Development of visual category selectivity in ventral visual cortex does not require visual experience

Significance The brain’s ability to recognize visual categories is guided by category-selective ventral-temporal cortex (VTC). Whether visual experience is required for the functional organization of VTC into distinct functional subregions remains unknown, hampering our understanding of the mechanisms that drive category recognition. Here, we demonstrate that VTC in individuals who were blind since birth shows robust discriminatory responses to natural sounds representing different categories (faces, scenes, body parts, and objects). These activity patterns in the blind also could predict successfully which category was visually perceived by controls. The functional cortical layout in blind individuals showed remarkable similarity to the well-documented layout observed in sighted controls, suggesting that visual functional brain organization does not rely on visual input. To what extent does functional brain organization rely on sensory input? Here, we show that for the penultimate visual-processing region, ventral-temporal cortex (VTC), visual experience is not the origin of its fundamental organizational property, category selectivity. In the fMRI study reported here, we presented 14 congenitally blind participants with face-, body-, scene-, and object-related natural sounds and presented 20 healthy controls with both auditory and visual stimuli from these categories. Using macroanatomical alignment, response mapping, and surface-based multivoxel pattern analysis, we demonstrated that VTC in blind individuals shows robust discriminatory responses elicited by the four categories and that these patterns of activity in blind subjects could successfully predict the visual categories in sighted controls. These findings were confirmed in a subset of blind participants born without eyes and thus deprived from all light perception since conception. The sounds also could be decoded in primary visual and primary auditory cortex, but these regions did not sustain generalization across modalities. Surprisingly, although not as strong as visual responses, selectivity for auditory stimulation in visual cortex was stronger in blind individuals than in controls. The opposite was observed in primary auditory cortex. Overall, we demonstrated a striking similarity in the cortical response layout of VTC in blind individuals and sighted controls, demonstrating that the overall category-selective map in extrastriate cortex develops independently from visual experience.