shows right lateralization in childhood but becomes progressively bilateral during adolescence, driven by a reduction in volume in the right hemisphere. Analysis of the twin sample showed that genetic and shared environmental factors influence the anatomy of those segments that lateralize earlier, whereas specific environmental effects drive the variability in the volume of the posterior segment that continues to change in adolescence and adulthood. Our results suggest that the age-related differences in the lateralization of the language perisylvian pathways are related to the relative contribution of genetic and environmental effects specific to each segment.

Significance statement: Our study shows that, by early childhood, frontotemporal (long segment) and frontoparietal (anterior segment) connections of the arcuate fasciculus are left and right lateralized, respectively, and remain lateralized throughout adolescence and early adulthood. In contrast, temporoparietal (posterior segment) connections are right lateralized in childhood, but become progressively bilateral during adolescence. Preliminary twin analysis suggested that lateralization of the arcuate fasciculus is a heterogeneous process that depends on the interplay between genetic and environment factors specific to each segment. Tracts that exhibit higher age effects later in life (i.e., posterior segment) appear to be influenced more by specific environmental factors.

Keywords: arcuate fasciculus; diffusion tensor tractography; heritability; language; lateralization; network asymmetry.

Figure 1.

Steps involved in the twin study design.

Figure 2.

Age-related differences in the volume of the long (frontotemporal), anterior (frontoparietal), and posterior (temporoparietal) segments of the arcuate fasciculus for each hemisphere. Group volumes for each age window (i.e., average volume calculated from subjects with an age range of ±5 years around each year) are indicated by triangles for the right segments and circles for the left segments. The axial slices above the graphs show the visitations maps for four representative age groups. A, The volume of the long segment is left lateralized in 10-year-old subjects and remains left lateralized throughout adolescence and early adulthood (differences between left and right volumes are statistically significant at all ages, p < 0.001). B, An opposite pattern of lateralization is observed for the anterior indirect segment, which exhibits right lateralization (differences between left and right volumes are statistically significant at all ages, p < 0.001). C, The posterior segment shows a statistically significant right lateralization before adolescence (age 9–11). Left and right differences diminish progressively throughout adolescence and adulthood. Asterisks indicate statistically significant differences between left and right (p < 0.001).

Figure 3.

Plots of LI for each of the three arcuate segments in MZ versus DZ twins. ***p < 0.001.

Figure 4.

The relative contribution (in percentages) of genetic, shared environmental, and specific environmental factors on the variability of the number of streamlines of the long, anterior and posterior segments in the left (L) and right (R) hemisphere. The border between familial (genetic and shared environmental) and specific environmental influences is shown with a triangle. The example of the virtual dissection of three perisylvian segments in one MZ and DZ twin pair is shown as a visual reference (segments are shown as detached from one another for clearer visual inspection).

Figure 5.

The relative proportion of A, C, and E on the variability of the number of streamlines, volume, FA, mean diffusivity, and their LIs for the long (in red), anterior (in green), and posterior (in yellow) segments. A box was drawn around A and C values in cases in which A and C were not significant individually, but reached significance when combined. *Significant contribution at p < 0.05.