Temporal-callosal pathway diffusivity predicts phonological skills in children

The development of skilled reading requires efficient communication between distributed brain regions. By using diffusion tensor imaging, we assessed the interhemispheric connections in a group of children with a wide range of reading abilities. We segmented the callosal fibers into regions based on their likely cortical projection zones, and we measured diffusion properties in these segmented regions. Phonological awareness (a key factor in reading acquisition) was positively correlated with diffusivity perpendicular to the main axis of the callosal fibers that connect the temporal lobes. These results could be explained by several physiological properties. For example, good readers may have fewer but larger axons connecting left and right temporal lobes, or their axon membranes in these regions may be more permeable than the membranes of poor readers. These measurements are consistent with previous work suggesting that good readers have reduced interhemispheric connectivity and are better at processing rapidly changing visual and auditory stimuli.

[1]  Steven L. Miller,et al.  Language learning impairments: integrating basic science, technology, and remediation , 1998, Experimental Brain Research.

[2]  Kazimierz Krynicki,et al.  Pressure and temperature dependence of self-diffusion in water , 1978 .

[3]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[4]  W. Rushton A theory of the effects of fibre size in medullated nerve , 1951, The Journal of physiology.

[5]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[6]  N. Geschwind,et al.  Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. , 1985, Archives of neurology.

[7]  M. Eckert Neuroanatomical Markers for Dyslexia: A Review of Dyslexia Structural Imaging Studies , 2004, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[8]  Hao Huang,et al.  DTI tractography based parcellation of white matter: Application to the mid-sagittal morphology of corpus callosum , 2005, NeuroImage.

[9]  P. Basser,et al.  A model for diffusion in white matter in the brain. , 2005, Biophysical journal.

[10]  Luis Concha,et al.  Imaging brain connectivity in children with diverse reading ability , 2005, NeuroImage.

[11]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .

[12]  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.

[13]  B. Wandell,et al.  Children's Reading Performance is Correlated with White Matter Structure Measured by Diffusion Tensor Imaging , 2005, Cortex.

[14]  P. Skudlarski,et al.  Development of left occipitotemporal systems for skilled reading in children after a phonologically- based intervention , 2004, Biological Psychiatry.

[15]  Manjit,et al.  Neurology , 1912, NeuroImage.

[16]  S. F. Witelson Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. , 1989, Brain : a journal of neurology.

[17]  J. Neil,et al.  Evidence that both fast and slow water ADC components arise from intracellular space , 2002, Magnetic resonance in medicine.

[18]  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.

[19]  R. Dougherty,et al.  Cross‐subject comparison of principal diffusion direction maps , 2005, Magnetic resonance in medicine.

[20]  R. N. Davis,et al.  Dyslexia-specific brain activation profile becomes normal following successful remedial training , 2002, Neurology.

[21]  J. Stein,et al.  The magnocellular theory of developmental dyslexia. , 2001, Dyslexia.

[22]  Elise Temple,et al.  Brain mechanisms in normal and dyslexic readers , 2002, Current Opinion in Neurobiology.

[23]  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.

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

[25]  Judith M. Rumsey,et al.  Corpus callosum morphology, as measured with MRI, in dyslexic men , 1996, Biological Psychiatry.

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

[27]  C. Beaulieu,et al.  The basis of anisotropic water diffusion in the nervous system – a technical review , 2002, NMR in biomedicine.

[28]  D. Heeger,et al.  Brain activity in visual cortex predicts individual differences in reading performance. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[29]  F. Robichon,et al.  Abnormal Callosal Morphology in Male Adult Dyslexics: Relationships to Handedness and Phonological Abilities , 1998, Brain and Language.

[30]  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.

[31]  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.

[32]  J. Rumsey,et al.  The biology of developmental dyslexia. , 1992, JAMA.

[33]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

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

[35]  Karl J. Friston,et al.  Generative and recognition models for neuroanatomy , 2004, NeuroImage.

[36]  S. F. Witelson The brain connection: the corpus callosum is larger in left-handers. , 1985, Science.

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

[38]  Albert M. Galaburda,et al.  Neurology of developmental dyslexia , 1992, Current Opinion in Neurobiology.

[39]  Nicolae Duta,et al.  Less developed corpus callosum in dyslexic subjects—a structural MRI study , 2002, Neuropsychologia.

[40]  James C. Gee,et al.  Spatial transformations of diffusion tensor magnetic resonance images , 2001, IEEE Transactions on Medical Imaging.

[41]  J. Rumsey,et al.  Failure to activate the left temporoparietal cortex in dyslexia. An oxygen 15 positron emission tomographic study. , 1992, Archives of neurology.

[42]  Roland Bammer,et al.  Occipital‐Callosal Pathways in Children: Validation and Atlas Development , 2005, Annals of the New York Academy of Sciences.

[43]  N. Geschwind,et al.  Left-handedness: association with immune disease, migraine, and developmental learning disorder. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[44]  G. D. Rosen,et al.  Interhemispheric connections differ between symmetrical and asymmetrical brain regions , 1989, Neuroscience.

[45]  J. Winn,et al.  Brain , 1878, The Lancet.

[46]  Bruce D. McCandliss,et al.  Left lateralized white matter microstructure accounts for individual differences in reading ability and disability , 2006, Neuropsychologia.

[47]  R. Woods,et al.  Abnormal processing of visual motion in dyslexia revealed by functional brain imaging , 1996, Nature.

[48]  M. Livingstone,et al.  Physiological and anatomical evidence for a magnocellular defect in developmental dyslexia. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[49]  P. Basser Inferring microstructural features and the physiological state of tissues from diffusion‐weighted images , 1995, NMR in biomedicine.

[50]  E. Ross,et al.  Topography of the Human Corpus Callosum , 1985, Journal of neuropathology and experimental neurology.

[51]  D. Pandya,et al.  Fiber Pathways of the Brain , 2006 .