The emergence of long-range language network structural covariance and language abilities

Language skills increase as the brain matures. Language processing, especially the comprehension of syntactically complex sentences, is supported by a brain network involving functional interactions between left inferior frontal and left temporal regions in the adult brain, with reduced functional interactions in children. Here, we examined the gray matter covariance of the cortical thickness network relevant for syntactic processing in relation to language abilities in preschool children (i.e., 5-year-olds) and analyzed the developmental changes of the cortical thickness covariance cross-sectionally by comparing preschool children, school age children, and adults. Further, to demonstrate the agreement of cortical thickness covariance and white matter connectivity, tractography analyses were performed. Covariance of language-relevant seeds in preschoolers was strongest in contralateral homologous regions. A more adult-like, significant cortical thickness covariance between left frontal and left temporal regions, however, was observed in preschoolers with advanced syntactic language abilities. By comparing the three age groups, we could show that the cortical thickness covariance pattern from the language-associated seeds develops progressively from restricted in preschoolers to widely-distributed brain regions in adults. In addition, our results suggest that the cortical thickness covariance difference of the left inferior frontal gyrus to superior temporal gyrus/sulcus between preschoolers and adults is accompanied by distinctions in the white matter tracts linking these two areas, with more mature white matter in the arcuate fasciculus in adults compared to preschoolers. These findings provide anatomical evidence for developmental changes in language both from the perspective of gray matter structure co-variation within the language network and white matter maturity as the anatomical substrate for the structural covariance.