Retinotopy-biased functional coupling in the face-processing network is shaped by early visual input

Abstract The ventral occipital temporal cortex (VOTC) exhibits a category-selective organization, with distinct regions preferentially responding to certain visual categories such as faces and scenes. This functional organization has been linked to retinotopic biases with face-selective regions of the fusiform gyrus predominantly responding to fovea-representing regions of early visual cortex (EVC) and scene-selective regions of the parahippocampal place area predominantly receiving input from EVC representing more peripheral parts of the visual field. Resting-state functional magnetic resonance imaging (rs-fMRI) studies have supported this view, by showing stronger functional connectivity (FC) between face-selective regions of the VOTC and fovea representing V1, and between scene-selective regions and peripheral visual field representing V1. These FC patterns have been reported to exist as early as in infancy and have been proposed to provide a scaffold for the later development of category-selectivity in the VOTC. Other studies have, however, indicated that intrinsic FC profiles are profoundly shaped by postnatal sensory experience raising the question of whether early visual experience is essential for the refinement of the retinotopy-biased, category-specific FC. Here, we examined rs-fMRI data from individuals with a history of transient congenital blindness due to bilateral congenital cataracts and from age- and sex-matched normally sighted participants. In normally sighted individuals we replicated significant FC between foveal V1 and face-selective areas of VOTC. By contrast, individuals with reversed congenital cataracts lacked a significant foveal bias in FC of face-selective regions but instead showed a significant FC between V1 representing parafoveal visual field and face-selective VOTC. No significant retinotopy-biased FC was observed for the scene-processing regions in either group. We concluded that early visual input drives the refinement of the typical fovea-biased FC within the emerging face-processing network. Altered FC might contribute to the repeatedly observed reduced face-selectivity in individuals with reversed congenital cataracts and associated face processing deficits.