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

Volumn 82, Issue 5-6, 2010, Pages 264-270

  Matteau, Isabelle ^a   Kupers, Ron ^b,c   Ricciardi, Emiliano ^d   Pietrini, Pietro ^d,e   Ptito, Maurice ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF PISA   (Italy)

^e UNIVERSITY HOSPITAL OF PISA   (Italy)

Author keywords

Blindness; Cross modal plasticity; Dorsal stream; FMRI; Motion; Sensory substitution; Supramodality; Tongue display unit; Vision

Indexed keywords

ADULT; ARTICLE; BEHAVIOR THERAPY; BRAIN CORTEX; BRAIN REGION; CAUDATE NUCLEUS; CEREBELLUM; CINGULATE GYRUS; CLINICAL ARTICLE; CONGENITAL BLINDNESS; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INSULA; MALE; MOTOR CORTEX; MOVEMENT PERCEPTION; NORMAL HUMAN; OCCIPITAL CORTEX; OUTCOME ASSESSMENT; PARIETAL LOBE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SENSORY EVALUATION; TACTILE DISCRIMINATION; TACTILE STIMULATION; TEMPORAL CORTEX; THALAMOCORTICAL TRACT; THALAMUS; TONGUE; VISUAL INFORMATION; VISUAL STIMULATION; BLINDNESS; BLOOD; BRAIN MAPPING; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; MIDDLE AGED; MOTION; MOVEMENT (PHYSIOLOGY); NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PATHOPHYSIOLOGY; PERCEPTIVE DISCRIMINATION; PHYSIOLOGY; PROCEDURES; STIMULATION; TOUCH; VASCULARIZATION; VISUAL CORTEX;

ADULT; BLINDNESS; BRAIN MAPPING; DISCRIMINATION (PSYCHOLOGY); FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MOTION; MOTION PERCEPTION; MOVEMENT; OXYGEN; PHYSICAL STIMULATION; TOUCH; VISUAL CORTEX;

OXYGEN;

EID: 77955088448     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2010.05.001     Document Type: Article

References (52)

1. Amedi A., Malach R., Hendler T., Peled S., Zohary E. Visuo-haptic object-related activation in the ventral visual pathway. Nat. Neurosci. 2001, 4:324-330.
2. Amedi A., von Kriegstein K., van Atteveldt N.M., Beauchamp M.S., Naumer M.J. Functional imaging of human crossmodal identification and object recognition. Exp. Brain Res. 2005, 166:559-571.
3. Baumann O., Greenlee M.W. Neural correlates of coherent audiovisual motion perception. Cereb. Cortex 2007, 17:1433-1443.
4. Beauchamp M.S., Yasar N.E., Kishan N., Ro T. Human MST but not MT responds to tactile stimulation. J. Neurosci. 2007, 27:8261-8267.
5. Becker H.G., Erb M., Haarmeier T. Differential dependency on motion coherence in subregions of the human MT+ complex. Eur. J. Neurosci. 2008, 28:1674-1685.
6. Bicchi A., Scilingo E.P., Ricciardi E., Pietrini P. Tactile flow explains haptic counterparts of common visual illusions. Brain Res. Bull. 2008, 75:737-741.
7. Blake R., Sobel K.V., James T.W. Neural synergy between kinetic vision and touch. Psychol. Sci. 2004, 15:397-402.
8. Bonino D., Ricciardi E., Sani L., Gentili C., Vanello N., Guazzelli M., Vecchi T., Pietrini P. Tactile spatial working memory activates the dorsal extrastriate cortical pathway in congenitally blind individuals. Arch. Ital. Biol. 2008, 146:133-146.
9. Cattaneo Z., Vecchi T., Cornoldi C., Mammarella I., Bonino D., Ricciardi E., Pietrini P. Imagery and spatial processes in blindness and visual impairment. Neurosci. Biobehav. Rev. 2008, 32:1346-1360.
10. Celebrini S., Newsome W.T. Neuronal and psychophysical sensitivity to motion signals in extrastriate area MST of the macaque monkey. J. Neurosci. 1994, 14:4109-4124.
11. Chabot N., Charbonneau V., Laramée M.-E., Tremblay R., Boire D., Bronchti G. Subcortical auditory input to the primary visual cortex in anophthalmic mice. Neurosci. Lett. 2008, 433:129-134.
12. Christensen R., Grey M., Ptito M., Kupers R. Resting state brain metabolism and functional connectivity of the occipital cortex in congenital blindness: a combined rTMS and PET-FDG study. NeuroImage 2009, (Suppl.):649.
13. Cohen L.C., Celnik P., Pascual-Leone A., Corwell B., Faiz L., Dambrosia J., Honda M., Sadato N., Gerloff C., Dolores Catalá M., Hallett M. Functional relevance of cross-modal plasticity in blind humans. Nature 1997, 389:180-183.
14. De Volder A.G., Bol A., Blin J., Robert A., Arno P., Grandin C., Michel C., Veraart C. Brain energy metabolism in early blind subjects: neural activity in the visual cortex. Brain Res. 1997, 50:235-244.
15. Fujii T., Tanabe H.C., Kochiyama T., Sadato N. An investigation of cross-modal plasticity of effective connectivity in the blind by dynamic causal modeling of functional MRI data. Neurosci. Res. 2009, 65:175-186.
16. Goebel R., Khorram-Sefat D., Muckli L., Hacker H., Singer W. The constructive nature of vision: direct evidence from the functional magnetic resonance imaging studies of apparent motion and motion imagery. Eur. J. Neurosci. 1998, 10:1563-1573.
17. Hagen M.C., Franzén O., McGlone F., Essick G., Dancer C., Pardo J.V. Tactile motion activates the human middle temporal//V5 (MT/V5) complex. Eur. J. Neurosci. 2002, 16:957-964.
18. Heuer H.W., Britten K.H. Optic flow signals in extrastriate area MST: comparison of perceptual and neuronal sensitivity. J. Neurophysiol. 2004, 91:1314-1326.
19. Kupers R., Fumal A., Maertens de Noordhout A., Gjedde A., Schoenen J., Ptito M. Transcranial magnetic stimulation of the visual cortex induces somatotopically organized qualia in blind subjects. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:13256-13260.
20. Kupers R., Pappens M., Maertens de Noordhout A., Schoenen J., Ptito M., Fumal A. rTMS of the occipital cortex abolishes Braille reading and repetition priming in blind subjects. Neurology 2007, 68:691-693.
21. Laemle L.K., Strominger N.L., Carpenter D.O. Cross-modal innervation of primary visual cortex by auditory fibers in congenitally anophthalmic mice. Neurosci. Lett. 2006, 396:108-112.
22. Lewis J.W., Beauchamp M.S., DeYoe E.A. A comparison of visual and auditory motion processing in human cerebral cortex. Cereb. Cortex 2000, 10:873-888.
23. Mahon B.Z., Anzellotti S., Schwarzbach J., Zampini M., Caramazza A. Category-specific organization in the human brain does not require visual experience. Neuron 2009, 63:397-405.
24. McKeefry D.J., Watson J.D.G., Frackowiak R.S.J., Fong K., Zeki S. The activity in human areas V1/V2, V3, and V5 during the perception of coherent and incoherent motion. NeuroImage 1997, 5:1-12.
25. Noppeney U. The effects of visual deprivation on functional and structural organization of the human brain. Neurosci. Biobehav. Rev. 2007, 31:1169-1180.
26. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
27. Pietrini P., Furey M.L., Ricciardi E., Gobbini M.I., Wu H.-W.C., Cohen L., Guazzelli M., Haxby J.V. Beyond sensory images: object-based representation in the human ventral pathway. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:5658-5663.
28. Pietrini P., Ptito M., Kupers R. Blindness and consciousness: new light from the dark. The Neurology of Consciousness 2009, 360-374. Academic Press, Amsterdam. S. Laureys, G. Tononi (Eds.).
29. Poirier C., Collignon O., DeVolder A.G., Renier L., Vanlierde A., Tranduy D., Scheiber C. Specific activation of the V5 brain area by auditory motion processing: an fMRI study. Cogn. Brain Res. 2005, 25:650-658.
30. Poirier C., Collignon O., Scheiber C., Renier L., Vanlierde A., Tranduy D., Veraart C., De Volder A.G. Auditory motion perception activates visual motion areas in early blind subjects. NeuroImage 2006, 31:279-285.
31. Ptito M., Faubert J., Gjedde A., Kupers R. Separate neural pathways for contour and biological-motion cues in motion-defined animal shapes. NeuroImage 2003, 19:246-252.
32. Ptito M., Fumal A., de Noordhout A.M., Schoenen J., Gjedde A., Kupers R. TMS of the occipital cortex induces tactile sensations in the fingers of blind Braille readers. Exp. Brain Res. 2008, 184:193-200.
33. Ptito M., Kupers R. Cross-modal plasticity in early blindness. J. Integr. Neurosci. 2005, 4:479-488.
34. Ptito M., Kupers R., Faubert J., Gjedde A. Cortical representation of inward and outward radial motion in man. NeuroImage 2001, 14:1409-1415.
35. Ptito M., Matteau M.I., Gjedde A., Kupers R. Recruitment of the middle temporal area by tactile motion in congenital blindness. Neuroreport 2009, 22:543-547.
36. Ptito M., Moesgaard S.M., Gjedde A., Kupers R. Cross-modal plasticity revealed by elecrotactile stimulation of the tongue in the congenitally blind. Brain 2005, 128:606-614.
37. Ptito M., Schneider F.C., Paulson O.B., Kupers R. Alterations of the visual pathways in congenital blindness. Exp. Brain Res. 2008, 187:41-49.
38. Ricciardi E., Basso D., Bonino D., Sani L., Guazzelli M., Vecchi T., Miniussi C., Pietrini P. rTMS-mediated functional suppression of hMT+ impairs tactile flow discrimination in humans. Soc. Neurosci. 2007, Program No. 73.5/FF2. Washington, DC.
39. Ricciardi E., Bonino D., Gentili C., Sani L., Pietrini P., Vecchi T. Neural correlates of spatial working memory in humans: a functional magnetic resonance imaging study comparing visual and tactile processes. Neuroscience 2006, 139:339-349.
40. Ricciardi E., Bonino D., Sani L., Vecchi T., Guazzelli M., Haxby J.V., Fadiga L., Pietrini P. Do we really need vision? How blind people see the actions of others. J. Neurosci. 2009, 29:9719-9724.
41. Ricciardi E., Vanello N., Sani L., Gentili C., Scilingo E.P., Landini L., Guazzelli M., Bicchi A., Haxby J.V., Pietrini P. The effect of visual experience on the development of functional architecture in hMT+. Cereb. Cortex 2007, 17:2933-2939.
42. Rockland K.S., Ojima H. Multisensory convergence in calcarine visual areas in macaque monkey. Int. J. Psychophysiol. 2003, 50:19-26.
43. Saenz M., Lewis L.B., Huth A.G., Fine I., Koch C. Visual motion area MT+/V5 responds to auditory motion in human sight-recovery subjects. J. Neurosci. 2008, 28:5141-5148.
44. Sathian K. Visual cortical activity during tactile perception in the sighted and visually deprived. Dev. Psychobiol. 2005, 46:279-286.
45. Shimony J.S., Burton H., Epstein A.A., McLaren D.G., Sun S.W., Snyder A.Z. Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cereb. Cortex 2006, 61:1653-1661.
46. Smith A.T., Wall M.B., Williams A.L., Singh K.D. Sensitivity to optic flow in human cortical areas MT and MST. Eur. J. Neurosci. 2006, 23:561-569.
47. Stiers P., Peeters R., Lagae L., Van Hecke P., Sunaert S. Mapping multiple visual areas in the human brain with a short fMRI sequence. Neuroimage 2006, 29:74-89.
48. Summers I.R., Francis S.T., Bowtell R.W., McGlone F.P., Clemence M. A functional-magnetic-resonance-imaging investigation of cortical activation from moving vibrotactile stimuli on the fingertip. J. Acoust. Soc. Am. 2009, 125:1033-1039.
49. Sunaert S., Van Hecke P., Marchal G., Orban G.A. Motion-responsive regions of the human brain. Exp. Brain Res. 1999, 127:355-370.
50. Tootell R.B., Mendola J.D., Hadjikhani N.K., Ledden P.J., Liu A.K., Reppas J.B., Sereno M.I., Dale A.M. Functional analysis of V3A and related areas in human visual cortex. J. Neurosci. 1997, 17:7060-7078.
51. Week R., Horwitz B., Aziz-Sultan A., Tian B., Wessinger C.M., Cohen L.G., Hallett M., Rauschecker J.P. A positron emission tomographic study of auditory localization in the congenitally blind. J. Neurosci. 2000, 13:1-7.
52. Wittenberg G.F., Werhahn K.J., Wasserman E.M., Herscovitch P., Cohen L.G. Functional connectivity between somatosensory and visual cortex in early blind humans. Eur. J. Neurosci. 2004, 20:1923-1927.