Numerous studies have shown that phonological skills are critical for successful reading acquisition. However, how the brain network supporting phonological processing evolves and how it supports the initial course of learning to read is largely unknown. Here, for the first time, we characterized the emergence of the phonological network in 28 children over three stages (prereading, beginning reading, and emergent reading) longitudinally. Across these three time points, decreases in neural activation in the left inferior parietal cortex (LIPC) were observed during an audiovisual phonological processing task, suggesting a specialization process in response to reading instruction/experience. Furthermore, using the LIPC as the seed, a functional network consisting of the left inferior frontal, left posterior occipitotemporal, and right angular gyri was identified. The connection strength in this network co-developed with the growth of phonological skills. Moreover, children with above-average gains in phonological processing showed a significant developmental increase in connection strength in this network longitudinally, while children with below-average gains in phonological processing exhibited the opposite trajectory. Finally, the connection strength between the LIPC and the left posterior occipitotemporal cortex at the prereading level significantly predicted reading performance at the emergent reading stage. Our findings highlight the importance of the early emerging phonological network for reading development, providing direct evidence for the Interactive Specialization Theory and neurodevelopmental models of reading.

Background: Studies exploring neuroanatomic correlates of reading have associated white matter tissue properties with reading disability and related componential skills (e.g., phonological and single-word reading skills). Mean diffusivity (MD) and fractional anisotropy (FA) are widely used surrogate measures of tissue microstructure with high sensitivity; however, they lack specificity for individual microstructural features. Here we investigated neurite features with higher specificity in order to explore the underlying microstructural architecture. Methods: Diffusion weighted images (DWI) and a battery of behavioral and neuropsychological assessments were obtained from 412 children (6 – 16 years of age). Neurite indices influenced by orientation and density were attained from 23 major white matter tracts. Partial correlations were calculated between neurite indices and indicators of phonological processing and single-word reading skills using age, sex, and image quality metrics as covariates. In addition, mediation analysis was performed using structural equation modeling (SEM) to evaluate the indirect effect of phonological processing on reading skills. Results: We observed that orientation dispersion index (ODI) and neurite density index (NDI) were negatively correlated with single-word reading and phonological processing skills in several tracts previously shown to have structural correlates with reading efficiency. We also observed a significant and substantial effect in which phonological processing mediated the relationship between neurite indices and reading skills in most tracts. Conclusions: In sum, we established that better reading and phonological processing skills are associated with greater tract coherence (lower ODI) and lower neurite density (lower NDI). We interpret these findings as evidence that reading is associated with neural architecture and its efficiency.

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