[en] The study of the congenitally blind (CB) represents a unique opportunity to explore experience-dependant plasticity in a sensory region deprived of its natural inputs since birth. Although several studies have shown occipital regions of CB to be involved in nonvisual processing, whether the functional organization of the visual cortex observed in sighted individuals (SI) is maintained in the rewired occipital regions of the blind has only been recently investigated. In the present functional MRI study, we compared the brain activity of CB and SI processing either the spatial or the pitch properties of sounds carrying information in both domains (i.e., the same sounds were used in both tasks), using an adaptive procedure specifically designed to adjust for performance level. In addition to showing a substantial recruitment of the occipital cortex for sound processing in CB, we also demonstrate that auditory-spatial processing mainly recruits the right cuneus and the right middle occipital gyrus, two regions of the dorsal occipital stream known to be involved in visuospatial/motion processing in SI. Moreover, functional connectivity analyses revealed that these reorganized occipital regions are part of an extensive brain network including regions known to underlie audiovisual spatial abilities (i.e., intraparietal sulcus, superior frontal gyrus). We conclude that some regions of the right dorsal occipital stream do not require visual experience to develop a specialization for the processing of spatial information and to be functionally integrated in a preexisting brain network dedicated to this ability.
Disciplines :
Radiology, nuclear medicine & imaging
Author, co-author :
Collignon, Olivier
Vandewalle, Gilles ; Institut Universitaire de Gériatrie de Montréal > Unité de Neuroimagerie Fonctionnelle
Rauschecker JP (1995) Compensatory plasticity and sensory substitution in the cerebral cortex. Trends Neurosci 18:36-43.
Bavelier D, Neville HJ (2002) Cross-modal plasticity: Where and how? Nat Rev Neurosci 3:443-452.
Grill-Spector K, Malach R (2004) The human visual cortex. Annu Rev Neurosci 27: 649-677. (Pubitemid 39050416)
Wandell BA, Dumoulin SO, Brewer AA (2007) Visual field maps in human cortex. Neuron 56:366-383.
Stevens AA, Snodgrass M, Schwartz D, Weaver K (2007) Preparatory activity in occipital cortex in early blind humans predicts auditory perceptual performance. J Neurosci 27:10734-10741. (Pubitemid 47535860)
Kujala T, Alho K, Näätänen R (2000) Cross-modal reorganization of human cortical functions. Trends Neurosci 23:115-120. (Pubitemid 30110627)
Lewis LB, Saenz M, Fine I (2010) Mechanisms of cross-modal plasticity in early-blind subjects. J Neurophysiol 104:2995-3008.
Burton H, Sinclair RJ, Dixit S (2010) Working memory for vibrotactile frequencies: Comparison of cortical activity in blind and sighted individuals. Hum Brain Mapp 31: 1686-1701.
Collignon O, Voss P, Lassonde M, Lepore F (2009) Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects. Exp Brain Res 192:343-358.
Mishkin M, Lewis ME, Ungerleider LG (1982) Equivalence of parieto-preoccipital subareas for visuospatial ability in monkeys. Behav Brain Res 6:41-55. (Pubitemid 12007157)
Haxby JV, et al. (1991) Dissociation of object and spatial visual processing pathways in human extrastriate cortex. Proc Natl Acad Sci USA 88:1621-1625. (Pubitemid 21916277)
Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15:20-25.
Pietrini P, et al. (2004) Beyond sensory images: Object-based representation in the human ventral pathway. Proc Natl Acad Sci USA 101:5658-5663. (Pubitemid 38481212)
Mahon BZ, Anzellotti S, Schwarzbach J, Zampini M, Caramazza A (2009) Category-specific organization in the human brain does not require visual experience. Neuron 63:397-405.
Amedi A, et al. (2007) Shape conveyed by visual-to-auditory sensory substitution activates the lateral occipital complex. Nat Neurosci 10:687-689. (Pubitemid 46828516)
Gougoux F, et al. (2009) Voice perception in blind persons: A functional magnetic resonance imaging study. Neuropsychologia 47:2967-2974.
Collignon O, Lassonde M, Lepore F, Bastien D, Veraart C (2007) Functional cerebral reorganization for auditory spatial processing and auditory substitution of vision in early blind subjects. Cereb Cortex 17:457-465. (Pubitemid 46052783)
Ricciardi E, et al. (2007) The effect of visual experience on the development of functional architecture in hMT+. Cereb Cortex 17:2933-2939. (Pubitemid 350129449)
Saenz M, Lewis LB, Huth AG, Fine I, Koch C (2008) Visual motion area MT+/V5 responds to auditory motion in human sight-recovery subjects. J Neurosci 28: 5141-5148.
Weeks R, et al. (2000) A positron emission tomographic study of auditory localization in the congenitally blind. J Neurosci 20:2664-2672. (Pubitemid 30220354)
Poirier C, et al. (2006) Auditory motion perception activates visual motion areas in early blind subjects. Neuroimage 31:279-285. (Pubitemid 43728973)
Renier LA, et al. (2010) Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind. Neuron 68:138-148.
Rauschecker JP, Tian B (2000) Mechanisms and streams for processing of "what" and "where" in auditory cortex. Proc Natl Acad Sci USA 97:11800-11806.
Alain C, Arnott SR, Hevenor S, Graham S, Grady CL (2001) "What" and "where" in the human auditory system. Proc Natl Acad Sci USA 98:12301-12306.
Friston KJ, Penny W (2003) Posterior probability maps and SPMs. Neuroimage 19: 1240-1249. (Pubitemid 36918260)
Laurienti PJ, et al. (2002) Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci 14:420-429. (Pubitemid 34267542)
Lomber SG, Malhotra S (2008) Double dissociation of 'what' and 'where' processing in auditory cortex. Nat Neurosci 11:609-616.
Amedi A, Floel A, Knecht S, Zohary E, Cohen LG (2004) Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects. Nat Neurosci 7:1266-1270. (Pubitemid 39426247)
Amedi A, Raz N, Pianka P, Malach R, Zohary E (2003) Early 'visual' cortex activation correlates with superior verbal memory performance in the blind. Nat Neurosci 6: 758-766.
Tootell RB, et al. (1997) Functional analysis of V3A and related areas in human visual cortex. J Neurosci 17:7060-7078. (Pubitemid 27427885)
Tootell RB, et al. (1995) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J Neurosci 15:3215-3230.
Sunaert S, Van Hecke P, Marchal G, Orban GA (1999) Motion-responsive regions of the human brain. Exp Brain Res 127:355-370. (Pubitemid 29389650)
Watson JD, et al. (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. (Pubitemid 23100833)
Eickhoff SB, et al. (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36:511-521. (Pubitemid 46907638)
Gougoux F, Zatorre RJ, Lassonde M, Voss P, Lepore F (2005) A functional neuroimaging study of sound localization: Visual cortex activity predicts performance in early-blind individuals. PLoS Biol 3:e27.
Cornette L, et al. (1998) Human brain regions involved in direction discrimination. J Neurophysiol 79:2749-2765. (Pubitemid 28261655)
Bonda E, Petrides M, Ostry D, Evans A (1996) Specific involvement of human parietal systems and the amygdala in the perception of biological motion. J Neurosci 16: 3737-3744. (Pubitemid 26149509)
Tollin DJ, Yin TC (2002) The coding of spatial location by single units in the lateral superior olive of the cat. I. Spatial receptive fields in azimuth. J Neurosci 22: 1454-1467. (Pubitemid 34163746)
Lomber SG, Meredith MA, Kral A (2010) Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nat Neurosci 13:1421-1427.
Szczepanski SM, Konen CS, Kastner S (2010) Mechanisms of spatial attention control in frontal and parietal cortex. J Neurosci 30:148-160.
Paus T (1996) Location and function of the human frontal eye-field: A selective review. Neuropsychologia 34:475-483.
Garg A, Schwartz D, Stevens AA (2007) Orienting auditory spatial attention engages frontal eye fields and medial occipital cortex in congenitally blind humans. Neuropsychologia 45:2307-2321. (Pubitemid 46678098)
Shimony JS, et al. (2006) Diffusion tensor imaging reveals whitematter reorganization in early blind humans. Cereb Cortex 16:1653-1661. (Pubitemid 44526962)
Bedny M, Konkle T, Pelphrey K, Saxe R, Pascual-Leone A (2010) Sensitive period for a multimodal response in human visual motion area MT/MST. Curr Biol 20:1900-1906.
Innocenti GM, Price DJ (2005) Exuberance in the development of cortical networks. Nat Rev 6:955-965. (Pubitemid 41753089)
Huttenlocher PR, de Courten C (1987) The development of synapses in striate cortex of man. Hum Neurobiol 6:1-9. (Pubitemid 17058539)
Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377-401. (Pubitemid 41098910)
Falchier A, Clavagnier S, Barone P, Kennedy H (2002) Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci 22:5749-5759. (Pubitemid 35386498)
Rockland KS, Ojima H (2003) Multisensory convergence in calcarine visual areas in macaque monkey. Int J Psychophysiol 50:19-26. (Pubitemid 37162868)
Ghazanfar AA, Schroeder CE (2006) Is neocortex essentially multisensory? Trends Cogn Sci 10:278-285.
Collignon O, et al. (2008) Time-course of posterior parietal and occipital cortex contribution to sound localization. J Cogn Neurosci 20:1454-1463.
Klinge C, Eippert F, Röder B, Büchel C (2010) Corticocortical connections mediate primary visual cortex responses to auditory stimulation in the blind. J Neurosci 30: 12798-12805.
Lakatos S, Shepard RN (1997) Constraints common to apparent motion in visual, tactile, and auditory space. J Exp Psychol Hum Percept Perform 23:1050-1060. (Pubitemid 127458900)
