Retinotopically specific reorganization of visual cortex for tactile pattern recognition

Abstract

Although previous studies have shown that Braille reading and other tactile discrimination tasks activate the visual cortex of blind and sighted people, it is not known whether this kind of crossmodal reorganization is influenced by retinotopic organization. We have addressed this question by studying "S," a visually impaired adult with the rare ability to read print visually and Braille by touch. S had normal visual development until 6 years of age, and thereafter severe acuity reduction due to corneal opacification, but no evidence of visual-field loss. Functional magnetic resonance imaging revealed that, in S's early visual areas, tactile information processing activated what would be the foveal representation for normally sighted individuals, and visual information processing activated what would be the peripheral representation. Control experiments showed that this activation pattern was not due to visual imagery. S's high-level visual areas, which correspond to shape- and object-selective areas in normally sighted individuals, were activated by both visual and tactile stimuli. The retinotopically specific reorganization in early visual areas suggests an efficient redistribution of neural resources in the visual cortex.

Figure 1

fMRI activation maps by visual stimuli in S. Statistical significance maps (thresholded at corrected p < 0.01) are shown on the flattened surface reconstruction of the posterior part of S’s brain. Red regions were activated by visually presented digits (left), letters (middle) and shapes (right) contrasting with blank intervals. S’s foveal and peripheral representations in V1 are indicated by blue and yellow arrows respectively.

Figure 2

fMRI activation maps by visual letter string and Braille in S. Statistical significance maps (thresholded at corrected p < 0.01) are shown on the flattened surface reconstruction of the posterior part of S’s brain. Upper left: Red regions were activated by visual letter strings contrasting with blank intervals. Upper middle: Green regions were activated by Braille contrasting with blank intervals. Upper right: Blue regions were activated by both visual letter strings and Braille contrasting with blank intervals. Lower left: Visual letter string and Braille conditions were contrasted with each other. Red regions showed higher response to visual letter strings than to Braille, and green regions showed the opposite. S’s foveal and peripheral representations in V1 are indicated by blue and yellow arrows respectively. Lower right: BOLD signals evoked by Braille and visual letter strings relative to blank intervals in three V1 subregions (Talairach coordinates shown in parentheses) – fovea (left: −21, −95,−4; right: 17, −95, −8), parafovea (left: −6, −94, −9; right: 4, −92, −7) and periphery (left: −5, −75, −6; right: 3, −75, −1). The three subregions are delineated by blue curves in the lower left panel. Error bars denote 1 standard error of mean across scans.

Figure 3

fMRI activation maps by visual and tactile shapes in S and two age-matched control participants. Statistical significance maps (thresholded at corrected p < 0.01) are shown on the flattened surface reconstruction of the posterior part of participants’ brains. Left: Visual shape and tactile shape conditions were contrasted with each other. Red regions showed higher response to visual shape than to tactile shape, and green regions showed the opposite. Participants’ foveal and peripheral representations in V1 are indicated by blue and yellow arrows respectively. Right: BOLD signals evoked by tactile and visual shapes relative to blank intervals in three V1 subregions (fovea, parafovea and periphery), which are delineated by blue curves on the flattened surfaces. Error bars denote 1 standard error of mean across scans.

Figure 4

fMRI activation maps by visual imagery and Braille in S. Statistical significance maps (thresholded at corrected p < 0.01) are shown on the flattened surface reconstruction of the posterior part of S’s brain. Left: Red regions were activated by visual imagery contrasting with blank intervals. Middle: Green regions were activated by Braille contrasting with blank intervals. Right: Blue regions were activated by both visual imagery and Braille contrasting with blank intervals. S’s foveal and peripheral representations in V1 are indicated by blue and yellow arrows respectively.