Effects of visual experience on the human MT+ functional connectivity networks: An fMRI study of motion perception in sighted and congenitally blind individuals

Frontiers in Systems Neuroscience

Volumn 4, Issue , 2010, Pages

  Sani, Lorenzo ^a,b   Ricciardi, Emiliano ^a,c   Gentili, Claudio ^a,c   Vanello, Nicola ^a,c   Haxby, James V ^d   Pietrini, Pietro ^a,b  

^a UNIVERSITY OF PISA   (Italy)

^b UNIVERSITY HOSPITAL OF PISA   (Italy)

^c CNR   (Italy)

^d Dartmouth College   (United States)

Author keywords

Blindness; fMRI; Functional connectivity; Human middle temporal complex; Supramodality; Tactile motion; Visual motion

Indexed keywords

ADULT; ARTICLE; CASE REPORT; CONGENITAL BLINDNESS; CONTROLLED STUDY; EXTRASTRIATE BODY AREA; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFERIOR FRONTAL GYRUS; INFERIOR TEMPORAL CORTEX; MALE; MIDDLE TEMPORAL GYRUS; MOVEMENT PERCEPTION; NERVE CELL NETWORK; OCCIPITAL LOBE; POSTERIOR PARIETAL CORTEX; PREMOTOR CORTEX; SOMATOSENSORY CORTEX; STIMULUS RESPONSE; TACTILE STIMULATION; VISUAL STIMULATION;

EID: 79957880202     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2010.00159     Document Type: Article

References (56)

1. Amedi, A., Malach, R., Hendler, T., Peled, S., and Zohary, E. (2001). Visuo-haptic object-related activation in the ventral visual pathway. Nat. Neurosci. 4, 324-330.
2. Amedi, A., von Kriegstein, K., van Atteveldt, N. M., Beauchamp, M. S., and Naumer, M. J. (2005). Functional imaging of human crossmodal identification and object recognition. Exp. Brain Res. 166, 559-571.
3. Beauchamp, M. S., Yasar, N. E., Frye, R. E., and Ro, T. (2008). Touch, sound and vision in human superior temporal sulcus. Neuroimage 41, 1011-1020.
4. Beauchamp, M. S., Yasar, N. E., Kishan, N., and Ro, T. (2007). Human MST but not MT responds to tactile stimulation. J. Neurosci. 27, 8261-8267.
5. Birn, R. M., Diamond, J. B., Smith, M. A., and Bandettini, P. A. (2006). Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 31, 1536-1548.
6. Biswal, B., Yetkin, F. Z., Haughton, V. M., and Hyde, J. S. (1995). Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 34, 537-541.
7. Bonino, D., Ricciardi, E., Sani, L., Gentili, C., Vanello, N., Guazzelli, M., Vecchi, T., and Pietrini, P. (2008). Tactile spatial working memory activates the dorsal extrastriate cortical pathway in congenitally blind individuals. Arch. Ital. Biol. 146, 133-146.
8. Bremmer, F., Schlack, A., Shah, N. J., Zafiris, O., Kubischik, M., Hoffmann, K., Zilles, K., and Fink, G. R. (2001). Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron 29, 287-296.
9. Cattaneo, Z., Vecchi, T., Cornoldi, C., Mammarella, I., Bonino, D., Ricciardi, E., and Pietrini, P. (2008). Imagery and spatial processes in blindness and visual impairment. Neurosci. Biobehav. Rev. 32, 1346-1360.
10. Chang, C., and Glover, G. H. (2009). Effects of model-based physiological noise correction on default mode network anti-correlations and correlations. Neuroimage 47, 1448-1459.
11. Cordes, D., Haughton, V. M., Arfanakis, K., Carew, J. D., Turski, P. A., Moritz, C. H., Quigley, M. A., and Meyerand, M. E. (2001). Frequencies contributing tofunctional connectivity in the cerebral cortex in resting-state data. AJNR Am. J. Neuroradiol. 22, 1326-1333.
12. Cowey, A. (2010). The blindsight saga. Exp. Brain Res. 200, 3-24.
13. Cox, R. W. (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162-173.
14. Fox, M. D., Snyder, A. Z., Vincent, J. L., Corbetta, M., Van Essen, D. C., and Raichle, M. E. (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U.S.A. 102, 9673-9678.
15. Friston, K. J., Frith, C. D., Liddle, P. F., and Frackowiak, R. S. J. (1993). Functional connectivity: the principal-component analysis of large (PET) data sets. J. Cereb. Blood Flow Metab. 13, 5-14.
16. Fujii, T., Tanabe, H. C., Kochiyama, T., and Sadato, N. (2009). An investigation of cross-modal plasticity of effective connectivity in the blind by dynamic causal modeling of functional MRI data. Neurosci. Res. 65, 175-186.
17. Gaglianese, A., Sani, L., Roebroeck, A., Handjaras, G., Bernardi, G., Costagli, M., Ricciardi, E., and Pietrini, P. (2010). fMRI Functional and Effective Connectivity in Humans Supports a Direct Pathway from Thalamus to hMT·+. Presented at the 16th Annual Meeting of the Organization for Human Brain Mapping, Barcelona.
18. Goebel, R., Khorram-Sefat, D., Muckli, L., Hacker, H., and Singer, W. (1998). The constructive nature of vision: direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery. Eur. J. Neurosci. 10, 1563-1573.
19. Grefkes, C., Weiss, P. H., Zilles, K., and Fink, G. R. (2002). Crossmodal processing of object features in human anterior intraparietal cortex: an fMRI study implies equivalencies between humans and monkeys. Neuron 35, 173-184.
20. Greicius, M. D., Krasnow, B., Reiss, A. L., and Menon, V. (2003). Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc. Natl. Acad. Sci. U.S.A. 100, 253-258.
21. Hagen, M. C., Franzen, O., McGlone, F., Essick, G., Dancer, C., and Pardo, J. V. (2002). Tactile motion activates the human middle temporal/V5 (MT/ V5) complex. Eur. J. Neurosci. 16, 957-964.
22. Hampson, M., Olson, I. R., Leung, H. C., Skudlarski, P., and Gore, J. C. (2004). Changes in functional connectivity of human MT/V5 with visual motion input. Neuroreport 15, 1315-1319.
23. Horwitz, B. (2003). The elusive concept of brain connectivity. Neuroimage 19, 466-470.
24. Horwitz, B., Warner, B., Fitzer, J., Tagamets, M. A., Husain, F. T., and Long, T. W. (2005). Investigating the neural basis for functional and effective connectivity. Application to fMRI. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 360, 1093-1108.
25. Jiang, A., Kennedy, D. N., Baker, J. R., Weisskoff, R. M., Tootell, B. H., Woods, R. P., Benson, R. R., Kwong, K. K., Brady, T. J., Rosen, B. R., and Belliveau, J. W. (1995). Motion detection and correction in functional MR imaging. Hum. Brain Mapp. 3, 224-235.
26. Kourtzi, Z., and Kanwisher, N. (2000). Activation in human MT/MST by static images with implied motion. J. Cogn. Neurosci. 12, 48-55.
27. Kupers, R., Chebat, D. R., Madsen, K. H., Paulson, O. B., and Ptito, M. (2010). Neural correlates of virtual route recognition in congenital blindness. Proc. Natl. Acad. Sci. U.S.A. 107, 12716-12721.
28. Kupers, R., Fumal, A., Maertens de Noordhout, A., Gjedde, A., Schoenen, J., and Ptito, M. (2006). Transcranial magnetic stimulation of the visual cortex induces somatotopically organized qualia in blind subjects. Proc. Natl. Acad. Sci. U.S.A. 103, 13256-13260.
29. Liang, M., Zhou, Y., Jiang, T., Liu, Z., Tian, L., Liu, H., and Hao, Y. (2006). Widespread functional disconnectivity in schizophrenia with resting-state functional magnetic resonance imaging. Neuroreport 17, 209-213.
30. Lowe, M. J., Mock, B. J., and Sorenson, J. A. (1998). Functional connectivity in single and multislice echo planar imaging using resting state fluctuations. Neuroimage 7, 119-132.
31. Mahon, B. Z., Anzellotti, S., Schwarzbach, J., Zampini, M., and Caramazza, A. (2009). Category-specific organization in the human brain does not require visual experience. Neuron 63, 397-405.
32. Mahon, B. Z., Schwarzbach, J., and Caramazza, A. (2010). The representation of tools in left parietal cortex is independent of visual experience. Psychol. Sci. 21,764-771.
33. Mather, G., Pavan, A., Campana, G., and Casco, C. (2008). The motion aftereffect reloaded. Trends Cogn. Sci. 12, 481-487.
34. Matteau, I., Kupers, R., Ricciardi, E., Pietrini, P., and Ptito, M. (2010). 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 Res. Bull. 82, 264-270.
35. Mennes, M., Kelly, C., Zuo, X. N., Di Martino, A., Biswal, B. B., Castellanos, F. X., and Milham, M. P. (2010). Interindividual differences in resting-state functional connectivity predict taskinduced BOLD activity. Neuroimage 50, 1690-1701.
36. Murphy, K., Birn, R. M., Handwerker, D. A., Jones, T. B., and Bandettini, P. A. (2009). The impact of global signal regression on resting state correlations: are anti-correlated networks introduced? Neuroimage 44, 893-905.
37. Peltier, S., Stilla, R., Mariola, E., LaConte, S., Hu, X., and Sathian, K. (2007). Activity and effective connectivity of parietal and occipital cortical regions during haptic shape perception. Neuropsychologia 45, 476-483.
38. Pietrini, P., Furey, M. L., Ricciardi, E., Gobbini, M. I., Wu, W. H., Cohen, L., Guazzelli, M., and Haxby, J. V. (2004). Beyond sensory images: object-based representation in the human ventral pathway. Proc. Natl. Acad. Sci. U.S.A. 101, 5658-5663.
39. Pietrini, P., Ptito, M., and Kupers, R. (2009). "Blindness and consciousness: new light from the dark," in The Neurology of Consciousness, eds S. Laureys and G. Tononi (Amsterdam: Academic Press), 360-374.
40. Poirier, C., Collignon, O., Scheiber, C., Renier, L., Vanlierde, A., Tranduy, D., Veraart, C., and De Volder, A. G. (2006). Auditory motion perception activates visual motion areas in early blind subjects. Neuroimage 31, 279-285.
41. Ptito, M., Fumal, A., de Noordhout, A. M., Schoenen, J., Gjedde, A., and Kupers, R. (2008). TMS of the occipital cortex induces tactile sensations in the fingers of blind Braille readers. Exp. Brain Res. 184, 193-200.
42. Ptito, M., and Kupers, R. (2005). Crossmodal plasticity in early blindness. J. Integr. Neurosci. 4, 479-488.
43. Ptito, M., Matteau, I., Gjedde, A., and Kupers, R. (2009). Recruitment of the middle temporal area by tactile motion in congenital blindness. Neuroreport 20, 543-547.
44. Raichle, M. E., MacLeod, A. M., Snyder, A. Z., Powers, W. J., Gusnard, D. A., and Shulman, G.L. (2001). A default mode of brain function. Proc. Natl. Acad. Sci. U.S.A. 98, 676-682.
45. Ricciardi, E., Basso, D., Bonino, D., Sani, L., Guazzelli, M., Vecchi, T., Pietrini, P., and Miniussi, C. (2010). Functional inhibition of the human middle temporal cortex affects non-visual motion perception: a repetitive transcranial magnetic stimulation study during tactile speed discrimination. Exp. Biol. Med. (Maywood) doi: 10.1258/ ebm.2010.010230.
46. Ricciardi, E., Bonino, D., Gentili, C., Sani, L., Pietrini, P., and Vecchi, T. (2006). Neural correlates of spatial working memory in humans: a functional magnetic resonance imaging study comparing visual and tactile processes. Neuroscience 139, 339-349.
47. Ricciardi, E., Bonino, D., Sani, L., Vecchi, T., Guazzelli, M., Haxby, J. V., Fadiga, L., and Pietrini, P. (2009). Do we really need vision? How blind people "see" the actions of others. J. Neurosci. 29, 9719-9724.
48. Ricciardi, E., Vanello, N., Sani, L., Gentili, C., Scilingo, E. P., Landini, L., Guazzelli, M., Bicchi, A., Haxby, J. V., and Pietrini, P. (2007). The effect of visual experience on the development of functional architecture in hMT+. Cereb. Cortex 17, 2933-2939.
49. Shulman, G. L., Schwarz, J., Miezin, F. M., and Petersen, S. E. (1998). Effect of motion contrast on human cortical responses to moving stimuli. J. Neurophysiol. 79, 2794-2803.
50. Summers, I. R., Francis, S. T., Bowtell, R. W., McGlone, F. P., and Clemence, M. (2009). A functional-magneticresonance- imaging investigation of cortical activation from moving vibrotactile stimuli on the fingertip. J. Acoust. Soc. Am. 125, 1033-1039.
51. Talairach, J., and Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain. New York: Thieme Classics.
52. Tootell, R. B., Reppas, J. B., Dale, A. M., Look, R. B., Sereno, M. I., Malach, R., Brady, T. J., and Rosen, B. R. (1995). Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature 375, 139-141.
53. Watson, J. D., Myers, R., Frackowiak, R. S., Hajnal, J. V., Woods, R. P., Mazziota, J. C., Shipp, S., and Zeki, S. (1993). Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. Cereb. Cortex 3, 79-94.
54. Whalley, H. C., Simonotto, E., Marshall, I., Owens, D. G., Goddard, N. H., Johnstone, E. C., and Lawrie, S. M. (2005). Functional disconnectivity in subjects at high genetic risk of schizophrenia. Brain 128, 2097-2108.
55. Wittenberg, G. F., Werhahn, K. J., Wassermann, E. M., Herscovitch, P., and Cohen, L. G. (2004). Functional connectivity between somatosensory and visual cortex in early blind humans. Eur. J. Neurosci. 20, 1923-1927.
56. Zeki, S., Watson, J. D., and Frackowiak, R. S. (1993). Going beyond the information given: the relation of illusoryvisual motion to brain activity. Proc. Biol. Sci. 252, 215-222.