Cortex
Volume 46, Issue 6 , Pages 739-749 , June 2010

White matter microstructural differences linked to left perisylvian language network in children with dyslexia

  • Sheryl L. Rimrodt

      Affiliations

    • Kennedy Krieger Institute, Baltimore, MD, USA
    • Department of Pediatrics, Johns Hopkins School of Medicine, Baltimore, MD, USA
  • ,
  • Daniel J. Peterson

      Affiliations

    • Kennedy Krieger Institute, Baltimore, MD, USA
  • ,
  • Martha B. Denckla

      Affiliations

    • Kennedy Krieger Institute, Baltimore, MD, USA
    • Department of Pediatrics, Johns Hopkins School of Medicine, Baltimore, MD, USA
    • Department of Neurology, Johns Hopkins School of Medicine, Baltimore, MD, USA
  • ,
  • Walter E. Kaufmann

      Affiliations

    • Kennedy Krieger Institute, Baltimore, MD, USA
    • Department of Pediatrics, Johns Hopkins School of Medicine, Baltimore, MD, USA
    • Department of Neurology, Johns Hopkins School of Medicine, Baltimore, MD, USA
    • Department of Radiology, Johns Hopkins School of Medicine, Baltimore, MD, USA
  • ,
  • Laurie E. Cutting

      Affiliations

    • Kennedy Krieger Institute, Baltimore, MD, USA
    • Department of Neurology, Johns Hopkins School of Medicine, Baltimore, MD, USA
    • Department of Education, Johns Hopkins School of Medicine, Baltimore, MD, USA
    • Corresponding Author InformationCorresponding author. Kennedy Krieger Institute, Department of Developmental Cognitive Neurology, 707N Broadway, Suite 232, Baltimore, MD 21205, USA.

Received 16 October 2008 ,Revised 5 June 2009 ,Accepted 16 July 2009.

References 

  1. Beaulieu C, Plewes C, Paulson LA, Roy D, Snook L, Concha L, et al. Imaging brain connectivity in children with diverse reading ability. NeuroImage. 2005;25:1266–1271
  2. Brown WE, Eliez S, Menon Rumsey M, White CD, Reiss AL. Preliminary evidence of widespread morphological variations of the brain in dyslexia. Neurology. 2001;56:781–783
  3. Carter JC, Lanham DC, Cutting LE, Clements-Stephens AM, Chen X, Hadzipasic M, et al. A dual DTI approach to analyzing white matter in children with dyslexia. Psychiatry Research. Apr 5, 2009;
  4. Catani M, Jones DK, ffytche DH. Perisylvian language networks of the human brain. Annals of Neurology. 2005;57:8–16
  5. Catani M, Mesulam M. The arcuate fasciculus and the disconnection theme in language and aphasia: History and current state. Cortex. 2008;44:953–961
  6. Chang LC, Jones DK, Pierpaoli C. RESTORE: Robust estimation of tensors by outlier rejection. Magnetic Resonance in Medicine. 2005;53:1088–1095
  7. Cook PA, Bai Y, Nedjati-Gilani S, Seunarine KK, Hall MG, Parker GJ, et al. Camino: Open-Source Diffusion-MRI Reconstruction and Processing. 14th Scientific Meeting of the International Society for Magnetic Resonance in Medicine. Seattle, WA, USA, 2006: 2759.
  8. Deutsch GK, Dougherty RF, Bammer R, Siok WT, Gabrieli JD, Wandell BA. Children's reading performance is correlated with white matter structure measured by diffusion tensor imaging. Cortex. 2005;41:354–363
  9. Dougherty RF, Ben-Shachar M, Deutsch GK, Hernandez A, Fox GR, Wandell BA. Temporal-callosal pathway diffusivity predicts phonological skills in children. Proceedings of the National Academy of Sciences, United States of America. 2007;104:8556–8561
  10. Eden GF, Jones KM, Cappell K, Gareau L, Wood FB, Zeffiro TA, et al. Neural changes following remediation in adult developmental dyslexia. Neuron. 2004;44:411–422
  11. Epelbaum S, Pinel P, Gaillard R, Delmaire C, Perrin M, Dupont S, et al. Pure alexia as a disconnection syndrome: New diffusion imaging evidence for an old concept. Cortex, 44: 962–974, 2008.
  12. Fiez JA, Petersen SE. Neuroimaging studies of word reading. Proceedings of the National Academy of Science. 1998;95:914–921
  13. Flitney D, Webster M, Patenaude B, Seidman L, Goldstein J, Tordesillas Gutiérrez D, et al. Anatomical brain atlases and their application in the FSL View visualisation tool. Thirteenth Annual Meeting of the Organization for Human Brain Mapping. Chicago, IL, USA, 2007.
  14. Galaburda AM, Kemper TL. Cytoarchitectonic abnormalities in developmental dyslexia: A case study. Annals of Neurology. 1979;6:94–100
  15. Galaburda AM, Sherman GF, Rosen GD, Aboitiz F, Geschwind N. Developmental dyslexia: Four consecutive patients with cortical anomalies. Annals of Neurology. 1985;18:222–233
  16. Galaburda AM, Corsiglia J, Rosen GD, Sherman GF. Planum temporale asymmetry: Reappraisal since Geschwind and Levitsky. Neuropsychologia. 1987;25:853–868
  17. Gold BT, Powell DK, Xuan L, Jiang Y, Hardy PA. Speed of lexical decision correlates with diffusion anisotropy in left parietal and frontal white matter: Evidence from diffusion tensor imaging. Neuropsychologia. 2007;45:2439–2446
  18. Hua K, Zhang J, Wakana S, Jiang H, Li X, Reich DS, et al. Tract probability maps in stereotaxic spaces: Analyses of white matter anatomy and tract-specific quantification. NeuroImage. 2008;39:336–347
  19. Humphreys P, Kaufmann WE, Galaburda AM. Developmental dyslexia in women neuropathological findings in three patients. Annals of Neurology. 1990;28:727–738
  20. Jenkinson M, Smith S. A global optimisation method for robust affine registration of brain images. Medical Image Analysis. 2001;5:143–156
  21. Kaufmann WE, Galaburda AM. Cerebrocortical microdysgenesis in neurologically normal subjects: A histopathologic study. Neurology. 1989;39:238–244
  22. Klingberg T, Hedehus M, Temple E, Salz T, Gabrieli JD, Moseley ME, et al. Microstructure of temporo-parietal white matter as a basis for reading ability: Evidence from diffusion tensor magnetic resonance imaging. Neuron. 2000;25:493–500
  23. Lancaster JL, Woldorff MG, Parsons LM, Liotti M, Freitas CS, Rainey L, et al. Automated Talairach Atlas labels for functional brain mapping. Human Brain Mapping. 2000;10:120–131
  24. Landman BA, Farrell JA, Mori S, van Zijl PC, and Prince JL. On the Coregistration of Diffusion Weighted Images. International Society for Magnetic Resonance in Medicine Meeting. Seattle, Washington, USA, 2006.
  25. Landman B, Bazin PL, and Prince JL. Diffusion Tensor Estimation by Maximizing Rician Likelihood. Eleventh Institute of Electrical and Electronics Engineers Computer Society International Conference, Computer Vision Workshop on Mathematical Methods in Biomedical Image Analysis. Rio de Janerio, Brazil, 2007a.
  26. Landman BA, Farrell JA, Jones CK, Smith SA, Prince JL, Mori S. Effects of diffusion weighting schemes on the reproducibility of DTI-derived fractional anisotropy, mean diffusivity, and principal eigenvector measurements at 1.5T. NeuroImage. 2007;36:1123–1138
  27. Landman BA, Farrell JA, Patel N, Mori S, and Prince, JL. DTI Fiber Tracking: The Importance of Adjusting DTI Gradient Tables for Motion Correction. CATNAP – A Tool to Simplify and Accelerate DTI Analysis. Organization for Human Brain Mapping Meeting. Chicago, Illinois, USA, 2007c.
  28. Lin CP, Tseng WY, Cheng HC, Chen JH. Validation of diffusion tensor magnetic resonance axonal fiber imaging with registered manganese-enhanced optic tracts. NeuroImage. 2001;14:1035–1047
  29. Melhem ER, Mori S, Mukundan G, Kraut MA, Pomper MG, van Zijl PC. Diffusion tensor MR imaging of the brain and white matter tractography. Amercian Journal of Roentgenology. 2002;178:3–16
  30. Molko N, Cohen L, Mangin JF, Chochon F, Lehericy S, Le Bihan D, et al. Visualizing the neural bases of a disconnection syndrome with diffusion tensor imaging. Journal of Cognitive Neuroscience. 2002;14:629–636
  31. Mori S, Kaufmann WE, Pearlson GD, Crain BJ, Stieltjes B, Solaiyappan M, et al. In vivo visualization of human neural pathways by magnetic resonance imaging. Annals of Neurology. 2000;47:412–414
  32. Nagy Z, Westerberg H, Klingberg T. Maturation of white matter is associated with the development of cognitive functions during childhood. Journal of Cognitive Neuroscience. 2004;16:1227–1233
  33. Nichols TE, Holmes AP. Nonparametric permutation tests for functional neuroimaging: A primer with examples. Human Brain Mapping. 2002;15:1–25
  34. Niogi SN, McCandliss BD. Left lateralized white matter microstructure accounts for individual differences in reading ability and disability. Neuropsychologia. 2006;44:2178–2188
  35. Parker GJM, Haroon HA, Wheeler-Kingshott CAM. A framework for a streamline-based probabilistic index of connectivity (PICo) using a structural interpretation of MRI diffusion measurements. Journal of Magnetic Resonance Imaging. 2003;18:242–254
  36. Paulesu E, Demonet JF, Fazio F, McCrory E, Chanoine V, Brunswick N, et al. Dyslexia: Cultural diversity and biological unity. Science. 2001;291:2165–2167
  37. Price C, Moore C, Frackowiak RSJ. The effect of varying stimulus rate and duration on brain activity during reading. NeuroImage. 1996;3:40–52
  38. Pugh KR, Shaywitz BA, Shaywitz SE, Constable TR, Skudlarski P, Fulbright RK, et al. Cerebral organization of component processes in reading. Brain. 1996;119:1221–1238
  39. Pugh KR, Mencl WE, Jenner AR, Katz L, Frost SJ, Lee JR, et al. Functional neuroimaging studies of reading and reading disability (developmental dyslexia). Mental Retardation and Developmental Disabilities Research Review. 2000;6:207–213
  40. Pugh KR, Mencl WE, Jenner AR, Katz L, Frost SJ, Lee JR, et al. Neurobiological studies of reading and reading disability. Journal of Communication Disorders. 2001;34:479–492
  41. Qiu D, Tan LH, Zhou K, Khong PL. Diffusion tensor imaging of normal white matter maturation from late childhood to young adulthood: Voxel-wise evaluation of mean diffusivity, fractional anisotropy, radial and axial diffusivities, and correlation with reading development. NeuroImage. 2008;41:223–232
  42. Reich W, Welner Z, Herjanic B. Diagnostic Interview for Children-IV (DICA-IV). Toronto, Ontario, Canada: Multi-Health Systems Incorporated; 1997;
  43. Richards T, Stevenson J, Crouch J, Johnson LC, Maravilla K, Stock P, et al. Tract-based spatial statistics of diffusion tensor imaging in adults with dyslexia. American Journal of Neuroradiology. 2008;29:1134–1139
  44. Rumsey JM, Nace K, Donohue B, Wise D, Maisog JM, Andreason P. A positron emission tomographic study of impaired word recognition and phonological processing in dyslexic men. Archives of Neurology. 1997;54:562–573
  45. Schwartzman A, Dougherty RF, Taylor JE. Cross-subject comparison of principal diffusion direction maps. Magnetic Resonance in Medicine. 2005;53:1423–1431
  46. Shaywitz BA, Shaywitz SE, Blachman BA, Pugh KR, Fulbright RK, Skudlarski P, et al. Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention. Biological Psychiatry. 2004;55:926–933
  47. Shaywitz BA, Shaywitz SE, Pugh KR, Mencl WE, Fulbright RK, Skudlarski P, et al. Disruption of posterior brain systems for reading in children with developmental dyslexia. Biological Psychiatry. 2002;52:101–110
  48. Shaywitz SE. Dyslexia. New England Journal of Medicine. 1998;338:307–312
  49. Simos PG, Breier JI, Fletcher JM, Bergman E, Papanicolaou AC. Cerebral mechanisms involved in word reading in dyslexic children: A magnetic source imaging approach. Cerebral Cortex. 2000;10:809–816
  50. Simos PG, Breier JI, Fletcher JM, Foorman BR, Bergman E, Fishbeck K, et al. Brain activation profiles in dyslexic children during non-word reading: A magnetic source imaging study. Neuroscience Letters. 2000;290:61–65
  51. Simos PG, Fletcher JM, Denton C, Sarkari S, Billingsley-Marshall R, Papanicolaou AC. Magnetic source imaging studies of dyslexia interventions. Developmental Neuropsychology. 2006;30:591–611
  52. Steinbrink C, Vogt K, Kastrup A, Muller HP, Juengling FD, Kassubek J, et al. The contribution of white and gray matter differences to developmental dyslexia: Insights from DTI and VBM at 3T. Neuropsychologia. 2008;
  53. Stieltjes B, Kaufmann WE, van Zijl PCM, Fredericksen K, Pearlson GD, Mori S. Diffusion tensor imaging and axonal tracking in the human brainstem. NeuroImage. 2001;14:723–735
  54. Torgesen JK, Wagner RK, Rashotte C. Test of Word Reading Efficiency (TOWRE). Austin, Texas, USA: Pro-Ed Incorporated; 1999;
  55. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage. 2002;15:273–289
  56. Wakana S, Caprihan A, Panzenboeck MM, Fallon JH, Perry M, Gollub RL, et al. Reproducibility of quantitative tractography methods applied to cerebral white matter. NeuroImage. 2007;36:630–644
  57. Wakana S, Jiang H, Nagae-Poetscher LM, van Zijl PC, Mori S. Fiber tract-based atlas of human white matter anatomy. Radiology. 2004;230:77–87
  58. Wechsler D. Wechsler Individual Achievement Tests. (WIAT-II) 2nd ed.. San Antonio, Texas, USA: The Psyhcological Corporation; 2001;
  59. Wechsler D. Wechsler Intelligence Scale for Children – Fourth Edition. San Antonio, TX: The Psychological Corporation; 2003;
  60. Woodcock RW, McGrew KS, Mather N. Woodcock-Johnson III – Tests of Achievement (WJ-III). Itasca, Illinois, USA: Riverside Publishing; 2001;

PII: S0010-9452(09)00222-6

doi: 10.1016/j.cortex.2009.07.008

Cortex
Volume 46, Issue 6 , Pages 739-749 , June 2010