Rapid and reversible recruitment of early visual cortex for touch

Lotfi B Merabet, Roy Hamilton, Gottfried Schlaug, Jascha D Swisher, Elaine T Kiriakopoulos, Naomi B Pitskel, Thomas Kauffman, Alvaro Pascual-Leone, Lotfi B Merabet, Roy Hamilton, Gottfried Schlaug, Jascha D Swisher, Elaine T Kiriakopoulos, Naomi B Pitskel, Thomas Kauffman, Alvaro Pascual-Leone

Abstract

Background: The loss of vision has been associated with enhanced performance in non-visual tasks such as tactile discrimination and sound localization. Current evidence suggests that these functional gains are linked to the recruitment of the occipital visual cortex for non-visual processing, but the neurophysiological mechanisms underlying these crossmodal changes remain uncertain. One possible explanation is that visual deprivation is associated with an unmasking of non-visual input into visual cortex.

Methodology/principal findings: We investigated the effect of sudden, complete and prolonged visual deprivation (five days) in normally sighted adult individuals while they were immersed in an intensive tactile training program. Following the five-day period, blindfolded subjects performed better on a Braille character discrimination task. In the blindfold group, serial fMRI scans revealed an increase in BOLD signal within the occipital cortex in response to tactile stimulation after five days of complete visual deprivation. This increase in signal was no longer present 24 hours after blindfold removal. Finally, reversible disruption of occipital cortex function on the fifth day (by repetitive transcranial magnetic stimulation; rTMS) impaired Braille character recognition ability in the blindfold group but not in non-blindfolded controls. This disruptive effect was no longer evident once the blindfold had been removed for 24 hours.

Conclusions/significance: Overall, our findings suggest that sudden and complete visual deprivation in normally sighted individuals can lead to profound, but rapidly reversible, neuroplastic changes by which the occipital cortex becomes engaged in processing of non-visual information. The speed and dynamic nature of the observed changes suggests that normally inhibited or masked functions in the sighted are revealed by visual loss. The unmasking of pre-existing connections and shifts in connectivity represent rapid, early plastic changes, which presumably can lead, if sustained and reinforced, to slower developing, but more permanent structural changes, such as the establishment of new neural connections in the blind.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Study design.
Figure 1. Study design.
(a) Subjects were randomized to a blindfolded or non blindfolded group. Tactile behavioral assessments were obtained at day 1 and day 5. Both groups were immersed in an intensive tactile stimulation program that included formal Braille instruction. A subset of subjects participated in a neuroimaging study on day 1, day 3, day 5, and day 6 (i.e. 24 hours after blindfold removal) and a different subset of subjects participated in a TMS study (day 5 and day 6) (b) Photograph of a subject wearing the blindfold used in the study.
Figure 2. Behavioral results.
Figure 2. Behavioral results.
Group performance assessing touch thresholds with (a) von Frey Hairs and (b) tactile spatial acuity with JVP Domes over the course of the study. Performance is separated by right and left hand (blindfold: filled symbols, non blindfold: open symbols). Overall performance improved over the course of the study period in both the blindfold and blindfold groups.
Figure 3. Behavioral results.
Figure 3. Behavioral results.
Group performance on the Braille character discrimination task for both study groups over the course of the study. (a) Performance separated by right and left hand. Note that there is an overall improvement (decrease in error rate) over the five day period in both study groups. (b) Performance separated by day of study. Note that on day 1 of the study, no statistical significance in performance was observed between the groups however performance for the right (trained) hand was significantly better for the blindfold group compared to non blindfold controls after 5 days of blindfolding (* = p

Figure 4. Neuroimaging results.

(a) Differential tactile…

Figure 4. Neuroimaging results.

(a) Differential tactile activation maps contrasting the blindfold and non blindfold…

Figure 4. Neuroimaging results.
(a) Differential tactile activation maps contrasting the blindfold and non blindfold groups are shown for each fMRI session of the study. (b) A region of interest (ROI) was defined by the area of occipital activation found on day 5 in the group maps. The average differential tactile activity between groups in this ROI is plotted here in z-score units across days of the study. The difference between groups was significant on day 5, as expected from the definition of the ROI, but did not reach significance on any other day.

Figure 5. Effect of TMS on Braille…

Figure 5. Effect of TMS on Braille discrimination.

The effect of 1Hz rTMS on Braille…

Figure 5. Effect of TMS on Braille discrimination.
The effect of 1Hz rTMS on Braille discrimination ability (% error rate) is compared to baseline performance, sham stimulation and after a 10 min washout period. On day 5 (part a), rTMS (but not sham) had a significant effect on Braille character discrimination in the blindfold group (filled symbols) but not in the non blindfolded group (open symbols) (* = 
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Figure 4. Neuroimaging results.
Figure 4. Neuroimaging results.
(a) Differential tactile activation maps contrasting the blindfold and non blindfold groups are shown for each fMRI session of the study. (b) A region of interest (ROI) was defined by the area of occipital activation found on day 5 in the group maps. The average differential tactile activity between groups in this ROI is plotted here in z-score units across days of the study. The difference between groups was significant on day 5, as expected from the definition of the ROI, but did not reach significance on any other day.
Figure 5. Effect of TMS on Braille…
Figure 5. Effect of TMS on Braille discrimination.
The effect of 1Hz rTMS on Braille discrimination ability (% error rate) is compared to baseline performance, sham stimulation and after a 10 min washout period. On day 5 (part a), rTMS (but not sham) had a significant effect on Braille character discrimination in the blindfold group (filled symbols) but not in the non blindfolded group (open symbols) (* = 

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