We previously demonstrated that using a sensory substitution device (SSD) for one week, tactile stimulation results in faster activation of lateral occipital complex in blind children than in seeing controls.
Objective:
We used long-term haptic tactile stimulation training with an SSD to test if it results in stable cross-modal reassignment of visual pathways after six months, to provide high level processing of tactile semantic content.
Methods:
We enrolled 12 blind and 12 sighted children. The SSD transforms images to a stimulation matrix in contact with the dominant hand. Subjects underwent twice-daily training sessions, 5 days/week for six months. Children were asked to describe line orientation, name letters, and read words. ERP sessions were performed at baseline and 6 months to analyze the N400 ERP component and reaction times (RT). N400 sources were estimated with Low Resolution Electromagnetic Tomography (LORETA). SPM8 was used to make population-level inferences.
Results:
We found no group differences in RTs, accuracy of identifications, N400 latencies or distributions with the line task at 1 week or at 6 months. RTs on the letter recognition task were also similar. After 6 months, behavioral training increased accurate letter identification in both seeing and blind children (Chi 2 = 11906.934, p = 0.000), but the increase was larger in blind children (Chi 2 = 8.272, p = 0.004). Behavioral training shifted peak N400 amplitude to left occipital and bilateral parietal cortices in blind children, but to left precentral and postcentral and bilateral occipital cortices in sighted controls.
Conclusions:
Blind children learn to recognize SSD-delivered letters better than seeing controls and had greater N400 amplitude in the occipital region. To the best of our knowledge, our results provide the first published example of standard letter recognition (not Braille) by children with blindness using a tactile delivery system.
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References
1.
Amedi, A., Raz, N., Azulay, H., Malach, R., & Zohary, E. (2010). Cortical activity during tactile exploration of objects in blind and sighted humans.Restorative Neurology and Neuroscience, 28(2), 143–156. https://doi.org/10.3233/RNN-2010-0503
2.
Amedi, A., Raz, N., Pianka, P., Malach, R., & Zohary, E. (2003). Early ``visual'' cortex activation correlates with superior verbal memory performance in the blind.Nature Neuroscience, 6(7), 758–766. https://doi.org/10.1038/nn1072
Bhattacharjee, A., Ye, A.J., Lisak, J.A., Vargas, M.G., & Goldreich, D. (2010). Vibrotactile masking experiments reveal accelerated somatosensory processing in congenitally blind braille readers.The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 30(43), 14288–14298. https://doi.org/10.1523/JNEUROSCI.1447-10.2010
5.
Brunet, E., Sarfati, Y., Hardy-Baylé, M.C., & Decety, J. (2000). A PET investigation of the attribution of intentions with a nonverbal task.NeuroImage, 11(2), 157–166. https://doi.org/10.1006/nimg.1999.0525
6.
Brunyé, T.T., Moran, J.M., Holmes, A., Mahoney, C.R., & Taylor, H.A. (2017). Non-invasive brain stimulation targeting the right fusiform gyrus selectively increases working memory for faces.Brain and Cognition, 113, 32–39. https://doi.org/10.1016/j.bandc.2017.01.006
7.
Burton, H., Diamond, J.B., & McDermott, K.B. (2003). Dissociating cortical regions activated by semantic and phonological tasks: a FMRI study in blind and sighted people.Journal of Neurophysiology, 90(3), 1965–1982. https://doi.org/10.1152/jn.00279.2003
8.
Burton, H., McLaren, D.G., & Sinclair, R.J. (2006). Reading embossed capital letters: an fMRI study in blind and sighted individuals.Human Brain Mapping, 27(4), 325–339. https://doi.org/10.1002/hbm.20188
9.
Burton, H., Sinclair, R.J., & Dixit, S. (2010). Working memory for vibrotactile frequencies: comparison of cortical activity in blind and sighted individuals.Human Brain Mapping, 31(11), 1686–1701. https://doi.org/10.1002/hbm.20966
10.
Carbonell, F., Galán, L., Valdés, P., Worsley, K., Biscay, R.J., Díaz-Comas, L., … & Parra, M. (2004). Random field-union intersection tests for EEG/MEG imaging.NeuroImage, 22(1), 268–276. https://doi.org/10.1016/j.neuroimage.2004.01.020
11.
Cohen, L., Dehaene, S., Vinckier, F., Jobert, A., & Montavont, A. (2008). Reading normal and degraded words: Contribution of the dorsal and ventral visual pathways.NeuroImage, 40(1), 353–366. https://doi.org/10.1016/j.neuroimage.2007.11.036
12.
Davenport, T., & Coulson, S. (2013). Hemispheric asymmetry in interpreting novel literal language: An event-related potential study.Neuropsychologia, 51(5), 907–921. https://doi.org/10.1016/j.neuropsychologia.2013.01.018
13.
Deacon, D., Hewitt, S., Yang, C., & Nagata, M. (2000). Event-related potential indices of semantic priming using masked and unmasked words: evidence that the N400 does not reflect a post-lexical process.Brain Research. Cognitive Brain Research, 9(2), 137–146.
14.
Deacon, D., Shelley-Tremblay, J.F., Ritter, W., & Dynowska, A. (2013). Electrophysiological evidence for the action of a center-surround mechanism on semantic processing in the left hemisphere.Frontiers in Psychology, 4, 936. https://doi.org/10.3389/fpsyg.2013.00936
15.
Feldman, D.E., & Brecht, M. (2005). Map plasticity in somatosensory cortex.Science (New York, N.Y.), 310(5749), 810–815. https://doi.org/10.1126/science.1115807
16.
Fiehler, K., & Rösler, F. (2010). Plasticity of multisensory dorsal stream functions: evidence from congenitally blind and sighted adults.Restorative Neurology and Neuroscience, 28(2), 193–205. https://doi.org/10.3233/RNN-2010-0500
17.
Flowers, D.L., Jones, K., Noble, K., VanMeter, J., Zeffiro, T.A., Wood, F.B., & Eden, G.F. (2004). Attention to single letters activates left extrastriate cortex.NeuroImage, 21(3), 829–839. https://doi.org/10.1016/j.neuroimage.2003.10.002
18.
Frey, S., Zlatkina, V., & Petrides, M. (2009). Encoding touch and the orbitofrontal cortex.Human Brain Mapping, 30(2), 650–659. https://doi.org/10.1002/hbm.20532
19.
Friederici, A.D. (2004). Event-related brain potential studies in language.Current Neurology and Neuroscience Reports, 4(6), 466–470.
20.
Frings, C., Amendt, A., & Spence, C. (2011). When seeing doesn't matter: assessing the after-effects of tactile distractor processing in the blind and the sighted.Journal of Experimental Psychology. Human Perception and Performance, 37(4), 1174–1181. https://doi.org/10.1037/a0022336
21.
Frishkoff, G.A., Tucker, D.M., Davey, C., & Scherg, M. (2004). Frontal and posterior sources of event-related potentials in semantic comprehension.Brain Research. Cognitive Brain Research, 20(3), 329–354. https://doi.org/10.1016/j.cogbrainres.2004.02.009
22.
Garrett, A.S., Flowers, D.L., Absher, J.R., Fahey, F.H., Gage, H.D., Keyes, J.W., & Wood, F.B. (2000). Cortical activity related to accuracy of letter recognition.NeuroImage, 11(2), 111–123. https://doi.org/10.1006/nimg.1999.0528
23.
Goldreich, D., & Kanics, I.M. (2003). Tactile acuity is enhanced in blindness.The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 23(8), 3439–3445.
24.
Grossi, G., Savill, N., Thomas, E., & Thierry, G. (2012). Electrophysiological cross-language neighborhood density effects in late and early english-welsh bilinguals.Frontiers in Psychology, 3, 408. https://doi.org/10.3389/fpsyg.2012.00408
25.
Gurtubay-Antolin, A., & Rodríguez-Fornells, A. (2017). Neurophysiological evidence for enhanced tactile acuity in early blindness in some but not all haptic tasks.NeuroImage, 162, 23–31. https://doi.org/10.1016/j.neuroimage.2017.08.054
26.
Hata, M., Homae, F., & Hagiwara, H. (2011). Semantic relatedness between words in each individual brain: an event-related potential study.Neuroscience Letters, 501(2), 72–77. https://doi.org/10.1016/j.neulet.2011.06.044
Kupers, R., & Ptito, M. (2014). Compensatory plasticity and cross-modal reorganization following early visual deprivation.Neuroscience and Biobehavioral Reviews, 41, 36–52. https://doi.org/10.1016/j.neubiorev.2013.08.001
Lage-Castellanos, A., Martínez-Montes, E., Hernández-Cabrera, J.A., & Galán, L. (2010). False discovery rate and permutation test: an evaluation in ERP data analysis.Statistics in Medicine, 29(1), 63–74. https://doi.org/10.1002/sim.3784
31.
Legge, G.E., Madison, C., Vaughn, B.N., Cheong, A.M.Y., & Miller, J.C. (2008). Retention of high tactile acuity throughout the life span in blindness.Perception & Psychophysics, 70(8), 1471–1488. https://doi.org/10.3758/PP.70.8.1471
32.
Merabet, L.B., Hamilton, R., Schlaug, G., Swisher, J.D., Kiriakopoulos, E.T., Pitskel, N.B., … & Pascual-Leone, A. (2008). Rapid and reversible recruitment of early visual cortex for touch.PloS One, 3(8), e3046. https://doi.org/10.1371/journal.pone.0003046
33.
Merabet, L.B., & Pascual-Leone, A. (2010). Neural reorganization following sensory loss: the opportunity of change.Nature Reviews. Neuroscience, 11(1), 44–52. https://doi.org/10.1038/nrn2758
34.
Murray, M.M., Lewkowicz, D.J., Amedi, A., & Wallace, M.T. (2016). Multisensory Processes: A Balancing Act across the Lifespan.Trends in Neurosciences, 39(8), 567–579. https://doi.org/10.1016/j.tins.2016.05.003
Ortells, J.J., Kiefer, M., Castillo, A., Megías, M., & Morillas, A. (2016). The semantic origin of unconscious priming: Behavioral and event-related potential evidence during category congruency priming from strongly and weakly related masked words.Cognition, 146, 143–157. https://doi.org/10.1016/j.cognition.2015.09.012
37.
Ortiz Alonso, T., Santos, J.M., Ortiz Terán, L., Borrego Hernández, M., Poch Broto, J., & de Erausquin, G.A. (2015). Differences in Early Stages of Tactile ERP Temporal Sequence (P100) in Cortical Organization during Passive Tactile Stimulation in Children with Blindness and Controls.PloS One, 10(7), e0124527. https://doi.org/10.1371/journal.pone.0124527
38.
Ortiz, T., Poch, J., Santos, J.M., Requena, C., Martínez, A.M., Ortiz-Terán, L., … & Pascual-Leone, A. (2011). Recruitment of Occipital Cortex during Sensory Substitution Training Linked to Subjective Experience of Seeing in People with Blindness.PLoS ONE, 6(8), e23264. https://doi.org/10.1371/journal.pone.0023264
39.
Pascual-Marqui, R.D., Michel, C.M., & Lehmann, D. (1994). Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain.International Journal of Psychophysiology: Official Journal of the International Organization of Psychophysiology, 18(1), 49–65.
40.
Qu, J., Qian, L., Chen, C., Xue, G., Li, H., Xie, P., & Mei, L. (2017). Neural Pattern Similarity in the Left IFG and Fusiform Is Associated with Novel Word Learning.Frontiers in Human Neuroscience, 11, 424. https://doi.org/10.3389/fnhum.2017.0042410.3389/fnhum.2017.00424.
Raz, N., Amedi, A., & Zohary, E. (2005). V1 activation in congenitally blind humans is associated with episodic retrieval.Cerebral Cortex (New York, N.Y.: 1991), 15(9), 1459–1468. https://doi.org/10.1093/cercor/bhi026
43.
Reuter, E.-M., Voelcker-Rehage, C., Vieluf, S., & Godde, B. (2012). Touch perception throughout working life: effects of age and expertise.Experimental Brain Research, 216(2), 287–297. https://doi.org/10.1007/s00221-011-2931-5
44.
Reuter, E.-M., Voelcker-Rehage, C., Vieluf, S., Winneke, A.H., & Godde, B. (2014). Extensive occupational finger use delays age effects in tactile perception-an ERP study.Attention, Perception & Psychophysics, 76(4), 1160–1175. https://doi.org/10.3758/s13414-014-0634-2
45.
Ricciardi, E., Bonino, D., Pellegrini, S., & Pietrini, P. (2014). Mind the blind brain to understand the sighted one! Is there a supramodal cortical functional architecture??Neuroscience and Biobehavioral Reviews, 41, 64–77. https://doi.org/10.1016/j.neubiorev.2013.10.006
46.
Röder, B., Teder-Sälejärvi, W., Sterr, A., Rösler, F., Hillyard, S.A., & Neville, H.J. (1999). Improved auditory spatial tuning in blind humans.Nature, 400(6740), 162–166. https://doi.org/10.1038/22106
47.
RohautB, & NaccacheL.Disentangling conscious from unconscious cognitive processing with event-related EEG potentials.Rev Neurol (Paris).2017Jul-Aug;173(7-8):521-528. doi:10.1016/j.neurol.2017.08.001.Epub 2017 Aug 24.
Sathian, K., & Stilla, R. (2010). Cross-modal plasticity of tactile perception in blindness.Restorative Neurology and Neuroscience, 28(2), 271–281. https://doi.org/10.3233/RNN-2010-0534
Striem-Amit, E., Cohen, L., Dehaene, S., & Amedi, A. (2012). Reading with sounds: sensory substitution selectively activates the visual word form area in the blind.Neuron, 76(3), 640–652. https://doi.org/10.1016/j.neuron.2012.08.026
52.
Stronks, H.C., Nau, A.C., Ibbotson, M.R., & Barnes, N. (2015). The role of visual deprivation and experience on the performance of sensory substitution devices.Brain Research, 1624, 140–152. https://doi.org/10.1016/j.brainres.2015.06.033
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.NeuroImage, 15(1), 273–289. https://doi.org/10.1006/nimg.2001.0978
55.
Veispak, A., Boets, B., & Ghesquière, P. (2013). Differential cognitive and perceptual correlates of print reading versus braille reading.Research in Developmental Disabilities, 34(1), 372–385. https://doi.org/10.1016/j.ridd.2012.08.012
Wong, M., Gnanakumaran, V., & Goldreich, D. (2011). Tactile spatial acuity enhancement in blindness: evidence for experience-dependent mechanisms.The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 31(19), 7028–7037. https://doi.org/10.1523/JNEUROSCI.6461-10.2011JNEUROSCI.6461-10.2011
