'Visual' cortices of congenitally blind adults are sensitive to response selection demands in a go/no-go task

Abstract

Studies of occipital cortex plasticity in blindness provide insight into how intrinsic constraints interact with experience to determine cortical specialization. We tested the cognitive nature and anatomical origins of occipital responses during non-verbal, non-spatial auditory tasks. In a go/no-go task, congenitally blind (N=23) and sighted (N=24) individuals heard rapidly occurring (<1/s) non-verbal sounds and made one of two button presses (frequent-go 50%, infrequent-go 25%) or withheld a response (no-go, 25%). Rapid and frequent button presses heighten response selection/inhibition demands on the no-go trials: In sighted and blind adults a right-lateralized prefrontal (PFC) network responded most to no-go trials, followed by infrequent-go and finally frequent-go trials. In the blind group only, a right-lateralized occipital network showed the same response profile and the laterality of occipital and PFC responses was correlated across blind individuals. A second experiment with spoken sentences and equations (N=16) found that no-go responses in occipital cortex are distinct from previously identified occipital responses to spoken language. Finally, in resting-state data (N=30 blind, N=31 blindfolded sighted), no-go responsive 'visual' cortex of blind relative to sighted participants was more synchronized with PFC and less synchronized with primary auditory and sensory-motor cortices. No-go responsive occipital cortex showed higher resting-state correlations with no-go responsive PFC than language responsive inferior frontal cortex. We conclude that in blindness, a right-lateralized occipital network responds to non-verbal executive processes, including response selection. These results suggest that connectivity with fronto-parietal executive networks is a key mechanism for plasticity in blindness.

Keywords: Blindness; Executive demand; Executive function; Plasticity; Pluripotency; Response selection.

Figure 1.

Behavioral performance. Percent correct and response times for sighted (S) and blind (B) participants. Error bars indicate the within-subjects standard error of the mean.

Figure 2.

Beta values for task conditions within sighted (S) and congenitally blind (B) participants’ right prefrontal cortex (PFC), right occipital cortex (OC), bilateral sensorimotor cortex (SMC) ROIs. Error bars indicate the within-subjects SEM. Panel A shows vertices selected using the no-go > frequent-go contrast, Panel B shows vertices selected using the frequent-go + infrequent-go > no-go contrast. Search-spaces within which vertices (individual-subject ROIs) were selected shown in white below ROI results. See Figure S3 for overlap of individual-subject ROIs. (Panel C) Beta values from all conditions in go/no-go task for functional regions of interest of varying sizes defined as no-go > frequent-go vertices within the right occipital cortex (OC) search-space. ROI size ranges from 20 vertices (smallest) to 20% of entire ROI (largest). ROIs are defined according to a leave-one out analysis for response selective vertices.

Figure 3.

Vertices within occipital lobe color-coded according to which condition it responded to most across subjects in that group (condition producing the highest Beta-value).

Figure 4.

Responses to Language (Lang) and Math (in Betas) in right occipital go/no-go responsive cortices. Leave-one-run out analyses used to extract go/no-go responses in the same participants (N=16) and same vertices: frequent-go (FG), infrequent-go (IG), and no-go (NG). vertices.

Figure 5.

Whole brain contrasts for sighted (S), blind (B), and blind > sighted (B > S). Maps are thresholded at p<0.001 vertex-wise and p<0.05 cluster-corrected for multiple comparisons. Note that no vertices were more responsive in the sighted than blind group in any contrast.

Figure 6.

Laterality Results. (A) Sorted LIs for blind and sighted individuals. Each bar represents an individual participant’s LI. LIs range from +1, indicating strong left-lateralization, to −1, indicating strong right lateralization for the no-go > frequent-go contrast. Bars are color-coded according to degree of lateralization, white for left-lateralized, grey bilateral (threshold of +/− 0.2), and black right-lateralized. (B) Average LIs in frontal and occipital lobes of blind and sighted participants. Error bars reflect the standard error of the mean. C. Occipital LIs correlated with frontal LIs in blind individuals.

Figure 7.

Functional connectivity of no-go executive-function responsive occipital cortex (OC-EF). OC-EF identified as blind>sighted, no-go > frequent-go in a whole-cortex task-based analysis. (A) Regions of interest for resting-state analyses: OC-EF, primary auditory cortex (A1), primary sensorimotor cortices (S1/M1), executive-function responsive prefrontal cortices (PFC-EF), and language responsive prefrontal cortices (PFC-LG). (B) Fisher-transformed correlation coefficients between OC-EF and non-visual ROIs. Error bars indicate the within-subjects SEM.(C) Between-group differences in connectivity of executive-function responsive occipital cortex (OC-EF, in white) across the whole cortex. FDR-corrected contrasts for blind > sighted (in red) and sighted > blind (in blue).