Table of Contents Author Guidelines Submit a Manuscript
Neural Plasticity
Volume 2012 (2012), Article ID 304045, 9 pages
http://dx.doi.org/10.1155/2012/304045
Research Article

Crossmodal Recruitment of the Ventral Visual Stream in Congenital Blindness

1École d’Optométrie, Université de Montréal, Montréal, QC, Canada H3T 1P1
2Department of Neuroscience and Pharmacology, Panum Institute, University of Copenhagen, Blegdamsvej 3B, 2200 Copenhagen, Denmark
3Danish Research Centre for Magnetic Resonance, Copenhagen University Hospital Hvidovre, 2650 Hvidovre, Denmark
4Department of Radiology, Beijing Hospital, 100054 Beijing, China
5Neurobiology Research Unit, Rigshospitalet, Copenhagen University Hospital, 2100 Copenhagen, Denmark

Received 22 January 2012; Accepted 19 April 2012

Academic Editor: Pietro Pietrini

Copyright © 2012 Maurice Ptito et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. O. Collignon, G. Charbonneau, M. Lassonde, and F. Lepore, “Early visual deprivation alters multisensory processing in peripersonal space,” Neuropsychologia, vol. 47, no. 14, pp. 3236–3243, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. D. R. Chebat, J. K. Chen, F. Schneider, A. Ptito, R. Kupers, and M. Ptito, “Alterations in right posterior hippocampus in early blind individuals,” NeuroReport, vol. 18, no. 4, pp. 329–333, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Fieger, B. Röder, W. Teder-Sälejärvi, S. A. Hillyard, and H. J. Neville, “Auditory spatial tuning in late-onset blindness in humans,” Journal of Cognitive Neuroscience, vol. 18, no. 2, pp. 149–157, 2006. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Goldreich and I. M. Kanics, “Tactile acuity is enhanced in blindness,” Journal of Neuroscience, vol. 23, no. 8, pp. 3439–3445, 2003. View at Google Scholar · View at Scopus
  5. D. Goldreich and I. M. Kanics, “Performance of blind and sighted humans on a tactile grating detection task,” Perception and Psychophysics, vol. 68, no. 8, pp. 1363–1371, 2006. View at Google Scholar · View at Scopus
  6. R. W. Van Boven, J. E. Ingeholm, M. S. Beauchamp, P. C. Bikle, and L. G. Ungerleider, “Tactile form and location processing in the human brain,” Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 35, pp. 12601–12605, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Pascual-Leone and F. Torres, “Plasticity of the sensorimotor cortex representation of the reading finger in Braille readers,” Brain, vol. 116, no. 1, pp. 39–52, 1993. View at Google Scholar · View at Scopus
  8. A. G. De Volder, A. Bol, J. Blin et al., “Brain energy metabolism in early blind subjects: neural activity in the visual cortex,” Brain Research, vol. 750, no. 1-2, pp. 235–244, 1997. View at Publisher · View at Google Scholar · View at Scopus
  9. R. Kupers, P. Pietrini, E. Ricciardi, and M. Ptito, “The nature of consciousness in the visually-deprived brain,” Frontiers in Psychology, vol. 2, no. 4, 2011. View at Publisher · View at Google Scholar
  10. L. B. Merabet, J. F. Rizzo, A. Amedi, D. C. Somers, and A. Pascual-Leone, “What blindness can tell us about seeing again: merging neuroplasticity and neuroprostheses,” Nature Reviews Neuroscience, vol. 6, no. 1, pp. 71–77, 2005. View at Publisher · View at Google Scholar · View at Scopus
  11. U. Noppeney, “The effects of visual deprivation on functional and structural organization of the human brain,” Neuroscience and Biobehavioral Reviews, vol. 31, no. 8, pp. 1169–1180, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Pietrini, M. L. Furey, E. Ricciardi et al., “Beyond sensory images: object-based representation in the human ventral pathway,” Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 15, pp. 5658–5663, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. M. Ptito, S. M. Moesgaard, A. Gjedde, and R. Kupers, “Cross-modal plasticity revealed by electrotactile stimulation of the tongue in the congenitally blind,” Brain, vol. 128, no. 3, pp. 606–614, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Ptito, I. Matteau, A. Gjedde, and R. Kupers, “Recruitment of the middle temporal area by tactile motion in congenital blindness,” NeuroReport, vol. 20, no. 6, pp. 543–547, 2009. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Amedi, W. M. Stern, J. A. Camprodon et al., “Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex,” Nature Neuroscience, vol. 10, no. 6, pp. 687–689, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Büchel, C. Price, R. S. J. Frackowiak, and K. Friston, “Different activation patterns in the visual cortex of late and congenitally blind subjects,” Brain, vol. 121, no. 3, pp. 409–419, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. H. Burton, “Visual cortex activity in early and late blind people,” Journal of Neuroscience, vol. 23, no. 10, pp. 4005–4011, 2003. View at Google Scholar · View at Scopus
  18. H. Burton, D. G. McLaren, and R. J. Sinclair, “Reading embossed capital letters: an fMRI study in blind and sighted individuals,” Human Brain Mapping, vol. 27, no. 4, pp. 325–339, 2006. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Sadato, A. Pascual-Leone, J. Grafman et al., “Activation of the primary visual cortex by Braille reading in blind subjects,” Nature, vol. 380, no. 6574, pp. 526–528, 1996. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Sadato, A. Pascual-Leone, J. Grafman, M. P. Deiber, V. Ibañez, and M. Hallett, “Neural networks for Braille reading by the blind,” Brain, vol. 121, no. 7, pp. 1213–1229, 1998. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Kupers, D. R. Chebat, K. H. Madsen, O. B. Paulson, and M. Ptito, “Neural correlates of virtual route recognition in congenital blindness,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 28, pp. 12716–12721, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Kupers, A. Fumal, A. M. De Noordhout, A. Gjedde, J. Schoenen, and M. Ptito, “Transcranial magnetic stimulation of the visual cortex induces somatotopically organized qualia in blind subjects,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 35, pp. 13256–13260, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Ptito, F. C. G. Schneider, O. B. Paulson, and R. Kupers, “Alterations of the visual pathways in congenital blindness,” Experimental Brain Research, vol. 187, no. 1, pp. 41–49, 2008. View at Publisher · View at Google Scholar · View at Scopus
  24. L. G. Cohen, P. Celnik, A. Pascual-Leone et al., “Functional relevance of cross-modal plasticity in blind humans,” Nature, vol. 389, no. 6647, pp. 180–183, 1997. View at Publisher · View at Google Scholar · View at Scopus
  25. R. Kupers, M. Pappens, A. M. De Noordhout, J. Schoenen, M. Ptito, and A. Fumal, “rTMS of the occipital cortex abolishes Braille reading and repetition priming in blind subjects,” Neurology, vol. 68, no. 9, pp. 691–693, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Büchel, “Cortical hierarchy turned on its head,” Nature Neuroscience, vol. 6, no. 7, pp. 657–658, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. P. Pietrini, M. Ptito, and R. Kupers, “Blindness and consciousness: new lights from the dark,” in The Neurology of Consciousness, S. Laureys and G. Tononi , Eds., pp. 360–374, Elsevier, Amsterdam, The Netherlands, 2009. View at Google Scholar
  28. M. A. Goodale and A. David Milner, “Separate visual pathways for perception and action,” Trends in Neurosciences, vol. 15, no. 1, pp. 20–25, 1992. View at Google Scholar · View at Scopus
  29. C. Poirier, O. Collignon, C. Scheiber et al., “Auditory motion perception activates visual motion areas in early blind subjects,” NeuroImage, vol. 31, no. 1, pp. 279–285, 2006. View at Publisher · View at Google Scholar · View at Scopus
  30. C. C. Poirier, A. G. De Volder, D. Tranduy, and C. Scheiber, “Neural changes in the ventral and dorsal visual streams during pattern recognition learning,” Neurobiology of Learning and Memory, vol. 85, no. 1, pp. 36–43, 2006. View at Publisher · View at Google Scholar · View at Scopus
  31. E. Ricciardi, N. Vanello, L. Sani et al., “The effect of visual experience on the development of functional architecture in hMT+,” Cerebral Cortex, vol. 17, no. 12, pp. 2933–2939, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. J. V. Haxby, M. I. Gobbini, M. L. Furey, A. Ishai, J. L. Schouten, and P. Pietrini, “Distributed and overlapping representations of faces and objects in ventral temporal cortex,” Science, vol. 293, no. 5539, pp. 2425–2430, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. I. Matteau, R. Kupers, E. Ricciardi, P. Pietrini, and M. Ptito, “Beyond visual, aural and haptic movement perception: hMT+ is activated by electrotactile motion stimulation of the tongue in sighted and in congenitally blind individuals,” Brain Research Bulletin, vol. 82, no. 5-6, pp. 264–270, 2010. View at Publisher · View at Google Scholar · View at Scopus
  34. L. G. Underleider and M. Mishkin, “Two cortical visual systems,” in Analysis of Visual Behavior, M. A. Ingle, M. I. Goodale, and R. J. W. Masfield, Eds., pp. 549–586, MIT Press, Cambridge, Mass, USA, 1982. View at Google Scholar
  35. R. Farivar, “Dorsal-ventral integration in object recognition,” Brain Research Reviews, vol. 61, no. 2, pp. 144–153, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Amedi, G. Jacobson, T. Hendler, R. Malach, and E. Zohary, “Convergence of visual and tactile shape processing in the human lateral occipital complex zohary,” Cerebral Cortex, vol. 12, no. 11, pp. 1202–1212, 2002. View at Google Scholar · View at Scopus
  37. A. Amedi, R. Malach, T. Hendler, S. Peled, and E. Zohary, “Visuo-haptic object-related activation in the ventral visual pathway,” Nature Neuroscience, vol. 4, no. 3, pp. 324–330, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Amedi, N. Raz, P. Pianka, R. Malach, and E. Zohary, “Early 'visual' cortex activation correlates with superior verbal memory performance in the blind,” Nature Neuroscience, vol. 6, no. 7, pp. 758–766, 2003. View at Publisher · View at Google Scholar · View at Scopus
  39. T. W. James, G. K. Humphrey, J. S. Gati, P. Servos, R. S. Menon, and M. A. Goodale, “Haptic study of three-dimensional objects activates extrastriate visual areas,” Neuropsychologia, vol. 40, no. 10, pp. 1706–1714, 2002. View at Publisher · View at Google Scholar · View at Scopus
  40. C. R. Genovese, N. A. Lazar, and T. Nichols, “Thresholding of statistical maps in functional neuroimaging using the false discovery rate,” NeuroImage, vol. 15, no. 4, pp. 870–878, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. T. Kassuba, C. Klinge, C. Hölig et al., “The left fusiform gyrus hosts trisensory representations of manipulable objects,” NeuroImage, vol. 56, no. 3, pp. 1566–1577, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. S. C. Prather and K. Sathian, “Mental rotation of tactile stimuli,” Cognitive Brain Research, vol. 14, no. 1, pp. 91–98, 2002. View at Publisher · View at Google Scholar · View at Scopus
  43. C. L. Reed, S. Shoham, and E. Halgren, “Neural substrates of tactile object recognition: an fMRI study,” Human Brain Mapping, vol. 21, no. 4, pp. 236–246, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. M. R. Stoesz, M. Zhang, V. D. Weisser, S. C. Prather, H. Mao, and K. Sathian, “Neural networks active during tactile form perception: common and differential activity during macrospatial and microspatial tasks,” International Journal of Psychophysiology, vol. 50, no. 1-2, pp. 41–49, 2003. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Amedi, K. Von Kriegstein, N. M. Van Atteveldt, M. S. Beauchamp, and M. J. Naumer, “Functional imaging of human crossmodal identification and object recognition,” Experimental Brain Research, vol. 166, no. 3-4, pp. 559–571, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. B. Röder, O. Stock, S. Bien, H. Neville, and F. Rösler, “Speech processing activates visual cortex in congenitally blind humans,” European Journal of Neuroscience, vol. 16, no. 5, pp. 930–936, 2002. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Gougoux, F. Lepore, M. Lassonde, P. Voss, R. J. Zatorre, and P. Belin, “Neuropsychology: pitch discrimination in the early blind,” Nature, vol. 430, no. 6997, p. 309, 2004. View at Google Scholar · View at Scopus
  48. M. Beaulieu-Lefebvre, F. C. Schneider, R. Kupers, and M. Ptito, “Odor perception and odor awareness in congenital blindness,” Brain Research Bulletin, vol. 84, no. 3, pp. 206–209, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Zhang, V. D. Weisser, R. Stilla, S. C. Prather, and K. Sathian, “Multisensory cortical processing of object shape and its relation to mental imagery,” Cognitive, Affective and Behavioral Neuroscience, vol. 4, no. 2, pp. 251–259, 2004. View at Google Scholar · View at Scopus
  50. S. Lacey, P. Flueckiger, R. Stilla, M. Lava, and K. Sathian, “Object familiarity modulates the relationship between visual object imagery and haptic shape perception,” NeuroImage, vol. 49, no. 3, pp. 1977–1990, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Poirier, A. De Volder, D. Tranduy, and C. Scheiber, “Pattern recognition using a device substituting audition for vision in blindfolded sighted subjects,” Neuropsychologia, vol. 45, no. 5, pp. 1108–1121, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. D. Kaski, “Revision: is visual perception a requisite for visual imagery?” Perception, vol. 31, no. 6, pp. 717–731, 2002. View at Google Scholar · View at Scopus
  53. N. Sadato, T. Okada, M. Honda, and Y. Yonekura, “Critical period for cross-modal plasticity in blind humans: a functional MRI study,” NeuroImage, vol. 16, no. 2, pp. 389–400, 2002. View at Publisher · View at Google Scholar · View at Scopus
  54. T. Harada, D. N. Saito, K. I. Kashikura et al., “Asymmetrical neural substrates of tactile discrimination humans: a functional magnetic resonance imaging study,” Journal of Neuroscience, vol. 24, no. 34, pp. 7524–7530, 2004. View at Publisher · View at Google Scholar · View at Scopus
  55. D. N. Saito, T. Okada, M. Honda, Y. Yonekura, and N. Sadato, “Practice makes perfect: the neural substrates of tactile discrimination by Mah-Jong experts include the primary visual cortex,” BMC Neuroscience, vol. 7, article 79, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. L. B. Merabet, J. D. Swisher, S. A. McMains et al., “Combined activation and deactivation of visual cortex during tactile sensory processing,” Journal of Neurophysiology, vol. 97, no. 2, pp. 1633–1641, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Murata, V. Gallese, M. Kaseda, and H. Sakata, “Parietal neurons related to memory-guided hand manipulation,” Journal of Neurophysiology, vol. 75, no. 5, pp. 2180–2186, 1996. View at Google Scholar · View at Scopus
  58. H. Sakata, M. Taira, A. Murata, and S. Mine, “Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey,” Cerebral Cortex, vol. 5, no. 5, pp. 429–438, 1995. View at Google Scholar · View at Scopus
  59. A. Bodegård, S. Geyer, C. Grefkes, K. Zilles, and P. E. Roland, “Hierarchical processing of tactile shape in the human brain,” Neuron, vol. 31, no. 2, pp. 317–328, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. L. Jäncke, A. Kleinschmidt, S. Mirzazade, N. J. Shah, and H. J. Freund, “The role of the inferior parietal cortex in linking the tactile perception and manual construction of object shapes,” Cerebral Cortex, vol. 11, no. 2, pp. 114–121, 2001. View at Google Scholar · View at Scopus
  61. E. Shikata, F. Hamzei, V. Glauche et al., “Surface orientation discrimination activates caudal and anterior intraparietal sulcus in humans: an event-related fMRI study,” Journal of Neurophysiology, vol. 85, no. 3, pp. 1309–1314, 2001. View at Google Scholar · View at Scopus
  62. T. Fujii, H. C. Tanabe, T. Kochiyama, and N. Sadato, “An investigation of cross-modal plasticity of effective connectivity in the blind by dynamic causal modeling of functional MRI data,” Neuroscience Research, vol. 65, no. 2, pp. 175–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Chabot, S. Robert, R. Tremblay, D. Miceli, D. Boire, and G. Bronchti, “Audition differently activates the visual system in neonatally enucleated mice compared with anophthalmic mutants,” European Journal of Neuroscience, vol. 26, no. 8, pp. 2334–2348, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. N. Chabot, V. Charbonneau, M. E. Laramée, R. Tremblay, D. Boire, and G. Bronchti, “Subcortical auditory input to the primary visual cortex in anophthalmic mice,” Neuroscience Letters, vol. 433, no. 2, pp. 129–134, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. G. Bronchti, P. Heil, R. Sadka, A. Hess, H. Scheich, and Z. Wollberg, “Auditory activation of 'visual' cortical areas in the blind mole rat (Spalax ehrenbergi),” European Journal of Neuroscience, vol. 16, no. 2, pp. 311–329, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Burton, R. J. Sinclair, and D. G. McLaren, “Cortical activity to vibrotactile stimulation: an fMRI study in blind and sighted individuals,” Human Brain Mapping, vol. 23, no. 4, pp. 210–228, 2004. View at Publisher · View at Google Scholar · View at Scopus