Naturalistic stimuli reveal a sensitive period in cross modal responses of visual cortex: Evidence from adult-onset blindness

Abstract

How do life experiences impact cortical function? In people who are born blind, the "visual" cortices are recruited during nonvisual tasks, such as Braille reading and sound localization. Do visual cortices have a latent capacity to respond to nonvisual information throughout the lifespan? Alternatively, is there a sensitive period of heightened plasticity that makes visual cortex repurposing especially possible during childhood? To gain insight into these questions, we leveraged meaningful naturalistic auditory stimuli to simultaneously engage a broad range of cognitive domains and quantify cross-modal responses across congenitally blind (n = 22), adult-onset blind (vision loss >18 years-of-age, n = 14) and sighted (n = 22) individuals. During fMRI scanning, participants listened to two types of meaningful naturalistic auditory stimuli: excerpts from movies and a spoken narrative. As controls, participants heard the same narrative with the sentences shuffled and the narrative played backwards (i.e., meaningless sounds). We correlated the voxel-wise timecourses of different participants within condition and group. For all groups, all stimulus conditions induced synchrony in auditory cortex while only the narrative stimuli synchronized responses in higher-cognitive fronto-parietal and temporal regions. As previously reported, inter-subject synchrony in visual cortices was higher in congenitally blind than sighted blindfolded participants and this between-group difference was particularly pronounced for meaningful stimuli (movies and narrative). Critically, visual cortex synchrony was no higher in adult-onset blind than sighted blindfolded participants and did not increase with blindness duration. Sensitive period plasticity enables cross-modal repurposing in visual cortices.

Keywords: Blindness; Narratives; Sensitive periods; Synchrony; Visual cortex.

Figure 1.

Whole-brain inter-subject correlation (ISC) reliability maps for the Backwards Speech stimulus (BW) and the Audio-Movie stimulus in each subject group. Voxel-level synchronization is shown within the sighted (S) group; the congenitally blind (CB) group; a subset of the CB group (CB subset) that matches the size of the adult-onset blind (AB) group (both n=14); and the AB group. Maps showing above-threshold ISC for each individual stimulus condition (first and second columns) are corrected for multiple comparisons. For each subject group, the corresponding difference map (third column) is limited to voxels that exceeded the threshold for either individual stimulus condition.

Figure 1.

Whole-brain inter-subject correlation (ISC) reliability maps for the Backwards Speech stimulus (BW) and the Audio-Movie stimulus in each subject group. Voxel-level synchronization is shown within the sighted (S) group; the congenitally blind (CB) group; a subset of the CB group (CB subset) that matches the size of the adult-onset blind (AB) group (both n=14); and the AB group. Maps showing above-threshold ISC for each individual stimulus condition (first and second columns) are corrected for multiple comparisons. For each subject group, the corresponding difference map (third column) is limited to voxels that exceeded the threshold for either individual stimulus condition.

Figure 2.

Left: Within-group ISC values for each region of interest (ROI) and each subject group. Right: ROIs are displayed in the left hemisphere (A1 in yellow; PLT in orange; V1 in blue) but inter-subject correlations are calculated bilaterally. Results for each individual audio-movie appear in the order listed and are shown for illustration purposes only; the reported results for Audio-Movies are averaged across the three movies. A1= early auditory cortex; PLT = posterior lateral temporal cortex; V1 = primary visual cortex

Figure 3.

Relationship between participant age and ISC for the Audio-Movies condition in the PLT ROI (left) and the V1 ROI (right). Trend lines depict the linear relationship between age and ISC in each subject group. Participant age was not strongly correlated with ISC in either PLT (AB: r= −.28; CB: r= −.16; S: r= −.04) or V1 (AB: r= .09; CB: r= .03; S: r= 0.1).