Visual and auditory object representations in ventral visual cortex after restoring sight in humans

Abstract

Visual category-selective representations in human ventral occipital temporal cortex (VOTC) seem to emerge early in infancy. Surprisingly, the VOTC of congenitally blind humans features category-selectivity for auditory and haptic objects. Yet it has been unknown whether VOTC would show category-selective visual responses if sight were restored in congenitally blind humans. Assuming competition for synaptic space during development, cross-modal activation of VOTC as a consequence of congenital blindness might interfere with visual processing in sight-recovery individuals. To test this hypothesis, we investigated adults who had suffered a transient phase of congenital blindness due to bilateral dense cataracts before their sight was restored by cataract-removal surgery. In a functional magnetic resonance imaging (fMRI) study, participants watched movies of faces, scenes, body parts and other objects in the visual condition, while in the auditory condition they listened to the corresponding sounds. The most prominent group difference was the reduced face-selectivity in individuals with reversed congenital cataracts compared to age- and sex-matched normally-sighted individuals. In addition, a double dissociation was found: only sight-recovery individuals demonstrated significant decoding accuracy of visual categories based on auditory category representations in VOTC, while only normally-sighted individuals VOTC decoded auditory categories based on visual category representations. The present results uncovered the neural mechanisms of previously observed face processing impairments in individuals with reversed congenital blindness. We suggest that lower face-selectivity in the sight recovery group might arise from selective deficits in the cortical representation of the central visual field in lower-tier visual areas. Additionally, we speculate that in higher-order visual areas cross-modal activity might facilitate - rather than interfere - with visual functional recovery after congenital blindness.