Neural processing underlying tactile microspatial discrimination in the blind: A functional magnetic resonance imaging study

Journal of Vision

Volumn 8, Issue 10, 2008, Pages

  Stilla, Randall ^a   Hanna, Rebecca ^a   Hu, Xiaoping ^b   Mariola, Erica ^a   Deshpande, Gopikrishna ^b   Sathian, Krish ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Emory University   (United States)

^c ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Connectivity analysis; Plasticity; Somatosensory; Spatial cognition; Tactile spatial acuity; Visual cortex

Indexed keywords

ADULT; AGE; ARTICLE; BLINDNESS; BRAIN MAPPING; DEPTH PERCEPTION; FEMALE; HEMISPHERIC DOMINANCE; HUMAN; MALE; MIDDLE AGED; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; SOMATOSENSORY CORTEX; STATISTICS; STIMULATION; TEMPORAL LOBE; TOUCH; VISUAL CORTEX;

ADULT; AGE FACTORS; BLINDNESS; BRAIN MAPPING; FEMALE; FUNCTIONAL LATERALITY; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; PHYSICAL STIMULATION; SOMATOSENSORY CORTEX; SPACE PERCEPTION; TEMPORAL LOBE; TOUCH PERCEPTION; VISUAL CORTEX;

EID: 58149528231     PISSN: None     EISSN: 15347362     Source Type: Journal    
DOI: 10.1167/8.10.13     Document Type: Article

References (68)

1. Alho, K., Kujala, T., Paavilainen, P., Summala, H., & Näätänen, R. (1993). Auditory processing in visual brain areas of the early blind: Evidence from event-related potentials. Electroencephalography and Clinical Neurophysiology, 86, 418-427.
2. Amedi, A., Floel, A., Knecht, S., Zohary, E., & Cohen, L. G. (2004). Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects. Nature Neuroscience, 7, 1266-1270.
3. 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, 758-766.
4. Büchel, C., Price, C., Frackowiak, R. S., & Friston, K. (1998). Different activation patterns in the visual cortex of late and congenitally blind subjects. Brain, 121, 409-419.
5. Büchel, C., Price, C., & Friston, K. (1998). A multimodal language region in the ventral visual pathway. Nature, 394, 274-277.
6. Burton, H. (2003). Visual cortex activity in early and late blind people. Journal of Neuroscience, 23, 4005-4011.
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, 1965-1982.
8. Burton, H., & McLaren, D. G. (2006). Visual cortex activation in late-onset, Braille naive blind individuals: An fMRI study during semantic and phonological tasks with heard words. Neuroscience Letters, 392, 38-42.
9. 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, 325-339.
10. Burton, H., Sinclair, R. J., & McLaren, D. G. (2004). Cortical activity to vibrotactile stimulation: An fMRI study in blind and sighted individuals. Human Brain Mapping, 23, 210-228.
11. Burton, H., Snyder, A. Z., Conturo, T. E., Akbudak, E., Ollinger, J. M., & Raichle, M. E. (2002). Adaptive changes in early and late blind: A fMRI study of Braille reading. Journal of Neurophysiology, 87, 589-607.
12. Burton, H., Snyder, A. Z., Diamond, J. B., & Raichle, M. E. (2002). Adaptive changes in early and late blind: A fMRI study of verb generation to heard nouns. Journal of Neurophysiology, 88, 3359-3371.
13. Cohen, L. G., Celnik, P., Pascual-Leone, A., Corwell, B., Falz, L., Dambrosia, J., et al. (1997). Functional relevance of cross-modal plasticity in blind humans. Nature, 389, 180-183.
14. Cohen, L. G., Weeks, R. A., Sadato, N., Celnik, P., Ishii, K., & Hallett, M. (1999). Period of susceptibility for crossmodal plasticity in the blind. Annals of Neurology, 45, 451-460.
15. Deshpande, G., Hu, X., Stilla, R., & Sathian, K. (2008). Effective connectivity during haptic perception: A study using Granger causality analysis of functional magnetic resonance imaging data. Neuroimage, 40, 1807-1814.
16. Duvernoy, H. M. (1999). The human brain. Surface, blood supply and three-dimensional sectional anatomy. New York: Springer.
17. Eickhoff, S. B., Grefkes, C., Zilles, K., & Fink, G. R. (2007). The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. Cerebral Cortex, 17, 1800-1811.
18. Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., & Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magnetic Resonance in Medicine, 33, 636-647.
19. Garg, A., Schwartz, D., & Stevens, A. A. (2007). Orienting auditory spatial attention engages frontal eye fields and medial occipital cortex in congenitally blind humans. Neuropsychologia, 45, 2307-2321.
20. Genovese, C. R., Lazar, N. A., & Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage, 15, 870-878.
21. Geyer, S., Schleicher, A., & Zilles, K. (1999). Areas 3a, 3b, and 1 of human primary somatosensory cortex. Neuroimage, 10, 63-83.
22. Geyer, S., Schormann, T., Mohlberg, H., & Zilles, K. (2000). Areas 3a, 3b, and 1 of human primary somatosensory cortex. Part 2. Spatial normalization to standard anatomical space. Neuroimage, 11, 684-696.
23. Goldreich, D., & Kanics, I. M. (2003). Tactile acuity is enhanced in blindness. Journal of Neuroscience, 23, 3439-3445.
24. Goyal, M. S., Hansen, P. J., & Blakemore, C. B. (2006). Tactile perception recruits functionally related visual areas in the late-blind. Neuroreport, 17, 1381-1384.
25. Granger, C. W. J. (1969). Investigating causal relations by econometric models and cross-spectral methods. Econometrica, 37, 424-438.
26. Grant, A. C., Thiagarajah, M. C., & Sathian, K. (2000). Tactile perception in blind Braille readers: A psycho-physical study of acuity and hyperacuity using gratings and dot patterns. Perception & Psychophysics, 62, 301-312.
27. Grefkes, C., Geyer, S., Schormann, T., Roland, P., & Zilles, K. (2001). Human somatosensory area 2: Observer-independent cytoarchitectonic mapping, interindividual variability, and population map. Neuroimage, 14, 617-631.
28. Grill-Spector, K., & Malach, R. (2004). The human visual cortex. Annual Review of Neuroscience, 27, 649-677.
29. Hamilton, R., Keenan, J. P., Catala, M., & Pascual-Leone,A. (2000). Alexia for Braille following bilateral occipital stroke in an early blind woman. Neuroreport, 11, 237-240.
30. Hyvärinen, J., Carlson, S., & Hyvärinen, L. (1981). Early visual deprivation alters modality of neuronal responses in area 19 of monkey cortex. Neuroscience Letters, 26, 239-243.
31. Kujala, T., Alho, K., Paavilainen, P., Summala, H., & Näätänen, R. (1992). Neural plasticity in processing of sound location by the early blind: An event-related potential study. Electroencephalography and Clinical Neurophysiology, 84, 469-472.
32. Kujala, T., Huotilainen, M., Sinkkonen, J., Ahonen, A. I., Alho, K., Hämäläinen, M. S., et al. (1995). Visual cortex activation in blind humans during sound discrimination. Neuroscience Letters, 183, 143-146.
33. Kujala, T., Palva, M. J., Salonen, O., Alku, P., Huotilainen, M., Järvinen, A., et al. (2005). The role of blind humans' visual cortex in auditory change detection. Neuroscience Letters, 379, 127-131.
34. Liu, Y., Yu, C., Liang, M., Li, J., Tian, L., Zhou, Y., et al. (2007).Whole brain functional connectivity in the early blind. Brain, 130, 2085-2096.
35. Mugler, J. P., 3rd., & Brookeman, J. R. (1990). Three-dimensional magnetization-prepared rapid gradient-echo imaging (3D MP RAGE). Magnetic Resonance in Medicine, 15, 152-157.
36. Orban, G. A., Van Essen, D., & Vanduffel, W. (2004). Comparative mapping of higher visual areas in monkeys and humans. Trends in Cognitive Sciences, 8, 315-324.
37. Pascual-Leone, A., & Torres, F. (1993). Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers. Brain, 116, 39-52.
38. Pietrini, P., Furey, M. L., Ricciardi, E., Gobbini, M. I., Wu, W. H., Cohen, L., et al. (2004). Beyond sensory images: Object-based representation in the human ventral pathway. Proceedings of the National Academy of Sciences of the United States of America, 101, 5658-5663.
39. Pitzalis, S., Galletti, C., Huang, R. S., Patria, F., Committeri, G., Galati, G., et al. (2006), Wide-field retinotopy defines human cortical visual area V6. Journal of Neuroscience, 26, 7962-7973.
40. Ptito, M., Fumal, A., de Noordhout,A. M., Schoenen, J., Gjedde, A., & Kupers, R. (2008)., TMS of the occipital cortex induces tactile sensations in the fingers of blind Braille readers. Experimental Brain Research, 184, 193-200.
41. Ptito, M., Moesgaard, S. M., Gjedde, A., & Kupers, R. (2005). Cross-modal plasticity revealed by electrotactile stimulation of the tongue in the congenitally blind. Brain, 128, 606-614.
42. Raczkowski, D., Kalat, J. W., & Nebes, R. (1974). Reliability and validity of some handedness questionnaire items. Neuropsychologia, 12, 43-47.
43. Rauschecker, J. P., Tian, B., Korte, M.,.& Egert, U. (1992). Crossmodal changes in the somatosensory vibrissa/barrel system of visually deprived animals. Proceedings of the National Academy of Sciences of the United States of America, 89, 5063-5067.
44. Ricciardi, E., Vanello, N., Sani, L., Gentili, C., Scilingo, E. P., Landini, L., et al. (2007). The effect of visual experience on the development of functional architecture in hMT+. Cerebral Cortex, 17, 2933-2939.
45. Röder, B., Rösler, F., Hennighausen, E., & Näcker, F. (1996). Event-related potentials during auditory and somatosensory discrimination in sighted and blind human subjects. Brain Research: Cognitive Brain Research, 4, 77-93.
46. Röder, B., Stock, O., Bien, S., & Rösler, F. (2002). Speech processing activates visual cortex in congenitally blind humans. European Journal of Neuroscience, 16, 930-936.
47. Sadato, N., Okada, T., Honda, M., & Yonekura, Y. (2002). Critical period for cross-modal plasticity in blind humans: A functional MRI study. Neuroimage, 16, 389-400.
48. Sadato, N., Okada, T., Kubota, K., & Yonekura, Y. (2004). Tactile discrimination activates the visual cortex of the recently blind naive to Braille: A functional magnetic resonance imaging study in humans. Neuroscience Letters, 359, 49-52.
49. Sadato, N., Pascual-Leone, A., Grafman, J., Deiber, M. P., Ibanñez, V., & Hallett, M. (1998). Neural networks for Braille reading by the blind. Brain, 121, 1213-1229.
50. Sadato, N., Pascual-Leone, A., Grafman, J., Ibañez, V., Deiber, M. P., Dold, G., et al. (1996). Activation of the primary visual cortex by Braille reading in blind subjects. Nature, 380, 526-528.
51. Sathian, K., & Lacey, S. (2007). Journeying beyond classical somatosensory cortex. Canadian Journal of Experimental Psychology, 61, 254-264.
52. Sathian, K., Zangaladze, A., Hoffman, J. M., & Grafton, S. T. (1997). Feeling with the mind's eye. Neuroreport, 8, 3877-3881.
53. Shimony, J. S., Burton, H., Epstein, A. A., McLaren, D. G., Sun, S. W., & Snyder, A. Z. (2006) Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cerebral Cortex, 16, 1653-1661.
54. Sterr, A., Müller, M. M., Elbert, T., Rockstroh, B., Pantev, C., & Taub, E. (1998). Perceptual correlates of changes in cortical representation of fingers in blind multifinger Braille readers. Journal of Neuroscience, 18, 4417-4423.
55. Stevens, J. C., Foulke, E., & Patterson, M. Q. (1996). Tactile acuity, aging and Braille reading in long-term blindness. Journal of Experimental Psychology: Applied, 2, 91-106.
56. Stevens, A. A., Snodgrass, M., Schwartz, D., & Weaver, K. (2007). Preparatory activity in occipital cortex in early blind humans predicts auditory perceptual performance. Journal of Neuroscience, 27, 10734-10741.
57. Stilla, R., Deshpande, G., LaConte, S., Hu, X., & Sathian, K. (2007). Posteromedial parietal cortical activity and inputs predict tactile spatial acuity. Journal of Neuroscience, 27, 11091-11102.
58. Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the brain. New York: Thieme Medical.
59. Toldi, J., Farkas, T., & Völgyi, B. (1994). Neonatal enucleation induces cross-modal changes in the barrel cortex of rat. A behavioural and electrophysiological study. Neuroscience Letters, 167, 1-4.
60. Toldi, J., Rojik, I., & Fehe'r, O. (1994) Neonatal monocular enucleation-induced cross-modal effects observed in the cortex of adult rat. Neuroscience, 62, 105-114.
61. Van Boven, R. W., Hamilton, R. H., Kauffman, T., Keenan, J. P., & Pascual-Leone, A. (2000). Tactile spatial resolution in blind braille readers. Neurology, 54, 2230-2236.
62. Veraart, C., De Volder, A. G., Wanet-Defalque, M. C., Bol, A., Michel, C., & Goffinet, A. M. (1990). Glucose utilization in human visual cortex is abnormally elevated in blindness of early onset but decreased in blindness of late onset. Brain Research, 510, 115-121.
63. Weaver, K. E., & Stevens, A. A. (2007). Attention and sensory interactions within the occipital cortex in the early blind: An fMRI study. Journal of Cognitive Neuroscience, 19, 315-330.
64. Weeks, R., Horwitz, B., Aziz-Sultan, A., Tian, B., Wessinger, C. M., Cohen, L. G., et al. (2000). A positron emission tomographic study of auditory localization in the congenitally blind. Journal of Neuroscience, 20, 2664-2672.
65. Weisser, V., Stilla, R., Peltier, S., Hu, X., & Sathian, K. (2005). Short-term visual deprivation alters neural processing of tactile form. Experimental Brain Research, 166, 572-582.
66. Wheat, H. E., & Goodwin, A. W. (2000). Tactile discrimination of gaps by slowly adapting afferents: Effects of population parameters and anisotropy in the fingerpad. Journal of Neurophysiology, 84, 1430-1444.
67. Wittenberg, G. F., Werhahn, K. J., Wassermann, E. M., Herscovitch, P., & Cohen, L. G. (2004). Functional connectivity between somatosensory and visual cortex in early blind humans. European Journal of Neuroscience, 20, 1923-1927.
68. Zangaladze, A., Epstein, C.M., Grafton, S. T., & Sathian, K. (1999). Involvement of visual cortex in tactile discrimination of orientation. Nature, 401, 587-590.