Diffusion tensor imaging reveals white matter reorganization in early blind humans.

Multiple functional methods including functional magnetic resonance imaging, transcranial magnetic stimulation, and positron emission tomography have shown cortical reorganization in response to blindness. We investigated microanatomical correlates of this reorganization using diffusion tensor imaging and diffusion tensor tractography (DTT). Five early blind (EB) were compared with 7 normally sighted (NS) persons. DTT showed marked geniculocalcarine tract differences between EB and NS participants. All EB participants showed evidence of atrophy of the geniculocortical tracts. Connections between visual cortex and the orbital frontal and temporal cortices were relatively preserved in the EB group. Importantly, no additional tracts were found in any EB participant. Significant alterations of average diffusivity and relative anisotropy were found in the white matter (WM) of the occipital lobe in the EB group. These observations suggest that blindness leads to a reorganization of cerebral WM and plausibly support the hypothesis that visual cortex functionality in blindness is primarily mediated by corticocortical as opposed to thalamocortical connections.

[1]  W. Cowan.  Anterograde and Retrograde Transneuronal Degeneration in the Central and Peripheral Nervous System , 1970 .

[2]  Walle J. H. Nauta,et al.  Contemporary Research Methods in Neuroanatomy , 1970, Springer Berlin Heidelberg.

[3]  P. Rakic,et al.  Development of visual centers in the primate brain depends on binocular competition before birth. , 1981, Science.

[4]  J. Vonsattel,et al.  Direct demonstration of transsynaptic degeneration in the human visual system: a comparison of retrograde and anterograde changes , 1982, Journal of neurology, neurosurgery, and psychiatry.

[5]  J. Horton,et al.  Sex-linked hereditary bilateral anophthalmos. Pathologic and radiologic correlation. , 1984, Archives of ophthalmology.

[6]  P. Rakic.  Specification of cerebral cortical areas. , 1988, Science.

[7]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[8]  J. Tsuruda,et al.  Diffusion-weighted MR imaging of anisotropic water diffusion in cat central nervous system. , 1990, Radiology.

[9]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

[10]  J V Hajnal,et al.  Normal and abnormal white matter tracts shown by MR imaging using directional diffusion weighted sequences. , 1990, Journal of computer assisted tomography.

[11]  T. Chenevert,et al.  Anisotropic diffusion in human white matter: demonstration with MR techniques in vivo. , 1990, Radiology.

[12]  D. C. Essen,et al.  Modular and hierarchical organization of extrastriate visual cortex in the macaque monkey. , 1990, Cold Spring Harbor symposia on quantitative biology.

[13]  P. Rakić,et al.  A novel cytoarchitectonic area induced experimentally within the primate visual cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[14]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[15]  D C Van Essen,et al.  Information processing in the primate visual system: an integrated systems perspective. , 1992, Science.

[16]  L O Hall,et al.  Review of MR image segmentation techniques using pattern recognition. , 1993, Medical physics.

[17]  P. Basser,et al.  Estimation of the effective self-diffusion tensor from the NMR spin echo. , 1994, Journal of magnetic resonance. Series B.

[18]  J. Rauschecker.  Compensatory plasticity and sensory substitution in the cerebral cortex , 1995, Trends in Neurosciences.

[19]  R. Ilmoniemi,et al.  Visual cortex activation in blind humans during sound discrimination , 1995, Neuroscience Letters.

[20]  Jack L. Lancaster,et al.  A modality‐independent approach to spatial normalization of tomographic images of the human brain , 1995 .

[21]  Abraham Z. Snyder,et al.  CHAPTER 26 – Difference Image vs Ratio Image Error Function Forms in PET—PET Realignment , 1996 .

[22]  P. Basser,et al.  Toward a quantitative assessment of diffusion anisotropy , 1996, Magnetic resonance in medicine.

[23]  M. Hallett,et al.  Activation of the primary visual cortex by Braille reading in blind subjects , 1996, Nature.

[24]  F. Rösler,et al.  Event-related potentials during auditory and somatosensory discrimination in sighted and blind human subjects. , 1996, Brain research. Cognitive brain research.

[25]  R. Myers.  Quantification of brain function using PET , 1996 .

[26]  E. Akbudak,et al.  Encoding of anisotropic diffusion with tetrahedral gradients: A general mathematical diffusion formalism and experimental results , 1996, Magnetic resonance in medicine.

[27]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[28]  S. Maier,et al.  Microstructural Development of Human Newborn Cerebral White Matter Assessed in Vivo by Diffusion Tensor Magnetic Resonance Imaging , 1998, Pediatric Research.

[29]  R. Kikinis,et al.  Quantitative magnetic resonance imaging of brain development in premature and mature newborns , 1998, Annals of neurology.

[30]  M. Woldorff,et al.  Auditory attention in the congenitally blind: where, when and what gets reorganized? , 1998, Neuroreport.

[31]  Karl J. Friston,et al.  Different activation patterns in the visual cortex of late and congenitally blind subjects. , 1998, Brain : a journal of neurology.

[32]  F. Uhl,et al.  Morphological dissociation between visual pathways and cortex: MRI of visually-deprived patients with congenital peripheral blindness , 1998, Neuroradiology.

[33]  M. Hallett,et al.  Neural networks for Braille reading by the blind. , 1998 .

[34]  A. Snyder,et al.  Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. , 1998, Radiology.

[35]  C. Pierpaoli,et al.  Visualizing and characterizing white matter fiber structure and architecture in the human pyramidal tract using diffusion tensor MRI. , 1999, Magnetic resonance imaging.

[36]  S C Williams,et al.  Non‐invasive assessment of axonal fiber connectivity in the human brain via diffusion tensor MRI , 1999, Magnetic resonance in medicine.

[37]  G. Barker,et al.  Diffusion tensor imaging of lesions and normal-appearing white matter in multiple sclerosis , 1999, Neurology.

[38]  M. Solaiyappan,et al.  In vivo three‐dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging , 1999, Magnetic resonance in medicine.

[39]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[40]  A. Snyder,et al.  Quantitative diffusion-tensor anisotropy brain MR imaging: normative human data and anatomic analysis. , 1999, Radiology.

[41]  M. Raichle,et al.  Tracking neuronal fiber pathways in the living human brain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[42]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[43]  C. Poupon,et al.  Regularization of Diffusion-Based Direction Maps for the Tracking of Brain White Matter Fascicles , 2000, NeuroImage.

[44]  M. Lassonde,et al.  Brain functional reorganization in early blind humans revealed by auditory event‐related potentials , 2000, Neuroreport.

[45]  Martin Styner,et al.  Parametric estimate of intensity inhomogeneities applied to MRI , 2000, IEEE Transactions on Medical Imaging.

[46]  R Stollberger,et al.  Magnetic resonance diffusion tensor imaging for characterizing diffuse and focal white matter abnormalities in multiple sclerosis , 2000, Magnetic resonance in medicine.

[47]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[48]  J. Rauschecker,et al.  A Positron Emission Tomographic Study of Auditory Localization in the Congenitally Blind , 2000, The Journal of Neuroscience.

[49]  Sandra M. Sanabria-Bohórquez,et al.  Occipital Activation by Pattern Recognition in the Early Blind Using Auditory Substitution for Vision , 2001, NeuroImage.

[50]  E. D. de Haan,et al.  Visual imagery without visual experience: evidence from congenitally totally blind people , 2001, Neuroreport.

[51]  P. Basser,et al.  Water Diffusion Changes in Wallerian Degeneration and Their Dependence on White Matter Architecture , 2000 .

[52]  G. Pearlson,et al.  Diffusion Tensor Imaging and Axonal Tracking in the Human Brainstem , 2001, NeuroImage.

[53]  Peter Melzer,et al.  Cortical activation during Braille reading is influenced by early visual experience in subjects with severe visual disability: A correlational fMRI study , 2001, Human brain mapping.

[54]  M Cercignani,et al.  Diffusion tensor magnetic resonance imaging in multiple sclerosis , 2001, Neurology.

[55]  Á. Pascual-Leone,et al.  The metamodal organization of the brain. , 2001, Progress in brain research.

[56]  F. Rösler,et al.  Auditory memory in congenitally blind adults: a behavioral-electrophysiological investigation. , 2001, Brain research. Cognitive brain research.

[57]  M. Raichle,et al.  Adaptive changes in early and late blind: a fMRI study of Braille reading. , 2002, Journal of neurophysiology.

[58]  A. Snyder,et al.  Radial organization of developing preterm human cerebral cortex revealed by non-invasive water diffusion anisotropy MRI. , 2002, Cerebral cortex.

[59]  Manabu Honda,et al.  Critical Period for Cross-Modal Plasticity in Blind Humans: A Functional MRI Study , 2002, NeuroImage.

[60]  Steven P. Miller,et al.  Serial quantitative diffusion tensor MRI of the premature brain: Development in newborns with and without injury , 2002, Journal of magnetic resonance imaging : JMRI.

[61]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[62]  M. Raichle,et al.  Adaptive changes in early and late blind: a FMRI study of verb generation to heard nouns. , 2002, Journal of neurophysiology.

[63]  H. Kennedy,et al.  Anatomical Evidence of Multimodal Integration in Primate Striate Cortex , 2002, The Journal of Neuroscience.

[64]  J. R. Newton,et al.  Cross-modal plasticity after monocular enucleation of the adult rabbit , 2002, Experimental Brain Research.

[65]  Leah Krubitzer,et al.  Massive cross-modal cortical plasticity and the emergence of a new cortical area in developmentally blind mammals , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[66]  R C McKinstry,et al.  A prospective, longitudinal diffusion tensor imaging study of brain injury in newborns , 2002, Neurology.

[67]  P. Basser,et al.  A continuous tensor field approximation of discrete DT-MRI data for extracting microstructural and architectural features of tissue. , 2002, Journal of magnetic resonance.

[68]  A. Snyder,et al.  Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. , 2002, AJNR. American journal of neuroradiology.

[69]  T E Conturo,et al.  Diffusion tensor fiber tracking of human brain connectivity: aquisition methods, reliability analysis and biological results , 2002, NMR in biomedicine.

[70]  Annick Vanlierde,et al.  Occipito-parietal cortex activation during visuo-spatial imagery in early blind humans , 2003, NeuroImage.

[71]  Gareth J. Barker,et al.  Diffusion tractography based group mapping of major white-matter pathways in the human brain , 2003, NeuroImage.

[72]  E. R Gizewski,et al.  Cross-modal plasticity for sensory and motor activation patterns in blind subjects , 2003, NeuroImage.

[73]  Akram Aldroubi,et al.  Reconstruction of vector and tensor fields from sampled discrete data , 2003 .

[74]  R. Malach,et al.  Early ‘visual’ cortex activation correlates with superior verbal memory performance in the blind , 2003, Nature Neuroscience.

[75]  Derek K. Jones,et al.  Determining and visualizing uncertainty in estimates of fiber orientation from diffusion tensor MRI , 2003, Magnetic resonance in medicine.

[76]  H. Burton,et al.  Dissociating cortical regions activated by semantic and phonological tasks: a FMRI study in blind and sighted people. , 2003, Journal of neurophysiology.

[77]  H. Burton,et al.  Cortical activity to vibrotactile stimulation: An fMRI study in blind and sighted individuals , 2004, Human brain mapping.

[78]  Y. Mauss,et al.  Blindness and brain plasticity: contribution of mental imagery? An fMRI study. , 2004, Brain research. Cognitive brain research.

[79]  Roland G. Henry,et al.  Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns , 2004, NeuroImage.

[80]  A. Alexander,et al.  Diffusion tensor imaging of cerebral white matter: a pictorial review of physics, fiber tract anatomy, and tumor imaging patterns. , 2004, AJNR. American journal of neuroradiology.

[81]  Stefan Skare,et al.  See Blockindiscussions, Blockinstats, Blockinand Blockinauthor Blockinprofiles Blockinfor Blockinthis Blockinpublication Extensive Blockinpiano Blockinpracticing Blockinhas Blockinregionally Specific Blockineffects Blockinon Blockinwhite Blockinmatter Blockindevelopment , 2022 .

[82]  P. Alku,et al.  The role of blind humans’ visual cortex in auditory change detection , 2005, Neuroscience Letters.

[83]  Abraham Z Snyder,et al.  Registration of [18F]FDG microPET and small-animal MRI. , 2005, Nuclear medicine and biology.

[84]  Roland G. Henry,et al.  Quantitative diffusion tensor MRI fiber tractography of sensorimotor white matter development in premature infants , 2005, NeuroImage.

[85]  B. Wandell,et al.  Functional organization of human occipital-callosal fiber tracts. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Nikos Makris,et al.  An Approach To Validation of Diffusion MRI-based White Matter Tractography , 2005 .

[87]  H Burton,et al.  Reading embossed capital letters: An fMRI study in blind and sighted individuals , 2006, Human brain mapping.