Longitudinal associations between language network characteristics in the infant brain and school-age reading abilities are mediated by early-developing phonological skills

Abstract Reading acquisition is a prolonged learning process relying on language development starting in utero. Behavioral longitudinal studies reveal prospective associations between infant language abilities and preschool/kindergarten phonological development, which in turn relates to subsequent reading performance. More recently, pediatric neuroimaging work has begun to characterize the neural network underlying language development in infants. However, it is still unknown how the infant language network scaffolds long-term language and reading acquisition. We addressed this question in a 7-year longitudinal study from infancy to school-age. Seventy-six infants (33 females) completed resting-state fMRI scanning during natural sleep, and were followed until kindergarten, where their language skills, including phonological processing abilities, were assessed behaviorally. Of this larger cohort, forty-one (21 females) were further assessed on their emergent word reading abilities after receiving at least one year of reading instructions. Hierarchical clustering analyses first identified a tripartite modular structure within the infant language neural network, consisting of the inferior frontal, middle frontal, and temporoparietal regions, respectively. Infant functional connectivity (FC) of the inferior frontal module prospectively correlated with kindergarten-age phonological skills and emergent word reading abilities, controlling for infant age and head movement during scanning, nonverbal IQ, and critical environmental factors. Further, kindergarten-age phonological skills mediated the relationship between infant FC and school-age reading abilities, implying a critical mid-way milestone for long-term reading development starting in infancy. Overall, our findings shed light on the neurobiological mechanisms underlying the infant’s emergent language network serving as a scaffold for subsequent language and reading acquisition. Significance Statement A critical aspect of successful reading acquisition is language development starting in utero. While previous studies have started characterizing the neural network mechanisms underlying language development as early as infancy, their relationships to long-term language and reading acquisition remain unknown. Utilizing a seven-year longitudinal imaging dataset starting in infancy, the current study identified a modular infant language network in which functional connectivity (FC) of the inferior frontal module prospectively correlated with children’s phonological skills in kindergarten. Infant FC of the inferior frontal module further contributed to individual differences in emergent word reading abilities and this relationship was mediated by kindergarten-age phonological skills. Our findings shed light on the neurobiological mechanisms by which infant language capacities could scaffold long-term reading acquisition.