Evolution of reading and face circuits during the first three years of reading acquisition

Abstract

Although words and faces activate neighboring regions in the fusiform gyrus, we lack an understanding of how such category selectivity emerges during development. To investigate the organization of reading and face circuits at the earliest stage of reading acquisition, we measured the fMRI responses to words, faces, houses, and checkerboards in three groups of 60 French children: 6-year-old pre-readers, 6-year-old beginning readers and 9-year-old advanced readers. The results showed that specific responses to written words were absent prior to reading, but emerged in beginning readers, irrespective of age. Likewise, specific responses to faces were barely visible in pre-readers and continued to evolve in the 9-year-olds, yet primarily driven by age rather than by schooling. Crucially, the sectors of ventral visual cortex that become specialized for words and faces harbored their own functional connectivity prior to reading acquisition: the VWFA with left-hemispheric spoken language areas, and the FFA with the contralateral region and the amygdalae. The results support the view that reading acquisition occurs through the recycling of a pre-existing but plastic circuit which, in pre-readers, already connects the VWFA site to other distant language areas. We argue that reading acquisition does not compete with the face system directly, through a pruning of preexisting face responses, but indirectly, by hindering the slow growth of face responses in the left hemisphere, thus increasing a pre-existing right hemispheric bias. HighlightsO_LIWritten words and faces activate neighboring areas of the fusiform gyri, but their developmental trajectory is different. C_LIO_LIThe growth of word-induced activation in VWFA is primarily due to schooling. C_LIO_LIThe growth of face responses is primarily affected by age rather than by schooling. C_LIO_LIWord and face-related areas exhibit distinct functional connectivity even prior to reading acquisition C_LIO_LIVWFA is initially functionally connected with left-hemisphere spoken language areas, and FFA with amygdala and contralateral FFA. C_LI