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. 2022 Sep 23:16:902866.
doi: 10.3389/fnins.2022.902866. eCollection 2022.

Sight restoration reverses blindness-induced cross-modal functional connectivity changes between the visual and somatosensory cortex at rest

Negin Nadvar  1 , Noelle Stiles  2 , Jeiran Choupan  2 , Vivek Patel  3 , Hossein Ameri  2 , Yonggang Shi  2 , Zhongming Liu  1   4 , John Jonides  5 , James Weiland  1   6
Affiliations

Sight restoration reverses blindness-induced cross-modal functional connectivity changes between the visual and somatosensory cortex at rest

Negin Nadvar et al. Front Neurosci. .

Abstract

Resting-state functional connectivity (rsFC) has been used to assess the effect of vision loss on brain plasticity. With the emergence of vision restoration therapies, rsFC analysis provides a means to assess the functional changes following sight restoration. Our study demonstrates a partial reversal of blindness-induced rsFC changes in Argus II retinal prosthesis patients compared to those with severe retinitis pigmentosa (RP). For 10 healthy control (HC), 10 RP, and 7 Argus II subjects, four runs of resting-state functional magnetic resonance imaging (fMRI) per subject were included in our study. rsFC maps were created with the primary visual cortex (V1) as the seed. The rsFC group contrast maps for RP > HC, Argus II > RP, and Argus II > HC revealed regions in the post-central gyrus (PostCG) with significant reduction, significant enhancement, and no significant changes in rsFC to V1 for the three contrasts, respectively. These findings were also confirmed by the respective V1-PostCG ROI-ROI analyses between test groups. Finally, the extent of significant rsFC to V1 in the PostCG region was 5,961 in HC, 0 in RP, and 842 mm3 in Argus II groups. Our results showed a reduction of visual-somatosensory rsFC following blindness, consistent with previous findings. This connectivity was enhanced following sight recovery with Argus II, representing a reversal of changes in cross-modal functional plasticity as manifested during rest, despite the rudimentary vision obtained by Argus II patients. Future investigation with a larger number of test subjects into this rare condition can further unveil the profound ability of our brain to reorganize in response to vision restoration.

Keywords: blindness; cross-modal plasticity; fMRI; resting-state functional connectivity; retinal prosthesis; sight restoration.

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Conflict of interest statement

JW received research support from Second Sight Medical Products, Inc. outside of this study. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
Comparing rsFC between RP and HC. Group-level rsFC maps using V1 as the seed for HC (A), RP (B), and RP > HC contrast (C) were corrected for multiple comparisons using Gaussian Random Field Theory with an uncorrected voxel-level threshold of p < 0.001 and a cluster-level threshold of p < 0.05 FDR corrected for cluster size. Areas with lower rsFC to V1 covered regions of higher-level visual, primary/secondary somatosensory, motor, and parietal association cortex [blue blobs in (C)]. V1-to-PostCG ROI analysis (D) showed significantly lower rsFC effect size in RP vs. HC, using two-sample t-test [t (18) = –5.39, *p = 4 × 10–5].
FIGURE 2
FIGURE 2
Comparing rsFC between Argus and RP. Whole-brain rsFC map using V1 as the seed is calculated at the group level for RP (A) Argus II (B) and contrast Argus II > RP (C). rsFC maps were corrected for multiple comparisons using the Gaussian Random Field Theory with an uncorrected voxel-level threshold of p < 0.001 and a cluster-level threshold of p < 0.05 FDR corrected for cluster size. Areas with higher rsFC in Argus II than RP involved pre- and PostCG regions. The ROI-to-ROI rsFC analysis between V1 and PostCG (D) additionally showed significant [t (15) = 3.62, *p = 0.002] enhancement of this connectivity in Argus II compared with RP.
FIGURE 3
FIGURE 3
Comparing rsFC between Argus II and HC. Using the V1 seed, the group-level rsFC maps for Argus II (A), HC (B), and Argus II > HC contrast (C) were corrected for multiple comparisons using the Gaussian Random Field Theory with an uncorrected voxel-level threshold of p < 0.001 and a cluster-level threshold of p < 0.05 FDR corrected for cluster size. The contrast map shows that the areas depicting lower rsFC to V1 were found in some higher-level visual areas (shown in blue). The ROI-to-ROI rsFC analysis (D) revealed no significant difference in the V1-PostCG rsFC effect size between Argus II and HC groups, t (15) = –1.72, p = 0.1.
FIGURE 4
FIGURE 4
The extent of rsFC to V1. The volumetric extent in PostCG shows significant rsFC to V1 as the seed was calculated in mm3 (A). This spread of connectivity drastically reduced after blindness and partially increased following sight restoration in Argus II. Areas in the whole brain with significant rsFC to V1 for each of the three study groups are shown on the right (B). The dotted green area represents PostCG/primary somatosensory cortex boundary.
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