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Alterations of the visual pathways in congenital blindness

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Abstract

We used whole brain MRI voxel-based morphometry (VBM) to study the anatomical organization of the visual system in congenitally blind (CB) adults. Eleven CB without a history of visual perception were compared with 21 age- and sex-matched normal-sighted controls (NS). CB showed significant atrophy of the geniculo-striate system, encompassing the optic nerves, the optic chiasm, the optic radiations and the primary visual cortex (BA17). The volume decrease in BA17 reached 25% in both hemispheres. The pulvinar and its projections to the associative visual areas were also dramatically altered, BA18/19 and the middle temporal cortex (MT) showing volume reductions of up to 20%. Additional significant white matter alterations were observed in the inferior longitudinal tract and in the posterior part of the corpus callosum, which links the visual areas of both hemispheres. Our data indicate that the afferent projections to the visual cortex in CB are largely atrophied. Despite the massive volume reductions in the occipital lobes, there is compelling evidence from the literature (reviewed in Noppeney 2007; Ptito and Kupers 2005) that blind subjects activate their visual cortex when performing tasks that involve somatosensory or auditory inputs, suggesting a reorganization of the neural pathways that transmit sensory information to the visual cortex.

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References

  • Amunts K, Malikovic A, Mohlberg H, Schormann T, Zilles K (2000) Brodmann’s areas 17 and 18 brought into stereotaxic space—where and how variable? Neuroimage 11:66–84

    Article  PubMed  CAS  Google Scholar 

  • Ashburner J, Friston K (1997) Multimodal image coregistration and partitioning—a unified framework. Neuroimage 6:209–217

    Article  PubMed  CAS  Google Scholar 

  • Ashburner J, Friston KJ (2000) Voxel-based morphometry—the methods. Neuroimage 11:805–821

    Article  PubMed  CAS  Google Scholar 

  • Breitenseher M, Uhl F, Prayer Wimberger D, Deecke L, Trattnig S, Kramer J (1998) Morphological dissociation between visual pathways and cortex: MRI of visually-deprived patients with congenital peripheral blindness. Neuroradiology 40:424–427

    Article  PubMed  CAS  Google Scholar 

  • Brunquell PJ, Papale JH, Horton JC, Williams RS, Zgrabik MJ, Albert DM, Hedley-Whyte ET (1984) Sex-linked hereditary bilateral anophthalmos: pathologic and radiologic correlation. Arch Ophthalmol 102:108–113

    PubMed  CAS  Google Scholar 

  • Burgel U, Amunts K, Hoemke L, Mohlberg H, Gilsbach JM, Zilles K (2006) White matter fiber tracts of the human brain: three-dimensional mapping at microscopic resolution, topography and intersubject variability. Neuroimage 29:1092–1105

    Article  PubMed  Google Scholar 

  • Campbell G, Frost DO (1988) Synaptic organization of anomalous retinal projections to the somatosensory and auditory thalamus: target-controlled morphogenesis of axon terminals and synaptic glomeruli. J Comp Neurol 272:383–408

    Article  PubMed  CAS  Google Scholar 

  • Carmichael ST, Price JL (1995) Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J Comp Neurol 363:642–664

    Article  PubMed  CAS  Google Scholar 

  • Catani M, Jones DK, Donato R, Ffytche DH (2003) Occipito-temporal connections in the human brain. Brain 126:2093–2107

    Article  PubMed  Google Scholar 

  • Chebat DR, Chen JK, Schneider F, Ptito A, Kupers R, Ptito M (2007) Alterations in right posterior hippocampus in early blind individuals. Neuroreport 18:329–333

    Article  PubMed  Google Scholar 

  • De Volder AG, Bol A, Blin J, Grandin G, Michel C, Veraart C (1997) Brain energy metabolism in early blind subjects: neural activity in the visual cortex. Brain Res 750:235–244

    Article  PubMed  Google Scholar 

  • Eickhoff SB, Paus T, Caspers S, Grosbras MH, Evans A, Zilles K, Amunts K (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36:511–521

    Article  PubMed  Google Scholar 

  • Falchier A, Clavagnier S, Barone P, Kennedy H (2002) Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci 22:5749–5759

    PubMed  CAS  Google Scholar 

  • Frost DO (1981) Orderly anomalous retinal projections to the medial geniculate, ventrobasal, and lateral posterior nuclei of the hamster. J Comp Neurol 203:227–256

    Article  PubMed  CAS  Google Scholar 

  • Frost DO, Métin C (1985) Induction of functional retinal projections to the somatosensory system. Nature 317:162–164

    Article  PubMed  CAS  Google Scholar 

  • Frost DO, Boire D, Gingras G, Ptito M (2000) Surgically created neural pathways mediate visual pattern discrimination. Proc Natl Acad Sci USA 97:11068–11073

    Article  PubMed  CAS  Google Scholar 

  • Fu KMG, Johnston TA, Shah AS, Arnold L, Smiley J, Hackett TA, Garraghty PE, Schroeder CE (2003) Auditory cortical neurons respond to somatosensory stimulation. J Neurosci 23:7510–7515

    PubMed  CAS  Google Scholar 

  • Foxe JJ, Schroeder E (2005) The case for feedforward multisensory convergence during early cortical processing. Neuroreport 16:419–423

    Article  PubMed  Google Scholar 

  • Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15:870–878

    Article  PubMed  Google Scholar 

  • Good CD, Johnsrude IS, Asburner J, Henson RN, Friston KJ, Frackowiack RS (2001) A voxel-based morphometry study of ageing in 465 normal adult human brains. Neuroimage 14:31–36

    Google Scholar 

  • Hyvärinen J, Carlson S, Hyvärinen L (1981) Early visual deprivation alters modality of neuronal responses in area 19 of monkey cortex. Neurosci Lett 26:239–243

    Article  PubMed  Google Scholar 

  • Isaacs EB, Edmonds CJ, Chong WK, Lucas A, Morley R, Gadian DG (2004) Brain morphometry and IQ measurements in preterm children. Brain 127:2595–2607

    Article  PubMed  CAS  Google Scholar 

  • Kupers R, Fumal A, de Noordhout AM, Gjedde A, Schoenen J, Ptito M (2006) Transcranial magnetic stimulation of the visual cortex induces somatotopically organized qualia in blind subjects. Proc Natl Acad Sci USA 103:13256–13260

    Article  PubMed  CAS  Google Scholar 

  • Liu Y, Yu C, Liang M, Li J, Tian L, Zhou Y, Qin W, Li K, Jiang T (2007) Whole brain functional connectivity in the early blind. Brain (Epub ahead of print)

  • Malikovic A, Amunts K, Schleicher A, Mohlberg H, Eickhoff SB, Wilms M, Palomero-Gallagher N, Armstrong E, Zilles K (2007) Cytoarchitectonic analysis of the human extrastriate cortex in the region of V5/MT+: a probabilistic, stereotaxic map of area hOc5. Cereb Cortex 17:562–574

    Article  PubMed  Google Scholar 

  • Metin C, Frost DO (1989) Visual responses of neurons in somatosensory cortex of hamsters with experimentally induced retinal projections to somatosensory thalamus. Proc Natl Acad Sci USA 86:357–361

    Article  PubMed  CAS  Google Scholar 

  • Merabet LB, Rizzo JF, Amedi A, Somers DC, Pascual-Leone A (2005) What blindness can tell us about seeing again: merging neuroplasticity and neuroprostheses. Nat Rev Neurosci 6:71–77

    Article  PubMed  CAS  Google Scholar 

  • Molholm S, Sehatpour P, Mehta AD, Shpaner M, Gomez-Ramirez M, Ortigue S, Dyke JP, Schwartz TH, Foxe JJ (2006) Audio-visual multisensory integration in superior parietal lobule revealed by human intracranial recordings. J Neurophysiol 96:721–729

    Article  PubMed  Google Scholar 

  • Noppeney U (2007) The effects of visual deprivation on functional and structural organization of the human brain. Neurosci Biobehav Rev [Epub ahead of print]

  • Noppeney U, Friston KJ, Ashburner J, Frackowiak R, Price CJ (2005) Early visual deprivation induces structural plasticity in grey and white matter. Curr Biol 15:488–490

    Article  CAS  Google Scholar 

  • Pan WJ, Wu G, Li CX, Lin F, Sun J, Lei H (2007) Progressive atrophy in the optic pathway and visual cortex of early blind Chinese adults: a voxel-based morphometry magnetic resonance imaging study. Neuroimage 37:212–220

    Article  PubMed  Google Scholar 

  • Ptito M (2003) Functions of the corpus callosum as derived from split-brain studies in cats. In: Zaidel E, Iacoboni M (Eds) The parallel brain: the cognitive neuroscience of the corpus callosum. MIT Press, Massachusetts, pp. 139–153

  • Ptito M, Desgent S (2006) Sensory input-based adaptation and brain architecture. In: Baltes P, Reuter-Lorenz P, Rösler F (eds) Lifespan development and the brain: the perspective of biocultural co-constructivism. Cambridge University Press, Cambridge, pp 111–133

    Google Scholar 

  • Ptito M, Kupers R (2005) Cross-modal plasticity in early blindness. J Integr Neurosci 4:479–488

    Article  PubMed  Google Scholar 

  • Ptito M, Giguère JF, Boire D, Frost DO, Casanova C (2001) When the auditory cortex turns visual. Prog Brain Res 134:447–458

    Article  PubMed  CAS  Google Scholar 

  • Ptito M, Moesgaard SM, Gjedde A, Kupers R (2005) Cross-modal plasticity revealed by electrotactile stimulation of the tongue in the congenitally blind. Brain 128:606–614

    Article  PubMed  Google Scholar 

  • Rockland KS, Ojima H (2003) V1 as a multimodal convergence area. Int J Psychophysiol 50:19–26

    Article  PubMed  Google Scholar 

  • Rorden C, Brett M (2000) Stereotaxic display of brain lesions. Behav Neurol 12:191–200

    PubMed  Google Scholar 

  • Sadato N (2005) How the blind “see” Braille: lessons from functional magnetic resonance imaging. Neuroscientist 11:577–582

    Article  PubMed  Google Scholar 

  • Sathian K (2005) Visual cortical activity during tactile perception in the sighted and visually deprived. Dev Psychobiol 46:279–228

    Article  PubMed  CAS  Google Scholar 

  • Schroeder CE, Lindsey RW, Specht C, Marcovici A, Smiley JF, Javitt DC (2001) Somatosensory input to auditory association cortex in the macaque monkey. J Neurophysiol 85:1322–1327

    PubMed  CAS  Google Scholar 

  • Shimony JS, Burton H, Epstein AA, McLaren DG, Sun SW, Snyder AZ (2005) Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cereb Cortex 16:1653–1661

    Article  PubMed  Google Scholar 

  • Sur M, Garraghty PE, Roe AW (1988) Experimentally induced visual projections into auditory thalamus and cortex. Science 242:1437–1441

    Article  PubMed  CAS  Google Scholar 

  • Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, Stuttgart

  • Tusa RJ, Ungerleider LG (1985) The inferior longitudinal fasciculus: a reexamination in humans and monkeys. Ann Neurol 18:583–591

    Article  PubMed  CAS  Google Scholar 

  • Von Melchner L, Pallas SL, Sur M (2000) Visual behaviour mediated by retinal projections directed to the auditory pathway. Nature 404:871–876

    Article  CAS  Google Scholar 

  • Wittenberg GF, Werhahn KJ, Wasserman EM, Herscovitch P, Cohen LG (2004) Functional connectivity between somatosensory and visual cortex in early blind humans. Eur J Neurosci 20:1923–1927

    Article  PubMed  Google Scholar 

  • Yu C, Shu N, Li J, Qin W, Jiang T, Li K (2007) Plasticity of the corticospinal tract in early blindness revealed by quantitative analysis of fractional anisotropy based on diffusion tensor tractography. Neuroimage 36:411–417

    Article  PubMed  Google Scholar 

  • Zhou YD, Fuster JM (1996) Mnemonic neuronal activity in somatosensory cortex. Proc Natl Acad Sci USA 93:10533–10537

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work is supported by grants from the Harland Sanders Foundation (MP) and the Lundbeck Foundation (RK).

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Correspondence to Maurice Ptito.

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Ptito, M., Schneider, F.C.G., Paulson, O.B. et al. Alterations of the visual pathways in congenital blindness. Exp Brain Res 187, 41–49 (2008). https://doi.org/10.1007/s00221-008-1273-4

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  • DOI: https://doi.org/10.1007/s00221-008-1273-4

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