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Neural Plasticity
Volume 2012 (2012), Article ID 687659, 12 pages
http://dx.doi.org/10.1155/2012/687659
Review Article

Plasticity of the Dorsal “Spatial” Stream in Visually Deprived Individuals

1Centre de Recherche en Neuropsychologie et Cognition (CERNEC), Université de Montréal, Montreal, QC, Canada H3C 3J7
2Institute of Psychology and Institute of Neurosciences, Université Catholique de Louvain, 1348 Louvain-la-Neuve, Belgium
3Centre de Recherche du CHU Sainte-Justine, Université de Montréal, Montreal, QC, Canada H3T 1C5
4Center for Mind/Brain Sciences, University of Trento, 38060 Mattarello, Italy

Received 16 December 2011; Accepted 6 June 2012

Academic Editor: Pietro Pietrini

Copyright © 2012 Giulia Dormal 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. D. Bavelier and H. J. Neville, “Cross-modal plasticity: where and how?” Nature Reviews Neuroscience, vol. 3, no. 6, pp. 443–452, 2002. View at Google Scholar · View at Scopus
  2. 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
  3. 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
  4. H. Burton, A. Z. Snyder, T. E. Conturo, E. Akbudak, J. M. Ollinger, and M. E. Raichle, “Adaptive changes in early and late blind: a fMRI study of Braille reading,” Journal of Neurophysiology, vol. 87, no. 1, pp. 589–607, 2002. View at Google Scholar · View at Scopus
  5. H. Burton, A. Z. Snyder, J. B. Diamond, and M. E. Raichle, “Adaptive changes in early and late blind: a fMRI study of verb generation to heard nouns,” Journal of Neurophysiology, vol. 88, no. 6, pp. 3359–3371, 2002. View at Google Scholar · View at Scopus
  6. P. Voss, F. Gougoux, R. J. Zatorre, M. Lassonde, and F. Lepore, “Differential occipital responses in early- and late-blind individuals during a sound-source discrimination task,” NeuroImage, vol. 40, no. 2, pp. 746–758, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. J. V. Haxby, C. L. Grady, B. Horwitz et al., “Dissociation of object and spatial visual processing pathways in human extrastriate cortex,” Proceedings of the National Academy of Sciences of the United States of America, vol. 88, no. 5, pp. 1621–1625, 1991. View at Google Scholar · View at Scopus
  8. 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
  9. E. Striem-Amit, O. Dakwar, L. Reich, and A. Amedi, “The large-scale organization of “visual” streams emerges without visual experience,” Cerebral Cortex, vol. 22, no. 7, pp. 1698–1709, 2012. View at Publisher · View at Google Scholar · View at Scopus
  10. O. Collignon, P. Voss, M. Lassonde, and F. Lepore, “Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects,” Experimental Brain Research, vol. 192, no. 3, pp. 343–358, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. G. Dormal and O. Collignon, “Functional selectivity in sensory-deprived cortices,” Journal of Neurophysiology, vol. 105, no. 6, pp. 2627–2630, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. P. Voss and R. J. Zatorre, “Organization and reorganization of sensory-deprived cortex,” Current Biology, vol. 22, no. 5, pp. R168–R173, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. D. Maurer, T. L. Lewis, and C. J. Mondloch, “Missing sights: consequences for visual cognitive development,” Trends in Cognitive Sciences, vol. 9, no. 3, pp. 144–151, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Sunaert, P. Van Hecke, G. Marchal, and G. A. Orban, “Motion-responsive regions of the human brain,” Experimental Brain Research, vol. 127, no. 4, pp. 355–370, 1999. View at Publisher · View at Google Scholar · View at Scopus
  15. R. B. H. Tootell, J. B. Reppas, K. K. Kwong et al., “Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging,” Journal of Neuroscience, vol. 15, no. 4, pp. 3215–3230, 1995. View at Google Scholar · View at Scopus
  16. J. D. G. Watson, R. Myers, R. S. J. Frackowiak et al., “Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging,” Cerebral Cortex, vol. 3, no. 2, pp. 79–94, 1993. View at Google Scholar · View at Scopus
  17. D. Ellemberg, T. L. Lewis, D. Maurer, S. Brar, and H. P. Brent, “Better perception of global motion after monocular than after binocular deprivation,” Vision Research, vol. 42, no. 2, pp. 169–179, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. D. E. Mitchell, J. Kennie, and D. Kung, “Development of global motion perception requires postnatal exposure to pattern light,” Current Biology, vol. 19, no. 8, pp. 645–649, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. N. L. Rochefort, M. Narushima, C. Grienberger, N. Marandi, D. N. Hill, and A. Konnerth, “Development of direction selectivity in mouse cortical neurons,” Neuron, vol. 71, no. 3, pp. 425–432, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. Y. Li, D. Fitzpatrick, and L. E. White, “The development of direction selectivity in ferret visual cortex requires early visual experience,” Nature Neuroscience, vol. 9, no. 5, pp. 676–681, 2006. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Li, S. D. Van Hooser, M. Mazurek, L. E. White, and D. Fitzpatrick, “Experience with moving visual stimuli drives the early development of cortical direction selectivity,” Nature, vol. 456, no. 7224, pp. 952–956, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. O. Braddick, J. Atkinson, and J. Wattam-Bell, “Normal and anomalous development of visual motion processing: motion coherence and 'dorsal-stream vulnerability',” Neuropsychologia, vol. 41, no. 13, pp. 1769–1784, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Banton, B. I. Bertenthal, and J. Seaks, “Infants' sensitivity to statistical distributions of motion direction and speed,” Vision Research, vol. 39, no. 20, pp. 3417–3430, 1999. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Wattam-Bell, “Coherence thresholds for discrimination of motion direction in infants,” Vision Research, vol. 34, no. 7, pp. 877–883, 1994. View at Publisher · View at Google Scholar · View at Scopus
  25. E. E. Parrish, D. E. Giaschi, C. Boden, and R. Dougherty, “The maturation of form and motion perception in school age children,” Vision Research, vol. 45, no. 7, pp. 827–837, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. D. Ellemberg, T. L. Lewis, M. Dirks et al., “Putting order into the development of sensitivity to global motion,” Vision Research, vol. 44, no. 20, pp. 2403–2411, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Gunn, E. Cory, J. Atkinson et al., “Dorsal and ventral stream sensitivity in normal development and hemiplegia,” NeuroReport, vol. 13, no. 6, pp. 843–847, 2002. View at Google Scholar · View at Scopus
  28. B.-S. Hadad, D. Maurer, and T. L. Lewis, “Long trajectory for the development of sensitivity to global and biological motion,” Developmental Science, vol. 14, no. 6, pp. 1330–1339, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. S. Narasimhan and D. Giaschi, “The effect of dot speed and density on the development of global motion perception,” Vision Research, vol. 62, pp. 102–107, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. T. L. Lewis and D. Maurer, “Multiple sensitive periods in human visual development: evidence from visually deprived children,” Developmental Psychobiology, vol. 46, no. 3, pp. 163–183, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. D. Maurer, C. J. Mondloch, and T. L. Lewis, “Sleeper effects,” Developmental Science, vol. 10, no. 1, pp. 40–47, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Geldart, C. J. Mondloch, D. Maurer, S. De Schonen, and H. P. Brent, “The effect of early visual deprivation on the development of face processing,” Developmental Science, vol. 5, no. 4, pp. 490–501, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. R. Le Grand, C. J. Mondloch, D. Maurer, and H. P. Brent, “Neuroperception: early visual experience and face processing,” Nature, vol. 410, no. 6831, p. 890, 890. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Le Grand, C. J. Mondloch, D. Maurer, and H. P. Brent, “Impairment in holistic face processing following early visual deprivation,” Psychological Science, vol. 15, no. 11, pp. 762–768, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. D. Maurer, D. Ellemberg, and T. L. Lewis, “Repeated measurements of contrast sensitivity reveal limits to visual plasticity after early binocular deprivation in humans,” Neuropsychologia, vol. 44, no. 11, pp. 2104–2112, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. A. Pascual-Leone, A. Amedi, F. Fregni, and L. B. Merabet, “The plastic human brain cortex,” Annual Review of Neuroscience, vol. 28, pp. 377–401, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Bedny, T. Konkle, K. Pelphrey, R. Saxe, and A. Pascual-Leone, “Sensitive period for a multimodal response in human visual motion area MT/MST,” Current Biology, vol. 20, no. 21, pp. 1900–1906, 2010. View at Publisher · View at Google Scholar · View at Scopus
  38. O. Collignon, G. Vandewalle, P. Voss et al., “Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 11, pp. 4435–4440, 2011. View at Publisher · View at Google Scholar · View at Scopus
  39. 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
  40. T. Wolbers, P. Zahorik, and N. A. Giudice, “Decoding the direction of auditory motion in blind humans,” NeuroImage, vol. 56, no. 2, pp. 681–687, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Bonino, E. Ricciardi, L. Sani et al., “Tactile spatial working memory activates the dorsal extrastriate cortical pathway in congenitally blind individuals,” Archives Italiennes de Biologie, vol. 146, no. 3-4, pp. 133–146, 2008. View at Google Scholar · View at Scopus
  42. 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
  43. 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
  44. R. T. Born and D. C. Bradley, “Structure and function of visual area MT,” Annual Review of Neuroscience, vol. 28, pp. 157–189, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. F. Gougoux, R. J. Zatorre, M. Lassonde, P. Voss, and F. Lepore, “A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals,” PLoS Biology, vol. 3, no. 2, article e27, 2005. View at Google Scholar · View at Scopus
  46. L. A. Renier, I. Anurova, A. G. De Volder, S. Carlson, J. VanMeter, and J. P. Rauschecker, “Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind,” Neuron, vol. 68, no. 1, pp. 138–148, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. R. Weeks, B. Horwitz, A. Aziz-Sultan et al., “A positron emission tomographic study of auditory localization in the congenitally blind,” Journal of Neuroscience, vol. 20, no. 7, pp. 2664–2672, 2000. View at Google Scholar · View at Scopus
  48. R. B. H. Tootell, J. D. Mendola, N. K. Hadjikhani et al., “Functional analysis of V3A and related areas in human visual cortex,” Journal of Neuroscience, vol. 17, no. 18, pp. 7060–7078, 1997. View at Google Scholar · View at Scopus
  49. S. M. Szczepanski, C. S. Konen, and S. Kastner, “Mechanisms of spatial attention control in frontal and parietal cortex,” Journal of Neuroscience, vol. 30, no. 1, pp. 148–160, 2010. View at Publisher · View at Google Scholar · View at Scopus
  50. O. Collignon, M. Davare, E. Olivier, and A. G. De Volder, “Reorganisation of the right occipito-parietal stream for auditory spatial processing in early blind humans. a transcranial magnetic stimulation study,” Brain Topography, vol. 21, no. 3-4, pp. 232–240, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. O. Collignon, M. Lassonde, F. Lepore, D. Bastien, and C. Veraart, “Functional cerebral reorganization for auditory spatial processing and auditory substitution of vision in early blind subjects,” Cerebral Cortex, vol. 17, no. 2, pp. 457–465, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. E. Fischer, H. H. Bülthoff, N. K. Logothetis, and A. Bartels, “Visual motion responses in the posterior cingulate sulcus: a comparison to V5/MT and MST,” Cerebral Cortex, vol. 22, no. 4, pp. 865–876, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Larsson and D. J. Heeger, “Two retinotopic visual areas in human lateral occipital cortex,” Journal of Neuroscience, vol. 26, no. 51, pp. 13128–13142, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. M. I. Sereno, A. M. Dale, J. B. Reppas et al., “Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging,” Science, vol. 268, no. 5212, pp. 889–893, 1995. View at Google Scholar · View at Scopus
  55. O. Collignon, G. Albouy, G. Dormal et al., “Impact of early versus late acquired blindness on the functional organization and connectivity of the occipital cortex,” Journal of Vision, vol. 12, no. 9, p. 610, 2012. View at Google Scholar
  56. R. L. Gregory and J. Wallace, Recovery from Early Blindness: A Case Study, Experimental Psychology Society Monograph No. 2, Heffers, Cambridge, UK, 1963.
  57. R. Gregory, L.Concepts and Mechanisms of Perception, Duckworth, London, 1974.
  58. I. Fine, A. R. Wade, A. A. Brewer et al., “Long-term deprivation affects visual perception and cortex,” Nature Neuroscience, vol. 6, no. 9, pp. 915–916, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. N. Levin, S. O. Dumoulin, J. Winawer, R. F. Dougherty, and B. A. Wandell, “Cortical maps and white matter tracts following long period of visual deprivation and retinal image restoration,” Neuron, vol. 65, no. 1, pp. 21–31, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Saenz, L. B. Lewis, A. G. Huth, I. Fine, and C. Koch, “Visual motion area MT + /V5 responds to auditory motion in human sight-recovery subjects,” Journal of Neuroscience, vol. 28, no. 20, pp. 5141–5148, 2008. View at Publisher · View at Google Scholar · View at Scopus
  61. C. Ackroyd, N. K. Humphrey, and E. K. Warrington, “Lasting effects of early blindness, a case study,” Quarterly Journal of Experimental Psychology, vol. 26, no. 1, pp. 114–124, 1974. View at Google Scholar · View at Scopus
  62. Y. Ostrovsky, A. Andalman, and P. Sinha, “Vision following extended congenital blindness,” Psychological Science, vol. 17, no. 12, pp. 1009–1014, 2006. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Ostrovsky, E. Meyers, S. Ganesh, U. Mathur, and P. Sinha, “Visual parsing after recovery from blindness,” Psychological Science, vol. 20, no. 12, pp. 1484–1491, 2009. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Alink, W. Singer, and L. Muckli, “Capture of auditory motion by vision is represented by an activation shift from auditory to visual motion cortex,” Journal of Neuroscience, vol. 28, no. 11, pp. 2690–2697, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. S. Sadaghiani, J. X. Maier, and U. Noppeney, “Natural, metaphoric, and linguistic auditory direction signals have distinct influences on visual motion processing,” Journal of Neuroscience, vol. 29, no. 20, pp. 6490–6499, 2009. View at Publisher · View at Google Scholar · View at Scopus
  66. M. C. Hagen, O. Franzén, F. McGlone, G. Essick, C. Dancer, and J. V. Pardo, “Tactile motion activates the human middle temporal/V5 (MT/V5) complex,” European Journal of Neuroscience, vol. 16, no. 5, pp. 957–964, 2002. View at Publisher · View at Google Scholar · View at Scopus
  67. E. Ricciardi, D. Bonino, C. Gentili, L. Sani, P. Pietrini, and T. Vecchi, “Neural correlates of spatial working memory in humans: a functional magnetic resonance imaging study comparing visual and tactile processes,” Neuroscience, vol. 139, no. 1, pp. 339–349, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. K. Sathian, “Visual cortical activity during tactile perception in the sighted and the visually deprived,” Developmental Psychobiology, vol. 46, no. 3, pp. 279–286, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Pascual-Leone and R. Hamilton, “The metamodal organization of the brain,” Progress in Brain Research, vol. 134, pp. 427–445, 2001. View at Publisher · View at Google Scholar · View at Scopus
  70. E. Ricciardi and P. Pietrini, “New light from the dark: what blindness can teach us about brain function,” Current Opinion in Neurology, vol. 24, no. 4, pp. 357–363, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. S. M. Kosslyn, N. M. Alpert, W. L. Thompson et al., “Visual mental imagery activates topographically organized visual cortex: PET investigations,” Journal of Cognitive Neuroscience, vol. 5, no. 3, pp. 263–287, 1993. View at Google Scholar · View at Scopus
  72. S. D. Slotnick, W. L. Thompson, and S. M. Kosslyn, “Visual mental imagery induces retinotopically organized activation of early visual areas,” Cerebral Cortex, vol. 15, no. 10, pp. 1570–1583, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. S. M. Kosslyn and W. L. Thompson, “When is early visual cortex activated during visual mental imagery?” Psychological Bulletin, vol. 129, no. 5, pp. 723–746, 2003. View at Publisher · View at Google Scholar · View at Scopus
  74. P. J. Laurienti, J. H. Burdette, M. T. Wallace, Y. F. Yen, A. S. Field, and B. E. Stein, “Deactivation of sensory-specific cortex by cross-modal stimuli,” Journal of Cognitive Neuroscience, vol. 14, no. 3, pp. 420–429, 2002. View at Publisher · View at Google Scholar · View at Scopus
  75. 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
  76. C. Poirier, O. Collignon, A. G. DeVolder et al., “Specific activation of the V5 brain area by auditory motion processing: an fMRI study,” Cognitive Brain Research, vol. 25, no. 3, pp. 650–658, 2005. View at Publisher · View at Google Scholar · View at Scopus
  77. A. A. Ghazanfar and C. E. Schroeder, “Is neocortex essentially multisensory?” Trends in Cognitive Sciences, vol. 10, no. 6, pp. 278–285, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. O. Collignon, M. Davare, A. G. De Volder, C. Poirier, E. Olivier, and C. Veraart, “Time-course of posterior parietal and occipital cortex contribution to sound localization,” Journal of Cognitive Neuroscience, vol. 20, no. 8, pp. 1454–1463, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. D. Basso, A. Pavan, E. Ricciardi et al., “Touching Motion : rTMS on human middle temporal complex interferes with tactile speed perception,” Brain Topography. In press. View at Publisher · View at Google Scholar · View at Scopus
  80. E. Ricciardi, D. Basso, L. Sani et al., “Functional inhibition of the human middle temporal cortex affects non-visual motion perception: a repetitive transcranial magnetic stimulation study during tactile speed discrimination,” Experimental Biology and Medicine, vol. 236, no. 2, pp. 138–144, 2011. View at Publisher · View at Google Scholar · View at Scopus
  81. C. Cappe and P. Barone, “Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey,” European Journal of Neuroscience, vol. 22, no. 11, pp. 2886–2902, 2005. View at Publisher · View at Google Scholar · View at Scopus
  82. S. Clavagnier, A. Falchier, and H. Kennedy, “Long-distance feedback projections to area V1: implications for multisensory integration, spatial awareness, and visual consciousness,” Cognitive, Affective and Behavioral Neuroscience, vol. 4, no. 2, pp. 117–126, 2004. View at Google Scholar · View at Scopus
  83. A. Falchier, S. Clavagnier, P. Barone, and H. Kennedy, “Anatomical evidence of multimodal integration in primate striate cortex,” Journal of Neuroscience, vol. 22, no. 13, pp. 5749–5759, 2002. View at Google Scholar · View at Scopus
  84. K. S. Rockland and H. Ojima, “Multisensory convergence in calcarine visual areas in macaque monkey,” International Journal of Psychophysiology, vol. 50, no. 1-2, pp. 19–26, 2003. View at Publisher · View at Google Scholar · View at Scopus