Longitudinal trajectories of brain development from infancy to school age and their relationship to literacy development

Abstract

Reading is one of the most complex skills that we utilize daily, and it involves the early development and interaction of various lower-level subskills, including phonological processing and oral language. These subskills recruit brain structures, which begin to develop long before the skill manifests and exhibit rapid development during infancy. However, how longitudinal trajectories of early brain development in these structures support long-term acquisition of literacy subskills and subsequent reading is unclear. Children underwent structural and diffusion MRI scanning at multiple timepoints between infancy and second grade and were tested for literacy subskills in preschool and decoding and word reading in early elementary school. We developed and implemented a reproducible pipeline to generate longitudinal trajectories of early brain development to examine associations between these trajectories and literacy (sub)skills. Furthermore, we examined whether familial risk of reading difficulty and children's home literacy environments, two common literacy-related covariates, influenced those trajectories. Results showed that individual differences in curve features (e.g., intercepts and slopes) for longitudinal trajectories of volumetric, surface-based, and white matter organization measures were linked directly to phonological processing and indirectly to first-grade decoding and word reading skills via phonological processing. Altogether, these findings suggest that the brain bases of phonological processing, previously identified as the strongest behavioral predictor of reading and decoding skills, may already begin to develop by birth but undergo further refinement between infancy and preschool. The present study underscores the importance of considering academic skill acquisition from the very beginning of life.

Keywords: Biological Sciences/Neuroscience; MRI; brain; development; infant; literacy; longitudinal.

Figure 1.

Age distribution of longitudinal dataset from infancy to late childhood. All children had structural and/or diffusion MRI data from at least two observations (dots). Blue, New England cohort; orange, Calgary cohort.

Figure 2.

Average longitudinal trajectories from infancy to late childhood by measure. Raw estimates for each brain region examined and each measure were submitted to linear mixed effects models using a logarithmic function. Individual growth curves predicted by this model were averaged to show the overall longitudinal trajectory of the sample for each volumetric/surface-based (blue lines) and diffusion (green lines) measure. Absolute brain estimates were then converted to percent change values to visualize all brain measures along a single axis. For growth curves for separate brain regions and tracts, please see Supplementary Figures 17–22.

Figure 3.

Longitudinal trajectories of brain structure from infancy to late childhood according to phonological processing skill in preschool/early kindergarten. Graphs depict average trajectories for children with low (< 85), average ( – 115), and high (> 115) standardized phonological processing scores for measures and regions whose (A) intercepts, (B) slopes, or (C) both intercepts and slopes correlated with phonological processing (p_FDR < 0.05). Correlation statistics are reported adjacent to their corresponding plots; intercept and slope statistics for surface area averaged here for visualization purposes but reported separately in Supplemental Figure 23. As a group, children with low phonological processing in preschool/early kindergarten tended to have attenuated longitudinal trajectories, either because they began with lower estimates, as with less gray matter volume in the left banks of the superior temporal gyrus at birth (upper left graph), or because they had slower rates of development, as with white matter volume in other left hemisphere brain regions.

Figure 4.

Longitudinal trajectories of mean diffusivity from infancy to late childhood according to phonological processing skill in preschool/early kindergarten. Graph depicts average trajectories for children with low (< 85), average ( – 115), and high (> 115) standardized phonological processing scores for the left arcuate fasciculus nodes whose slopes correlated with phonological processing (p_FWE < 0.05). Children with low phonological processing tended to exhibit faster development (i.e., more negative slope) in anterior arcuate fasciculus.

Figure 5.

Phonological processing skill mediates the relationship between early brain development and decoding and word reading. Indirect effects (filled arrows) were found for (A) intercepts of gray matter volume in the left banks of the superior temporal sulcus; (B) slopes of white matter volume and (C) intercepts and slopes of surface area in left temporo-parietal and inferior frontal regions; and (D) slopes of mean diffusivity in left arcuate fasciculus (nodes 6–25, green). Note: indirect effects are depicted for surface area slopes only; surface area intercept effects are reported in Supplementary Tables 10, 11.