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Massive cortical reorganization in sighted Braille readers

  1. Katarzyna Siuda-Krzywicka
  2. Łukasz Bola
  3. Małgorzata Paplińska
  4. Ewa Sumera
  5. Katarzyna Jednoróg
  6. Artur Marchewka
  7. Magdalena W Śliwińska
  8. Amir Amedi
  9. Marcin Szwed  Is a corresponding author
  1. Jagiellonian University, Poland
  2. Institut du Cerveau et de la Moelle épinière (ICM), France
  3. Nencki Institute of Experimental Biology, Poland
  4. Academy of Special Education in Warsaw, Poland
  5. Institute for the Blind and Partially Sighted Children in Krakow, Poland
  6. University College London, United Kingdom
  7. The Hebrew University of Jerusalem, Israel
  8. Sorbonne Universite´s, UPMC Univ Paris 06, Institut de la Vision, France
Research Article
Cite this article as: eLife 2016;5:e10762 doi: 10.7554/eLife.10762
9 figures and 4 tables

Figures

Figure 1 with 3 supplements
Experimental design and brain regions activated by tactile Braille reading.

(A) The study consisted of two identical MRI sessions performed before and after an intensive 9-month tactile Braille course. In the fMRI experiment (B), subjects viewed visual words written in the regular alphabet and Braille words displayed on a screen (visual Braille) and touched tactile Braille words. As a control, they viewed strings of hash signs and meaningless pseudo-Braille dots and touched meaningless pseudo-Braille dots. The experiment used a block design (C); after each block, the subjects lifted their fingers from the table on which the tactile stimuli were presented. A new board with tactile stimuli was then placed on the table, the subjects put their fingers down, and a new block began. (D) Compared to the tactile control, tactile reading after the course evoked activations in the visual word form area (VWFA), the lateral occipital area and other areas (Tables 13). Similar areas were activated when we computed (E) an interaction between tactile Braille/tactile control stimuli and the before- and after-course time points and for (F) an interaction between tactile Braille/tactile control vs. visual reading/visual control stimuli and the before- and after-course time points. The latter confirmed that the increase in visual cortex activation after the course was specific for tactile reading. (G) When we modeled the modulation of fMRI responses to tactile Braille by the subjects’ reading speed, the only significant whole-brain correlate with tactile reading proficiency was found in the ventral visual system (k=103 voxels). Voxel-wise thresholds: (D) p<0.001; (E–G) p<0.005; Cluster-wise thresholds: (D–F) p<0.05; (G) uncorrected, k=100 voxels. For control fMRI experiment, see Figure 1—figure supplement 1 for procedures and Figure 1—figure supplement 2 for results. For supplementary fMRI results, see Figure 1—figure supplement 3.

https://doi.org/10.7554/eLife.10762.003
Figure 1—figure supplement 1
Control experiment stimuli and procedures.

(A) In the control imagery experiment, subjects were asked to read or imagine words in the regular alphabet or in visual and tactile Braille or to touch or imagine everyday objects. (B) Similar to the Main experiment (Figure 1C), stimuli in the control experiment were presented in blocks. In each block, after a sound indicating they should lift their fingers from the fiberglass table, subjects heard an auditory instruction informing them about the next task (read/touch or imagine). After 8–12 s, a sound signaled them to put their fingers down. Subjects began to read/touch/imagine after 4–7 s, when they heard the name of the stimulus to be read/touched or imagined. (C) Blocks in the main experiment consisted of 8 stimuli: words, control stimuli or fixation dots in the case of tactile conditions. Each stimulus was presented for 3500 ms and was followed by a 500 ms fixation dot, which was accompanied with a metronome tick indicating the change of the stimulus for the tactile conditions. (D) Blocks in the control imagery experiment consisted of 6 stimuli. After a 500 ms fixation dot, an auditory recording of the name of the subsequent stimulus was presented, either with (read/touch task) or without the stimulus (imagery task). For object stimuli, the block duration was the same, but only one stimulus was presented per block.

https://doi.org/10.7554/eLife.10762.007
Figure 1—figure supplement 2
Main results of the control experiment.

(A) Imagining Tactile Braille vs. rest elicited activity in motor/somatosensory areas, the cerebellum and left occipital areas, including the VWFA. Similar results were found for (B) Visual Braille imagery. However, (C) Tactile Braille imagery more strongly activated the somatosensory and motor areas and mesial frontal regions. (D) In addition to the parietal and sensory-motor activations, touching objects vs. rest resulted in activity in lateral occipital areas bilaterally. Thresholds: A,B p = 0.001 voxel-wise, p=0.05 cluster-wise; C, D p=0.005 voxel-wise, p=0.05 cluster wise.

https://doi.org/10.7554/eLife.10762.008
Figure 1—figure supplement 3
Supplementary fMRI results

(A) Visual word reading contrasted with the control task before the course activated left ventral occipital areas, including the VWFA and the middle occipital gyrus. (B) Visual Braille reading vs. control before the course elicited robust activation in occipital areas predominantly on the left side, including the VWFA and the inferior and middle occipital gyrus. Other activations included the left inferior and middle frontal gyri, the precuneus, the middle temporal gyrus and the left STS. (C) For visual Braille reading, the only increases in activation observed after the course were in the default mode network (mesial frontal cortex and bilateral temporal and parietal regions). (D) Similar to Braille word reading speed (Figure 1G), single-letter recognition speed modulated the activity for tactile Braille reading in the left occipital areas, including V1 and the fusiform gyrus (VWFA). Thresholds: A-C p=0.005 voxel-wise, p=0.05 cluster-wise; D p = 0.005 voxel-wise, uncorrected for cluster size.

https://doi.org/10.7554/eLife.10762.009
Response similarity and region-of-interest (ROI) analyses.

Response similarity analysis showed that (A) the activity patterns for both Braille alphabets were the most similar, whereas the patterns for tactile Braille and visual words differed the most. In the VWFA (B), the response to tactile Braille words changed from a de-activation to a positive activation. The VWFA also showed strong responses to visual Braille words; these, however, did not change significantly following the Braille course. The lateral occipital area (C) also saw the emergence of responses to tactile Braille words similar to the VWFA. In contrast, there was no effect of the Braille course in the somatosensory cortex (D). A drop in activation for the control condition was salient in the intraparietal sulcus (F), in which the activation to tactile Braille words remained unchanged, whereas the activation to the tactile control dropped to zero. Arrow thickness and the distance between scripts in (A) are proportional to correlation strength. (***) p<0.001; (**) p<0.01; (*) p<0.05. Dashed lines denote interactions. All ROIs are in the left hemisphere.

https://doi.org/10.7554/eLife.10762.010
Following the tactile Braille course, the VWFA increased its resting-state connectivity with the somatosensory cortex while decreasing its coupling with other visual areas and the motor cortex.

The connectivity between the VWFA and the somatosensory cortex was behaviorally relevant for tactile Braille reading. (A) Functional connectivity of the VWFA after the tactile Braille course relative to the before-course scan. Red represents increased correlation, and blue represents decreased correlation. The VWFA seed is marked in pink. Thresholds: p = 0.001 voxel-wise, p = 0.05 cluster-wise. (B) Correlation between after-course VWFA – left S1 functional connectivity and progress in tactile Braille reading speed in the last month of the course.

https://doi.org/10.7554/eLife.10762.011
TMS applied to the Visual Word Form Area selectively decreased the accuracy of Braille word reading.

(A) Illustration of the experimental design. Subjects read tactile Braille words or pseudowords and performed a lexical decision task based on them. In half of the trials, repetitive TMS was applied. The VWFA and two control sites (lateral occipital area and vertex) were tested in separate runs. (B) Mean accuracy of reading Braille words and pseudowords is shown for the VWFA and for both control sites, for the TMS and no TMS conditions separately. (*) p=0.016.

https://doi.org/10.7554/eLife.10762.012
Author response image 1
SI and SII activity for tactile stimuli before and after the course.
https://doi.org/10.7554/eLife.10762.014
Author response image 2
Possible contributions to the decrease of activity for tactile stimuli.

Two contributions to interaction for tactile stimuli (example for Visual Word Form Area, based on Figure 2).

https://doi.org/10.7554/eLife.10762.015
Author response image 3
LOA activates when French, Chinese-naive native speakers see Chinese characters.
https://doi.org/10.7554/eLife.10762.016
Author response image 4
The distribution of final Braille reading speed (words per minute, WPM).
https://doi.org/10.7554/eLife.10762.017
Author response image 5
Tactile Braille modulated by reading speed after course (outlier excluded).

Voxel-wise p=0.005, k=50.

https://doi.org/10.7554/eLife.10762.018

Tables

Table 1

Summary of main activations for tactile Braille reading contrasted with control conditions and visual reading across the tactile Braille course

https://doi.org/10.7554/eLife.10762.004
ContrastVoxel-wise
p threshold
RegionBAHemisphereZ scoreCluster
size
MNI coordinates
Tactile Braille vs. Control after trainingp = 0.001Fusiform Gyrus (VWFA)37Left5.1875-45-58-12
Inferior Frontal Gyrus9Left5.15467-42227
46Left3.4397-423211
47Right4.4811133263
45Right3.8266601123
Medial Frontal Gyrus6Left4.84467-6263
Superior Occipital Gyrus39Right5.0820833-7327
Precuneus7Right4.6320821-7047
7Left5.01401-21-7343
Inferior Parietal Lobule40Left4.55401-30-4343
40Right4.249345-3447
Middle Frontal Gyrus46Right3.55111422919
Cerebellum*Right4.3627427-64-24
Insula13Left4.3497-33233
Tactile Braille vs.
Control x after > before training
p = 0.005Superior Temporal Gyrus22Right5.4922548-25-1
Fusiform Gyrus (VWFA)37Left4.54606-45-61-12
Middle Frontal Gyrus6Left4.481031-45-143
Inferior Frontal Gyrus45Left4.221031-33267
47Right4.283393926-1
Insula13Right3.9533237
Middle Temporal Gyrus22Left4.13183-51-437
37Left3.92606-45-64-9
Superior Temporal Gyrus22Left3.62183-63-4011
22Left3.43-57-5211
Precuneus7Left4.10606-18-6743
7Right3.7871324-7331
Cerebellum*Right4.0171327-64-28
Middle Occipital Gyrus37Right3.8571339-70-5
Tactile Braille vs.Control – Visual
Reading vs.Control x after > before training
p = 0.005Inferior Frontal Gyrus9Left5.602469-45523
Superior Frontal Gyrus6Left5.48-3563
Precentral Gyrus6Left5.39-45-451
Cerebellum*Right4.7811546-79-36
*Left3.49-9-82-20
Fusiform Gyrus (VWFA)37Left4.051154-45-61-12
Inferior Temporal Gyrus37Left3.81-48-70-5
Inferior Parietal Lobule40Left4.21532-33-4951
Precuneus19Left4.08-27-7331
7Right4.3173827-7031
Cuneus30Right4.0227-763
Table 2

Summary of main activations for visual reading and visual Braille reading contrasted with control conditions across the tactile Braille course.

https://doi.org/10.7554/eLife.10762.005
ContrastVoxel-wise p tresholdRegionBAHemisphereZ scoreCluster sizeMNI coordinates
Visual words vs.
Control before training
p = 0.005Inferior Temporal Gyrus37Left7.43359-42-70-9
Fusiform Gyrus (VWFA)37Left5.02-42-52-16
Middle Occipital Gyrus18Left3.17-24-943
Visual Braille vs
Control before training
p = 0.005Precuneus19Right5.83176730-6439
Middle Temporal Gyrus37Right5.5845-64-9
Middle Occipital Gyrus19Right5.1948-76-1
19Left5.601640-45-85-1
Inferior Frontal Gyrus9Left5.811374-42227
Middle Frontal Gyrus6Left5.20-30-455
Precentral Gyrus6Left5.11-51-439
Fusiform Gyrus (VWFA)37Left5.621640-45-58-12
Inferior Occipital Gyrus19Left5.59-42-73-9
Visual Braille vs.
Control x after > before training
p = 0.005Precuneus7Right4.887976-6435
31Left4.29-9-6127
Middle Temporal Gyrus39Right4.0427551-6423
39Left4.00297-45-6727
39Left3.86-54-7023
Superior Temporal Gyrus13Right3.8327545-4923
Inferior Parietal Lobule40Right2.7860-5243
Superior Parietal Lobule7Left3.45297-45-6751
Medial Frontal Gyrus10Left3.791184-362-1
10Left3.73-950-5
Superior Frontal Gyrus8Right3.6494743
Table 3

Summary of activations for behavioural measures modulating the activity in reading.

https://doi.org/10.7554/eLife.10762.006
ContrastVoxel-wise p tresholdRegionBAHemisphereZ scoreCluster sizeMNI coordinates
Tactile reading speed
x activations in Tactile
Braille after training
p = 0.005Inferior Occipital Gyus19Left3.69103-45-76-13
Middle Occipital Gyrus19Left3.65103-39-85-1
Tactile letter recognition
x activations in Tactile Braille
after the training
p = 0.005Middle Occipital Gyrus19Left3.62170-48-73-12
19Left3.21170-39-85-1
Lingual Gyrus18Left3.42170-15-85-16
Fusiform Gyrus (VWFA)19Left3.17170-36-82-20
37Right3.176336-49-20
Inferior Occipital Gyrus18Left3.04170-39-85-16
Cerebellum*Right3.006330-58-12
Cuneus17Right3.014418-857
18Right2.76446-917
Table 4

Summary of main activations in the control experiment.

https://doi.org/10.7554/eLife.10762.013
ContrastVoxel-wise
p treshold
RegionBAHemisphereZ scoreCluster sizeMNI coordinates
Tactile Braille Imagine vs
Rest after course
p = 0.001Cerebellum*Right>851927-67-24
*Left3.43152-42-64-28
Inferior Frontal Gyrus9Left>88307-57827
Inferior Parietal Lobule40Left>8-39-4343
Medial Frontal Gyrus6Left>8-3-163
Middle Frontal Gyrus46Left>8-423223
Postcentral Gyrus3Left>8-57-1923
Precentral Gyrus6Left>8-39-759
Superior Temporal Gyrus22Left>8-548-1
40Right>839-4047
Middle Occipital Gyrus19Left6.60152-54-61-12
Fusiform Gyrus (VWFA)37Left5.95-45-61-12
Inferior Temporal Gyrus20Left4.22-51-49-16
Visual Braille Imagine vs Rest after coursep = 0.001Inferior Parietal Lobule40Left>83062-39-4343
40Right>8123339-4047
Middle Frontal Gyrus6Left>83062-24-451
6Right7.56123327-451
Precentral Gyrus6Left>83062-54239
Cerebellum*Right7.6313430-67-24
Inferior Frontal Gyrus44Right7.41123354823
Middle Occipital Gyrus19Left7.01119-48-58-12
Fusiform Gyrus (VWFA)37Left6.38-45-58-12
Superior Temporal Gyrus42Right4.8011366-257
Tactile Braille Imagine vs
Visual braille imagine after course
p = 0.005Inferior Parietal Lobule40Left6.846602-57-2223
40Right4.7266-3731
Cerebellum*Right6.7596224-52-24
Superior Frontal Gyrus10Left6.41672-305019
10Right5.356602274419
Precentral Gyrus4Left6.21-33-1955
Postcentral Gyrus3Right5.7260-1923
2Left4.88-57-2547
Middle Frontal Gyrus10Right5.21335015
9Left4.86672-422635
Objects Touchp = 0.005Cerebellum*Right>8121124-52-24
*Left>8-21-55-24
Postcentral Gyrus3Right>8541248-2251
Precentral Gyrus6Right>836-1359
4Left>8-39-2259
Middle Occipital Gyrus19Left5.1885-51-64-9
37Right4.77121151-6412

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