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

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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.

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Abbreviations

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

  • 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 

  • Adalsteinsson, D., & Sethian, J. (1995). A fast level set method for propagating interfaces. Journal of Computational Physics, 118, 269–277.

    Article  Google Scholar 

  • 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 

  • American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed.). Arlington: American Psychiatric Publishing. text rev.

    Google Scholar 

  • Birch, H., & Belmont, L. (1964). Auditory–visual integration in normal and retarded readers. American Journal of Orthopsychiatry, 34, 852–861.

    PubMed  Google Scholar 

  • Blank, M., & Bridger, W. (1964). Cross-modal transfer in nursery school children. Journal of Comparative Physiology and Psychology, 58, 277–282.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Bouman, C., & Sauer, K. (1993). A generalized Gaussian image model for edge-preserving MAP estimation. IEEE Transactions on Image Processing, 2, 296–310.

    Article  PubMed  Google Scholar 

  • Brodmann, K. (1913). Neue Forschungsergebnisse der Grosshirnrindenanatomie mit Besonderer Berücksichtigung Anthropologischer Fragen. Gesellschaft Deutscher Naturforscher und Ärzte, 85, 200–240.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Calvin, W. (1996). How brains think. New York: Basic Books.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Casanova, M. F., Buxhoeveden, D. P., Switala, A. E., & Roy, E. (2002c). Minicolumnar pathology in autism. Neurology, 58, 428–432.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Casanova, M. F., & Tillquist, C. R. (2008). Encephalization, emergent properties, and psychiatry: A minicolumnar perspective. The Neuroscientist, 14, 101–118.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Childs, J., & Blair, J. (1997). Valproic acid treatment of epilepsy in autistic twins. Journal of Neuroscience Nursing, 29, 244–248.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Frith, U. (2003). Autism: Explaining the enigma. Malden: Blackwell.

    Google Scholar 

  • Geschwind, N., & Galaburda, A. (1987). Cerebral lateralization: Biological mechanisms, associations, and pathology. Cambridge: MIT Press.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Gustafsson, L. (1997). Inadequate cortical feature maps: A neural circuit theory of autism. Biological Psychiatry, 42, 1138–1147.

    Article  PubMed  Google Scholar 

  • Hebb, D. O. (1949). The organization of behavior: A neuropsychological theory. New York: Wiley.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Jackendoff, R. (2002). Foundations of language. Oxford: Oxford University Press.

    Book  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • Kass, M., Witkin, A., & Terzopoulos, D. (1988). Snakes: Active contour models. International Journal of Computer Vision, 1, 321–331.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Mountcastle, V. B. (1998). Perpetual neuroscience: The cerebral cortex. Cambridge, MA: Harvard University Press.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Olson, D. (1977). From utterances to text: The bias of language in speech and writing. Harvard Educational Review, 41, 257–281.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Pillay, P., & Manger, P. R. (2007). Order-specific quantitative patterns of cortical gyrification. European Journal of Neuroscience, 25, 2705–2712.

    Article  PubMed  Google Scholar 

  • Pirozzolo, F., & Rayner, K. (1977). Hemispheric specialization in reading and word recognition. Brain and Language, 4, 248–261.

    Article  PubMed  Google Scholar 

  • Plioplys, A. (1994). Autism: Electroencephalogram abnormalities and clinical improvement with valproic acid. Archives of Pediatric and Adolescent Medicine, 148, 220–222.

    Google Scholar 

  • Prothero, J. W., & Sundsten, J. W. (1984). Folding of the cerebral cortex in mammals: A scaling model. Brain, Behavior and Evolution, 24, 152–167.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • Uvebrant, P., & Bauzienè, R. (1994). Intractable epilepsy in children: The efficacy of lamotrigine treatment, including non-seizure-related benefits. Neuropediatrics, 25, 284–289.

    Article  PubMed  Google Scholar 

  • Van Essen, D. C. (1997). A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature, 385, 313–318.

    Article  PubMed  Google Scholar 

  • Vargha-Khadem, F., Isaacs, E. B., & Paplelouidi, H. (1991). Development of language in six hemispherectomized patients. Brain, 114, 473–495.

    Article  PubMed  Google Scholar 

  • 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 

  • Vygotsky, L. (1962). Thought and language. Cambridge, MA: MIT Press.

    Book  Google Scholar 

  • Wolf, M. (2007). Proust and the squid: The story and science of the reading brain. New York: Harper Collins.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by grant funding from the National Alliance for Autism Research (NAAR) (MFC), and NIH grant numbers MH62654 and MH69991 (MFC). The series of patients and controls were collected under the guidance and support of Dr. Judith Rapoport, Chief of the Child Psychiatry Branch at the National Institute of Mental Heath.

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Authors and Affiliations

  1. Department of Psychiatry and Behavioral Sciences, University of Louisville, Louisville, KY, USA

    Manuel F. Casanova & Andrew E. Switala

  2. 500 South Preston St, Bldg 55A Rm 217, Louisville, KY, 40292, USA

    Manuel F. Casanova

  3. Department of Biomedical Engineering, University of Louisville, Louisville, KY, USA

    Ayman S. El-Baz

  4. Child Psychiatry Branch, National Institute of Mental Health, Bethesda, MD, USA

    Jay Giedd

  5. Neurodevelopmental Disorders Research Branch, National Institute of Mental Health, Bethesda, MD, USA

    Judith M. Rumsey

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  1. Manuel F. Casanova
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Correspondence to Manuel F. Casanova.

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Casanova, M.F., El-Baz, A.S., Giedd, J. et al. Increased White Matter Gyral Depth in Dyslexia: Implications for Corticocortical Connectivity. J Autism Dev Disord 40, 21–29 (2010). https://doi.org/10.1007/s10803-009-0817-1

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