Naturalistic stimuli reveal a critical period in visual cortex development: Evidence from adult-onset blindness

How do life experiences impact cortical function? In people who are born blind, the "visual" cortices are recruited for nonvisual tasks such as Braille reading and sound localization (e.g., Collignon et al., 2011; Sadato et al., 1996). The mechanisms of this recruitment are not known. Do visual cortices have a latent capacity to respond to nonvisual information that is equal throughout the lifespan? Alternatively, is there a sensitive period of heightened plasticity that makes visual cortex repurposing possible during childhood? To gain insight into these questions, we leveraged naturalistic auditory stimuli to quantify and compare cross-modal responses congenitally blind (CB, n=22), adult-onset blind (vision loss >18 years-of-age, AB, n=14) and sighted (n=22) individuals. Participants listened to auditory excerpts from movies; a spoken narrative; and matched meaningless auditory stimuli (i.e., shuffled sentences, backwards speech) during fMRI scanning. These rich naturalistic stimuli made it possible to simultaneous engage a broad range of cognitive domains. We correlated the voxel-wise timecourses of different participants within each group. For all groups, all stimulus conditions induced synchrony in auditory cortex and for all groups only the narrative stimuli synchronized responses in higher-cognitive fronto-parietal and temporal regions. Inter-subject synchrony in visual cortices was high in the CB group for the movie and narrative stimuli but not for meaningless auditory controls. In contrast, visual cortex synchrony was equally low among AB and sighted blindfolded participants. Even many years of blindness in adulthood fail to enable responses to naturalistic auditory information in visual cortices of people who had sight as children. These findings suggest that cross-modal responses in visual cortex of people born blind reflect the plasticity of developing visual cortex during a sensitive period.