Gray matter alteration in dyslexia: converging evidence from volumetric and voxel-by-voxel MRI analyses

Affecting up to 4-10% of the population, dyslexia is a highly prevalent, childhood onset developmental disorder adversely influencing multiple domains of adaptive functioning throughout the lifespan. The present brain imaging study was conducted in order to investigate the neuroanatomical correlates of developmental dyslexia. The MRI brain scans of 10 males with dyslexia and 14 matched controls were analyzed with (1) a classical volumetric method measuring gray and white matter lobar volumes and (2) a voxel-by-voxel method. The voxel-by-voxel method identifies changes in tissue density and localizes morphologic alterations without limiting the analyses to predefined regions. Subsequent correlations between gray matter density and neuropsychological performance on specific phonological processing tasks (rhyme judgment) were conducted. Volumetric analyses revealed significantly reduced gray matter volumes in both temporal lobes in dyslexic individuals. The voxel-by-voxel analyses further localized changes to the left temporal lobe, revealing reduced gray matter density in the middle and inferior temporal gyri. Conversely, increased gray matter density was found in the precentral gyri bilaterally. As a combined group, the dyslexic and control subjects demonstrated positive correlations between performance on the rhyme judgment tasks and gray matter density in the middle and inferior frontal gyri, and the middle temporal gyri bilaterally. The current study indicates that dyslexia is associated with a structural gray matter deficit involving a complex fronto-temporal network implicated in phonological processing.

[1]  M J Brammer,et al.  A functional study of auditory verbal imagery , 2001, Psychological Medicine.

[2]  W. Kaiser,et al.  fMRI during word processing in dyslexic and normal reading children. , 1999, Neuroreport.

[3]  P. Skudlarski,et al.  Disruption of posterior brain systems for reading in children with developmental dyslexia , 2002, Biological Psychiatry.

[4]  A. Reiss,et al.  Neuroanatomy in Rett syndrome , 1997, Neurology.

[5]  J N Giedd,et al.  A magnetic resonance imaging study of planum temporale asymmetry in men with developmental dyslexia. , 1997, Archives of neurology.

[6]  J. Régis,et al.  Effects of handedness and sex on the morphology of the corpus callosum: A study with brain magnetic resonance imaging , 1991, Brain and Cognition.

[7]  J. Maisog,et al.  A positron emission tomographic study of impaired word recognition and phonological processing in dyslexic men. , 1997, Archives of neurology.

[8]  U. Frith,et al.  Explicit and implicit processing of words and pseudowords by adult developmental dyslexics: A search for Wernicke's Wortschatz? , 1999, Brain : a journal of neurology.

[9]  R. Poldrack,et al.  Microstructure of Temporo-Parietal White Matter as a Basis for Reading Ability Evidence from Diffusion Tensor Magnetic Resonance Imaging , 2000, Neuron.

[10]  M. Habib,et al.  The neurological basis of developmental dyslexia: an overview and working hypothesis. , 2000, Brain : a journal of neurology.

[11]  Torleiv Høien,et al.  MRI evaluation of the size and symmetry of the planum temporale in adolescents with developmental dyslexia , 1990, Brain and Language.

[12]  N C Andreasen,et al.  Automatic atlas-based volume estimation of human brain regions from MR images. , 1996, Journal of computer assisted tomography.

[13]  J G Hennessey,et al.  Reliability and validity of an algorithm for fuzzy tissue segmentation of MRI. , 1998, Journal of computer assisted tomography.

[14]  R. Poldrack,et al.  Disruption of the neural response to rapid acoustic stimuli in dyslexia: evidence from functional MRI. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  N. Geschwind,et al.  Developmental dyslexia: Four consecutive patients with cortical anomalies , 1985, Annals of neurology.

[16]  Allan L. Reiss,et al.  Application of an automated parcellation method to the analysis of pediatric brain volumes , 1997, Psychiatry Research: Neuroimaging.

[17]  V. Menon,et al.  Preliminary evidence of widespread morphological variations of the brain in dyslexia , 2001, Neurology.

[18]  L. M. Hulit,et al.  Response Patterns to Central Auditory Tests and the Clinical Evaluation of Language Fundamentals—Revised: A Pilot Study , 1992, Perceptual and motor skills.

[19]  Victor W. Henderson,et al.  Anatomy of posterior pathways in reading: A reassessment , 1986, Brain and Language.

[20]  M. Annett,et al.  Types of dyslexia and the shift to dextrality. , 1996, Journal of child psychology and psychiatry, and allied disciplines.

[21]  A M Galaburda,et al.  Cytoarchitectonic abnormalities in developmental dyslexia: A case study , 1979, Annals of neurology.

[22]  A. Lundervold,et al.  Planum temporale, planum parietale and dichotic listening in dyslexia , 2000, Neuropsychologia.

[23]  Ranjan Duara,et al.  Temporal lobe surface area measurements on MRI in normal and dyslexic readers , 1993, Neuropsychologia.

[24]  Allan L. Reiss,et al.  Automated Talairach atlas-based parcellation and measurement of cerebral lobes in children , 1999, Psychiatry Research: Neuroimaging.

[25]  Colin M. Brown,et al.  The Neural Circuitry Involved in the Reading of German Words and Pseudowords: A PET Study , 1999, Journal of Cognitive Neuroscience.

[26]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[27]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[28]  D. Schaid,et al.  Incidence of reading disability in a population-based birth cohort, 1976-1982, Rochester, Minn. , 2001, Mayo Clinic proceedings.

[29]  S Eliez,et al.  Morphological alteration of temporal lobe gray matter in dyslexia: an MRI study. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[30]  David P. Corina,et al.  fMRI auditory language differences between dyslexic and able reading children , 2001, Neuroreport.

[31]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[32]  C. Leonard,et al.  Anomalous cerebral structure in dyslexia revealed with magnetic resonance imaging. , 1993, Archives of neurology.

[33]  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 .

[34]  A. Lundervold,et al.  Significant relation between MR measures of planum temporale area and dichotic processing of syllables in dyslexic children , 2003, Neuropsychologia.

[35]  A. Galaburda,et al.  Developmental dyslexia in women: Neuropathological findings in three patients , 1990, Annals of neurology.

[36]  M. Eckert,et al.  Structural imaging in dyslexia: the planum temporale. , 2000, Mental retardation and developmental disabilities research reviews.

[37]  A. Liberman,et al.  Functional disruption in the organization of the brain for reading in dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.