Visual deprivation selectively reshapes the intrinsic functional architecture of the anterior insula subregions

Abstract

The anterior insula (AI) is the core hub of salience network that serves to identify the most relevant stimuli among vast sensory inputs and forward them to higher cognitive regions to guide behaviour. As blind subjects were usually reported with changed perceptive abilities for salient non-visual stimuli, we hypothesized that the resting-state functional network of the AI is selectively reorganized after visual deprivation. The resting-state functional connectivity (FC) of the bilateral dorsal and ventral AI was calculated for twenty congenitally blind (CB), 27 early blind (EB), 44 late blind (LB) individuals and 50 sighted controls (SCs). The FCs of the dorsal AI were strengthened with the dorsal visual stream, while weakened with the ventral visual stream in the blind than the SCs; in contrast, the FCs of the ventral AI of the blind was strengthened with the ventral visual stream. Furthermore, these strengthened FCs of both the dorsal and ventral AI were partially negatively associated with the onset age of blindness. Our result indicates two parallel pathways that selectively transfer non-visual salient information between the deprived "visual" cortex and salience network in blind subjects.

Figure 1. Interactions between groups and locations of anterior insula on the resting-state functional connectivity.

A mixed-model ANOVA was performed with the groups (CB, EB, LB and SC) as between-subjects effect, and the hemispheres (left versus right AI) and locations (dorsal versus ventral AI) as within-subjects effects (q < 0.01, FDR corrected). Color bar represents the F value. (a) The AI subregions used for calculation of the FC were obtained from an early study by Deen and Pelphrey et al. (b) ANOVA revealed significant interactions between groups and AI locations, which were located in the bilateral IPA, CalS and LG, and MOG. Abbreviations: AI = anterior insula, ANOVA = analysis of variance, CalS = calcarine sulcus, CB = congenitally blind, EB = early blind, FC = functional connectivity, FDR = false discovery rate, IPA = intraparietal area, LB = late blind, LG = lingual gyrus, MOG = middle occipital gyrus, SC = sighted controls.

Figure 2. Intergroup differences in functional connectivity of the dorsal anterior insula.

A one way ANOVA was performed to test inter-group differences in FC of the dorsal AI within the brain regions that showed significant group × AI location interactions (q < 0.01, FDR corrected). The first row represents the AI subregions. The second row represents the findings of one-way ANOVA, and the color bar in this row represents F value. The remaining rows represents the paired-wise comparisons between the 4 groups, and the color bar represents T value. Abbreviations: AI = anterior insula, ANOVA = analysis of variance, CB = congenitally blind, EB = early blind, FC = functional connectivity, LB = late blind, SC = sighted controls, FDR = false discovery rate.

Figure 3. Intergroup differences in functional connectivity of the ventral AI.

A one way ANOVA was performed to test inter-group differences in FC of the ventral AI within the brain regions that showed significant group × AI location interactions (q < 0.01, FDR corrected). The first row represents the AI subregions. The second row row represents the findings of one-way ANOVA, and the color bar in this row represents F value. The remaining rows represents the paired-wise comparisons between the 4 groups, and the color bar represents T value. Abbreviations: AI = anterior insula, ANOVA = analysis of variance, CB = congenitally blind, EB = early blind, FC = functional connectivity, LB = late blind, SC = sighted controls, FDR = false discovery rate.

Figure 4. Relationship between functional connectivity of anterior insula subregions and the onset age of blindness.

voxel-wise regression analyses demonstrated significant negative correlations between the onset age of blindness and FC of right IPA with the dorsal AI, and between the onset age of blindness and FC of right LG with the ventral AI (q < 0.01, FDR corrected). Color bar represents the T value. The scatter plots (right panels) represent the association between the onset age of blindness and mean FC of the visual ROIs that showing significant correlations with the onset age. Abbreviations: AI = anterior insula, FC = functional connectivity, FDR = false discovery rate, IPA = intraparietal area, LG = lingual gyrus.