Increased left hemisphere impairment in high-functioning autism: A tract based spatial statistics study

There is evidence emerging from Diffusion Tensor Imaging (DTI) research that autism spectrum disorders (ASD) are associated with greater impairment in the left hemisphere. Although this has been quantified with volumetric region of interest analyses, it has yet to be tested with white matter integrity analysis. In the present study, tract based spatial statistics was used to contrast white matter integrity of 12 participants with high-functioning autism or Aspergers syndrome (HFA/AS) with 12 typically developing individuals. Fractional Anisotropy (FA) was examined, in addition to axial, radial and mean diffusivity (AD, RD and MD). In the left hemisphere, participants with HFA/AS demonstrated significantly reduced FA in predominantly thalamic and fronto-parietal pathways and increased RD. Symmetry analyses confirmed that in the HFA/AS group, WM disturbance was significantly greater in the left compared to right hemisphere. These findings contribute to a growing body of literature suggestive of reduced FA in ASD, and provide preliminary evidence for RD impairments in the left hemisphere.

[1]  Andrew L. Alexander,et al.  Diffusion tensor imaging of the corpus callosum in Autism , 2007, NeuroImage.

[2]  M. Behen,et al.  Alterations in frontal lobe tracts and corpus callosum in young children with autism spectrum disorder. , 2010, Cerebral cortex.

[3]  J. Mazziotta,et al.  Lateralization of the Human Mirror Neuron System , 2006, The Journal of Neuroscience.

[4]  Moo K. Chung,et al.  Diffusion tensor imaging of white matter in the superior temporal gyrus and temporal stem in autism , 2007, Neuroscience Letters.

[5]  J Townsend,et al.  The brain in infantile autism , 1994, Neurology.

[6]  Do P. M. Tromp,et al.  Diffusion Tensor Imaging in Autism Spectrum Disorder: A Review , 2012, Autism research : official journal of the International Society for Autism Research.

[7]  Talma Hendler,et al.  Abnormal white matter integrity in young children with autism , 2011, Human brain mapping.

[8]  Vicente L. Malave,et al.  Autism as a neural systems disorder: A theory of frontal-posterior underconnectivity , 2012, Neuroscience & Biobehavioral Reviews.

[9]  David A. Ziegler,et al.  Localization of white matter volume increase in autism and developmental language disorder , 2004, Annals of neurology.

[10]  R. E. Schmidt,et al.  Toward accurate diagnosis of white matter pathology using diffusion tensor imaging , 2007, Magnetic resonance in medicine.

[11]  Janet B W Williams,et al.  Diagnostic and Statistical Manual of Mental Disorders , 2013 .

[12]  Stephen M. Smith,et al.  Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference , 2009, NeuroImage.

[13]  Jessica R. Jones,et al.  Changes in prevalence of parent-reported autism spectrum disorder in school-aged U.S. children: 2007 to 2011-2012. , 2013, National health statistics reports.

[14]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[15]  Byron Bernal,et al.  The connectivity of the superior longitudinal fasciculus: a tractography DTI study. , 2010, Magnetic resonance imaging.

[16]  Ross T. Whitaker,et al.  Microstructural connectivity of the arcuate fasciculus in adolescents with high-functioning autism , 2010, NeuroImage.

[17]  T. Kemper,et al.  Neuropathology of infantile autism. , 1998, Journal of neuropathology and experimental neurology.

[18]  Y. Assaf,et al.  Diffusion Tensor Imaging (DTI)-based White Matter Mapping in Brain Research: A Review , 2007, Journal of Molecular Neuroscience.

[19]  A. Reiss,et al.  Diffusion tensor imaging reveals white matter abnormalities in Attention-Deficit/Hyperactivity Disorder , 2012, Psychiatry Research: Neuroimaging.

[20]  J. Ponsford,et al.  White Matter Integrity Following Traumatic Brain Injury: The Association with Severity of Injury and Cognitive Functioning , 2013, Brain Topography.

[21]  L. Lotspeich,et al.  Similar white matter aberrations in children with autism and their unaffected siblings: a diffusion tensor imaging study using tract-based spatial statistics. , 2010, Archives of general psychiatry.

[22]  Dc Washington.  Diagnostic and Statistical Manual of Mental Disorders, 4th Ed. , 1994 .

[23]  M. Reite,et al.  Smaller left hemisphere planum temporale in adults with autistic disorder , 2002, Neuroscience Letters.

[24]  Ralph-Axel Müller,et al.  Underconnected, but how? A survey of functional connectivity MRI studies in autism spectrum disorders. , 2011, Cerebral cortex.

[25]  Ralph-Axel Müller,et al.  Microstructural abnormalities of short-distance white matter tracts in autism spectrum disorder , 2011, Neuropsychologia.

[26]  Katharine N. Thakkar,et al.  Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD) , 2008, Brain : a journal of neurology.

[27]  Robert T. Schultz,et al.  Involvement of the anterior thalamic radiation in boys with high functioning autism spectrum disorders: A Diffusion Tensor Imaging study , 2011, Brain Research.

[28]  Derek K. Jones,et al.  Symmetries in human brain language pathways correlate with verbal recall , 2007, Proceedings of the National Academy of Sciences.

[29]  J K Smith,et al.  Temporal and Spatial Development of Axonal Maturation and Myelination of White Matter in the Developing Brain , 2008, American Journal of Neuroradiology.

[30]  Derek K. Jones,et al.  The effect of filter size on VBM analyses of DT-MRI data , 2005, NeuroImage.

[31]  W. Tseng,et al.  The loss of asymmetry and reduced interhemispheric connectivity in adolescents with autism: A study using diffusion spectrum imaging tractography , 2011, Psychiatry Research: Neuroimaging.

[32]  Jean Decety,et al.  Atypical development of white matter microstructure in adolescents with autism spectrum disorders , 2010, NeuroImage.

[33]  H. Yamasue,et al.  Comparison of white matter integrity between autism spectrum disorder subjects and typically developing individuals: a meta-analysis of diffusion tensor imaging tractography studies , 2013, Molecular Autism.

[34]  D. Amaral,et al.  Neuroanatomy of autism , 2008, Trends in Neurosciences.

[35]  P. Poulet,et al.  Brain dysmyelination and recovery assessment by noninvasive in vivo diffusion tensor magnetic resonance imaging , 2006, Journal of neuroscience research.

[36]  D. Shukla,et al.  White matter compromise of callosal and subcortical fiber tracts in children with autism spectrum disorder: a diffusion tensor imaging study. , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[37]  Nagesh Adluru,et al.  Atypical diffusion tensor hemispheric asymmetry in autism , 2010, Autism research : official journal of the International Society for Autism Research.

[38]  Daniel B Hier,et al.  Autism and unfavorable left-right asymmetries of the brain , 1979, Journal of autism and developmental disorders.

[39]  L. Soorya,et al.  Impaired Structural Connectivity of Socio-Emotional Circuits in Autism Spectrum Disorders: A Diffusion Tensor Imaging Study , 2011, PloS one.

[40]  Xenophon Papademetris,et al.  Diffusion Tensor Imaging in Autism Spectrum Disorders: Preliminary Evidence of Abnormal Neural Connectivity , 2011, The Australian and New Zealand journal of psychiatry.

[41]  Diane C. Chugani,et al.  Diffusion Tensor Imaging of Frontal Lobe in Autism Spectrum Disorder , 2008, Cerebral cortex.

[42]  D. Skuse,et al.  White matter microstructure correlates with autism trait severity in a combined clinical–control sample of high-functioning adults , 2013, NeuroImage: Clinical.

[43]  Lucia Billeci,et al.  White matter connectivity in children with autism spectrum disorders: a tract-based spatial statistics study , 2012, BMC Neurology.

[44]  R. Floris,et al.  White matter reduced streamline coherence in young men with autism and mental retardation , 2009, European journal of neurology.

[45]  K. Belov,et al.  Allorecognition in the Tasmanian Devil (Sarcophilus harrisii), an Endangered Marsupial Species with Limited Genetic Diversity , 2011, PloS one.

[46]  T. Roberts,et al.  Elevated Mean Diffusivity in the Left Hemisphere Superior Longitudinal Fasciculus in Autism Spectrum Disorders Increases with More Profound Language Impairment , 2012, American Journal of Neuroradiology.

[47]  D. Pandya,et al.  Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. , 2005, Cerebral cortex.

[48]  Jun Yoshino,et al.  Demyelination increases radial diffusivity in corpus callosum of mouse brain , 2005, NeuroImage.

[49]  Daniel Rueckert,et al.  Tract-based spatial statistics: Voxelwise analysis of multi-subject diffusion data , 2006, NeuroImage.

[50]  Eric Courchesne,et al.  A failure of left temporal cortex to specialize for language is an early emerging and fundamental property of autism. , 2012, Brain : a journal of neurology.

[51]  Aad van der Lugt,et al.  Fiber density asymmetry of the arcuate fasciculus in relation to functional hemispheric language lateralization in both right- and left-handed healthy subjects: A combined fMRI and DTI study , 2007, NeuroImage.

[52]  Mitchel S. Berger,et al.  Analysis of the subcomponents and cortical terminations of the perisylvian superior longitudinal fasciculus: a fiber dissection and DTI tractography study , 2012, Brain Structure and Function.