Journal of Autism and Developmental Disorders

, Volume 40, Issue 1, pp 21–29 | Cite as

Increased White Matter Gyral Depth in Dyslexia: Implications for Corticocortical Connectivity

  • Manuel F. Casanova
  • Ayman S. El-Baz
  • Jay Giedd
  • Judith M. Rumsey
  • Andrew E. Switala
Original Paper

Abstract

Recent studies provide credence to the minicolumnar origin of several developmental conditions, including dyslexia. Characteristics of minicolumnopathies include abnormalities in how the cortex expands and folds. This study examines the depth of the gyral white matter measured in an MRI series of 15 dyslexic adult men and eleven age-matched comparison subjects. Measurements were based upon the 3D Euclidean distance map inside the segmented cerebral white matter surface. Mean gyral white matter depth was 3.05 mm (SD ± 0.30 mm) in dyslexic subjects and 1.63 mm (SD ± 0.15 mm) in the controls. The results add credence to the growing literature suggesting that the attained reading circuit in dyslexia is abnormal because it is inefficient. Otherwise the anatomical substratum (i.e., corticocortical connectivity) underlying this inefficient circuit is normal. A deficit in very short-range connectivity (e.g., angular gyrus, striate cortex), consistent with results of a larger gyral window, could help explain reading difficulties in patients with dyslexia. The structural findings hereby reported are diametrically opposed to those reported for autism.

Keywords

Autistic disorder Cerebrum Corpus callosum Dyslexia Gyral window 

List of Symbols

S

Surface area

V

Volume

cx

Cerebral cortex (gray matter)

cw

Cerebral white matter

\( \left\langle g \right\rangle \)

Mean gyral depth (gyral window)

References

  1. Abd El Munim, H., Fahmi, R., El-Zehiry, N. Y., Farag, A. A., & Casanova, M. F. (2007). Volumetric MRI analysis of dyslexic subjects using a level set framework. In J. S. Suri & A. Farag (Eds.), Deformable models: Theory and biomaterial applications (pp. 461–492). New York: Springer.Google Scholar
  2. Adalsteinsson, D., & Sethian, J. (1995). A fast level set method for propagating interfaces. Journal of Computational Physics, 118, 269–277.CrossRefGoogle Scholar
  3. Almli, C. R., & Finger, S. (1987). Neural insult and critical period concepts. In M. H. Bornstein (Ed.), Sensitive periods in development: Interdisciplinary perspectives (pp. 123–143). Hillsdale: Lawrence Erlbaum.Google Scholar
  4. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed.). Arlington: American Psychiatric Publishing. text rev.Google Scholar
  5. Birch, H., & Belmont, L. (1964). Auditory–visual integration in normal and retarded readers. American Journal of Orthopsychiatry, 34, 852–861.PubMedGoogle Scholar
  6. Blank, M., & Bridger, W. (1964). Cross-modal transfer in nursery school children. Journal of Comparative Physiology and Psychology, 58, 277–282.CrossRefGoogle Scholar
  7. Bolger, D., Perfetti, C., & Schneider, W. (2005). Cross-cultural effect on the brain revisited: Universal structures plus writing system variation. Human Brain Mapping, 25, 92–104.CrossRefPubMedGoogle Scholar
  8. Bouman, C., & Sauer, K. (1993). A generalized Gaussian image model for edge-preserving MAP estimation. IEEE Transactions on Image Processing, 2, 296–310.CrossRefPubMedGoogle Scholar
  9. Brodmann, K. (1913). Neue Forschungsergebnisse der Grosshirnrindenanatomie mit Besonderer Berücksichtigung Anthropologischer Fragen. Gesellschaft Deutscher Naturforscher und Ärzte, 85, 200–240.Google Scholar
  10. Bush, E. C., & Allman, J. M. (2003). The scaling of white matter to gray matter in cerebellum and neocortex. Brain, Behavior and Evolution, 61, 1–5.CrossRefPubMedGoogle Scholar
  11. Buxhoeveden, D., & Casanova, M. F. (2005). Encephalization, minicolumns, and hominid evolution. In M. F. Casanova (Ed.), Neocortical modularity and the cell minicolumn (pp. 117–136). New York: Nova Biomedical.Google Scholar
  12. Calvin, W. (1996). How brains think. New York: Basic Books.Google Scholar
  13. Casanova, M. F., Araque, J., Giedd, J. N., & Rumsey, J. M. (2004). Reduced brain size and gyrification in the brains of dyslexic patients. Journal of Child Neurology, 19, 275–281.CrossRefPubMedGoogle Scholar
  14. Casanova, M. F., Buxhoeveden, D. P., & Brown, C. (2002a). Clinical and macroscopic correlates of minicolumnar pathology in autism. Journal of Child Neurology, 17, 692–695.CrossRefPubMedGoogle Scholar
  15. Casanova, M. F., Buxhoeveden, D. P., Cohen, M., Switala, A. E., & Roy, E. L. (2002b). Minicolumnar pathology in dyslexia. Annals of Neurology, 52, 108–110.CrossRefPubMedGoogle Scholar
  16. Casanova, M. F., Buxhoeveden, D., & Gomez, J. (2003). Disruption in the inhibitory architecture of the cell minicolumn: Implications for autism. The Neuroscientist, 9, 496–507.CrossRefPubMedGoogle Scholar
  17. Casanova, M. F., Buxhoeveden, D. P., Switala, A. E., & Roy, E. (2002c). Minicolumnar pathology in autism. Neurology, 58, 428–432.PubMedGoogle Scholar
  18. Casanova, M., Christensen, J., Giedd, J., Rumsey, J., Garver, D., & Postel, G. (2005). Magnetic resonance imaging study of brain asymmetries in dyslexic patients. Journal of Child Neurology, 20, 842–847.CrossRefPubMedGoogle Scholar
  19. Casanova, M. F., El-Baz, A., Mott, M., Mannheim, G., Hassan, H., Fahmi, R., et al. (2009). Reduced gyral window and corpus callosum size in autism: Possible macroscopic correlates of a minicolumnopathy. Journal of Autism and Developmental Disorders, 39, 751–764.CrossRefPubMedGoogle Scholar
  20. Casanova, M. F., Farag, A., El-Baz, A., Mott, M., Hassan, H., Fahmi, R., et al. (2007a). Abnormalities of the gyral window in autism: A macroscopic correlate to a putative minicolumnopathy. Journal of Special Education and Rehabilitation, 2006, 85–101.Google Scholar
  21. Casanova, M. F., & Tillquist, C. R. (2008). Encephalization, emergent properties, and psychiatry: A minicolumnar perspective. The Neuroscientist, 14, 101–118.CrossRefPubMedGoogle Scholar
  22. Casanova, M. F., Trippe, J., I. I., & Switala, A. (2007b). A temporal continuity to the vertical organization of the human neocortex. Cerebral Cortex, 17, 130–137.CrossRefPubMedGoogle Scholar
  23. Casanova, M. F., Van Kooten, I. A., Switala, A. E., Van Engeland, H., Heinsen, H., Steinbusch, H. W. M., et al. (2006). Minicolumnar abnormalities in autism. Acta Neuropathologica, 112, 287–303.CrossRefPubMedGoogle Scholar
  24. Childs, J., & Blair, J. (1997). Valproic acid treatment of epilepsy in autistic twins. Journal of Neuroscience Nursing, 29, 244–248.PubMedGoogle Scholar
  25. Devlin, A. M., Cross, J. H., Harkness, W., Chong, W. K., Harding, B., Vargha-Khadem, F., et al. (2003). Clinical outcomes of hemispherectomy for epilepsy in childhood and adolescence. Brain, 126, 556–566.CrossRefPubMedGoogle Scholar
  26. El-Baz, A., Farag, A., Ali, A., Gimel’farb, G., & Casanova, M. (2006). A framework for unsupervised segmentation of multi-modal medical images. In R. Beichel & M. Sonka (Eds.), Computer vision approaches to medical image analysis (pp. 120–131). New York: Springer.CrossRefGoogle Scholar
  27. El-Baz, A., & Gimel’farb, G. (2007). EM based approximation of empirical distributions with linear combinations of discrete Gaussians. ICIP’07 (vol IV) (pp. 373–376). Piscataway: IEEE.Google Scholar
  28. Eliez, S., Rumsey, J., Giedd, J., Schmitt, J., Patwardhan, A., & Reiss, A. (2000). Morphological alteration of temporal lobe gray matter in dyslexia: An MRI study. Journal of Child Psychology and Psychiatry, 41, 637–644.CrossRefPubMedGoogle Scholar
  29. El-Zehiry, N., Casanova, M. F., Hassan, H., & Farag, A. A. (2006). Effect of minicolumnar disturbance on dyslexic brains: An MRI study. Biomedical imaging: From nano to macro (pp. 1336–1339). Piscataway: IEEE.Google Scholar
  30. Frith, U. (2003). Autism: Explaining the enigma. Malden: Blackwell.Google Scholar
  31. Geschwind, N., & Galaburda, A. (1987). Cerebral lateralization: Biological mechanisms, associations, and pathology. Cambridge: MIT Press.Google Scholar
  32. Giedd, J. N., Snell, J. W., Lange, N., Rajapakse, J. C., Casey, B. J., Kozuch, P. L., et al. (1996). Quantitative magnetic resonance imaging of human brain development: Ages 4–18. Cerebral Cortex, 6, 551–560.CrossRefPubMedGoogle Scholar
  33. Gressens, P., & Evrard, P. (1993). The glial fascicle: An ontogenic and phylogenic unit guiding, supplying and distributing mammalian cortical neurons. Brain Research: Developmental Brain Research, 76, 272–277.CrossRefPubMedGoogle Scholar
  34. Gustafsson, L. (1997). Inadequate cortical feature maps: A neural circuit theory of autism. Biological Psychiatry, 42, 1138–1147.CrossRefPubMedGoogle Scholar
  35. Hebb, D. O. (1949). The organization of behavior: A neuropsychological theory. New York: Wiley.Google Scholar
  36. Heiervang, E., Hugdahl, K., Steinmets, H., Smievoll, A. I., Stevenson, J., Lund, A., et al. (2000). Planum temporale, planum parietale and dichotic listening in dyslexia. Neuropsychologia, 38, 1704–1713.CrossRefPubMedGoogle Scholar
  37. Herbert, M. R., Ziegler, D. A., Makris, N., Filipek, P. A., Kemper, T. L., Normandin, J. J., et al. (2004). Localization of white matter volume increase in autism and developmental language disorder. Annals of Neurology, 55, 530–540.CrossRefPubMedGoogle Scholar
  38. Horwitz, B., Rumsey, J. M., & Donohue, B. C. (1998). Functional connectivity of the angular gyrus in normal reading and dyslexia. Proceedings of the National Academy of Sciences of the United States of America, 95, 8939–8944.CrossRefPubMedGoogle Scholar
  39. Hynd, G., Hall, J., Novey, E., Eliopulos, D., Black, K., Gonzalez, J. J., et al. (1995). Dyslexia and corpus callosum morphology. Archives of Neurology, 52, 32–38.PubMedGoogle Scholar
  40. Jackendoff, R. (2002). Foundations of language. Oxford: Oxford University Press.CrossRefGoogle Scholar
  41. Jambaqué, I., Chiron, C., Dumas, C., Mumford, J., & Dulac, O. (2000). Mental and behavioural outcome of infantile epilepsy treated by vigabatrin in tuberous sclerosis patients. Epilepsy Research, 38, 151–160.CrossRefPubMedGoogle Scholar
  42. Jensen, J., & Brieger, D. (2005). Learning disorders. In K. Cheng & K. Myers (Eds.), Child and adolescent psychiatry: The essentials (pp. 281–298). Philadelphia: Lippincott, Williams and Wilkins.Google Scholar
  43. Kass, M., Witkin, A., & Terzopoulos, D. (1988). Snakes: Active contour models. International Journal of Computer Vision, 1, 321–331.CrossRefGoogle Scholar
  44. Klingberg, T., Hedehus, M., Temple, E., Salz, T., Gabrieli, J. D., Moseley, M. E., et al. (2000). Microstructure of temporo-parietal white matter as a basis of reading ability: Evidence from diffusion tensor magnetic resonance imaging. Neuron, 25, 493–500.CrossRefPubMedGoogle Scholar
  45. Lainhart, J., Lazar, M., Bigler, E., & Alexander, A. (2005). The brain during life in autism: Advances in neuroimaging research. In M. F. Casanova (Ed.), Recent developments in autism research (pp. 57–108). New York: Nova Biomedical.Google Scholar
  46. Mariotti, P., Iuvone, L., Torrioli, M. G., & Silveri, M. C. (1998). Linguistic and non-linguistic abilities in a patient with early left hemispherectomy. Neuropsychologia, 36, 1303–1312.CrossRefPubMedGoogle Scholar
  47. Moses, P., Courchesne, E., Stiles, J., Trauner, D., Egaas, B., & Edwards, E. (2000). Regional size reduction in the human corpus callosum following pre- and perinatal brain injury. Cerebral Cortex, 10, 1200–1210.CrossRefPubMedGoogle Scholar
  48. Mountcastle, V. B. (1998). Perpetual neuroscience: The cerebral cortex. Cambridge, MA: Harvard University Press.Google Scholar
  49. Niogi, S. N., & McCandliss, B. D. (2006). Left lateralized white matter microstructure accounts for individual differences in reading ability and disability. Neuropscyhologia, 44, 2178–2188.CrossRefGoogle Scholar
  50. Olson, D. (1977). From utterances to text: The bias of language in speech and writing. Harvard Educational Review, 41, 257–281.Google Scholar
  51. Pantev, C., Engelien, A., Candia, V., & Elbert, T. (2001). Representational cortex in musicians: Plastic alterations in response to musical practice. Annals of the New York Academy of Science, 930, 300–314.CrossRefGoogle Scholar
  52. Pillay, P., & Manger, P. R. (2007). Order-specific quantitative patterns of cortical gyrification. European Journal of Neuroscience, 25, 2705–2712.CrossRefPubMedGoogle Scholar
  53. Pirozzolo, F., & Rayner, K. (1977). Hemispheric specialization in reading and word recognition. Brain and Language, 4, 248–261.CrossRefPubMedGoogle Scholar
  54. Plioplys, A. (1994). Autism: Electroencephalogram abnormalities and clinical improvement with valproic acid. Archives of Pediatric and Adolescent Medicine, 148, 220–222.Google Scholar
  55. Prothero, J. W., & Sundsten, J. W. (1984). Folding of the cerebral cortex in mammals: A scaling model. Brain, Behavior and Evolution, 24, 152–167.CrossRefPubMedGoogle Scholar
  56. Pugh, K. R., Mencl, W. E., Jenner, A. R., Katz, L., Frost, S. J., Lee, J. R., et al. (2000). Functional neuroimaging studies of reading and reading disability (developmental dyslexia). Mental Retardation and Developmental Disabilities Research Reviews, 6, 207–213.CrossRefPubMedGoogle Scholar
  57. Richards, T., Stevenson, J., Crouch, J., Johnson, L. C., Maravilla, K., Stock, P., et al. (2008). Tract-based spatial statistics of diffusion tensor imaging in adults with dyslexia. American Journal of Neuroradiology, 29, 1134–1139.CrossRefPubMedGoogle Scholar
  58. Robichon, F., Bouchard, P., Démonet, J., & Habib, M. (2000). Developmental dyslexia: Re-evaluation of the corpus callosum in male adults. European Neurology, 43, 233–237.CrossRefPubMedGoogle Scholar
  59. Rumsey, J., Donohue, B., Brady, D., Nace, K., Giedd, J., & Andreason, P. (1997a). A magnetic resonance imaging study of planum temporale asymmetry in men with developmental dyslexia. Archives of Neurology, 54, 1481–1489.PubMedGoogle Scholar
  60. Rumsey, J., Nace, K., Donohue, B., Wise, D., Maisog, J., & Andreason, P. (1997b). A positron emission tomographic study of impaired word recognition and phonological processing in dyslexic men. Archives of Neurology, 54, 562–573.PubMedGoogle Scholar
  61. Sandak, R., Frost, S., & Pugh, K. (2004). The neurobiological basis of skilled and impaired reading: Recent findings and new directions. Scientific Studies of Reading, 8, 273–292.CrossRefGoogle Scholar
  62. Shaywitz, S. E., Shaywitz, B. A., Fulbright, R. K., Skudlarski, P., Mencl, W. E., Constable, R. T., et al. (2003). Neural systems for compensation and persistence: Young adult outcome of childhood reading disability. Biological Psychiatry, 54, 25–33.CrossRefPubMedGoogle Scholar
  63. Simos, P. G., Breier, J. I., Fletcher, J. M., Foorman, B. R., Bergman, E., Fishbeck, K., et al. (2000). Brain activation profiles in dyslexic children during non-word reading: A magnetic source imaging study. Neuroscience Letters, 290, 61–65.CrossRefPubMedGoogle Scholar
  64. Sokhadze, E. M., El-Baz, A., Baruth, J., Mathai, G., Sears, L., & Casanova, M. F. (2008). Effects of low frequency repetitive transcranial magnetic stimulation (rTMS) on gamma frequency oscillations and event-related potentials during processing of illusory figures in autism. Journal of Autism and Developmental Disorders, 39(4), 619–634.CrossRefPubMedGoogle Scholar
  65. Steinbrink, C., Vogt, K., Kastrup, A., Muller, H. P., Juengling, F. D., Kassubek, J., et al. (2008). The contribution of white and gray matter differences to developmental dyslexia: Insights from DTI and VBM at 3.0 T. Neuropsychologia, 46, 3170–3178.CrossRefPubMedGoogle Scholar
  66. Tallal, P., Merzenich, M. M., Miller, S., & Jenkins, W. (1998). Language learning impairments: Integrating basic science, technology, and remediation. Experimental Brain Research, 123, 210–219.CrossRefGoogle Scholar
  67. Torgesen, J. (2004). Lessons learned from research on interventions for students who experience difficulty learning to read. In P. McCardle & V. Chabra (Eds.), The voice of evidence in reading research (pp. 355–382). Baltimore: Brookes.Google Scholar
  68. Uvebrant, P., & Bauzienè, R. (1994). Intractable epilepsy in children: The efficacy of lamotrigine treatment, including non-seizure-related benefits. Neuropediatrics, 25, 284–289.CrossRefPubMedGoogle Scholar
  69. Van Essen, D. C. (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature, 385, 313–318.CrossRefPubMedGoogle Scholar
  70. Vargha-Khadem, F., Isaacs, E. B., & Paplelouidi, H. (1991). Development of language in six hemispherectomized patients. Brain, 114, 473–495.CrossRefPubMedGoogle Scholar
  71. Vellutino, F., & Scanlon, D. (1987). Phonological coding, phonological awareness, and reading ability: Evidence from a longitudinal and experimental study. Merril-Palmer Quarterly, 33, 321–363.Google Scholar
  72. Vygotsky, L. (1962). Thought and language. Cambridge, MA: MIT Press.CrossRefGoogle Scholar
  73. Wolf, M. (2007). Proust and the squid: The story and science of the reading brain. New York: Harper Collins.Google Scholar
  74. Wolosin, S., Richardson, M., Hennessey, J., Denckla, M., & Mostofsky, S. (2009). Abnormal cerebral cortex structure in children with ADHD. Human Brain Mapping, 30(1), 175–184.CrossRefPubMedGoogle Scholar
  75. Yeni-Komshian, G. H., Isenberg, D., & Goldberg, H. (1975). Cerebral dominance and reading disability: Left visual field deficit in poor readers. Neuropsychologia, 13, 83–94.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Manuel F. Casanova
    • 1
    • 2
  • Ayman S. El-Baz
    • 3
  • Jay Giedd
    • 4
  • Judith M. Rumsey
    • 5
  • Andrew E. Switala
    • 1
  1. 1.Department of Psychiatry and Behavioral SciencesUniversity of LouisvilleLouisvilleUSA
  2. 2.LouisvilleUSA
  3. 3.Department of Biomedical EngineeringUniversity of LouisvilleLouisvilleUSA
  4. 4.Child Psychiatry BranchNational Institute of Mental HealthBethesdaUSA
  5. 5.Neurodevelopmental Disorders Research BranchNational Institute of Mental HealthBethesdaUSA

Personalised recommendations