Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study

The underlying neurobiology of autism, a severe pervasive developmental disorder, remains unknown. Few neocortical brain MRI abnormalities have been reported. Using rest functional brain imaging, two independent studies have described localized bilateral temporal hypoperfusion in children with primary autism. In order to search for convergent evidence of anatomical abnormalities in autistic children, we performed an anatomical MRI study using optimized whole-brain voxel-based morphometry (VBM). High-resolution 3-D T1-weighted MRI data sets were acquired in 21 children with primary autism (mean age 9.3 +/- 2.2 years) and 12 healthy control children (mean age 10.8 +/- 2.7 years). By comparing autistic children to normal children, we found bilaterally significant decreases of grey matter concentration located in superior temporal sulcus (STS) (P < 0.05 corrected, after small volume correction; SVC). Children with autism were also found to have a decrease of white matter concentration located in the right temporal pole and in cerebellum (P < 0.05, corrected) compared to normal children. These results suggest that autism is associated with bilateral anatomical abnormalities localized in the STS and are remarkably consistent with functional hypoperfusion previously reported in children with autism. The multimodal STS areas are involved in highest level of cortical integration of both sensory and limbic information. Moreover, the STS is now recognized as a key cortical area of the "social brain" and is implicated in social perceptual skills that are characteristically impaired in autism. Therefore, the convergent anatomical and functional temporal abnormalities observed in autism may be important in the understanding of brain behavior relationships in this severe developmental disorder.

[1]  T. Kemper,et al.  Histoanatomic observations of the brain in early infantile autism , 1985, Neurology.

[2]  T. Uema,et al.  Abnormal regional cerebral blood flow in childhood autism. , 2000, Brain : a journal of neurology.

[3]  R. Adolphs Social cognition and the human brain , 1999, Trends in Cognitive Sciences.

[4]  J. Piven,et al.  An MRI study of brain size in autism. , 1995, The American journal of psychiatry.

[5]  S Arndt,et al.  An MRI study of the corpus callosum in autism. , 1997, The American journal of psychiatry.

[6]  E. Bullmore,et al.  Social intelligence in the normal and autistic brain: an fMRI study , 1999, The European journal of neuroscience.

[7]  S Arndt,et al.  Regional brain enlargement in autism: a magnetic resonance imaging study. , 1996, Journal of the American Academy of Child and Adolescent Psychiatry.

[8]  David A. Ziegler,et al.  Dissociations of cerebral cortex, subcortical and cerebral white matter volumes in autistic boys. , 2003, Brain : a journal of neurology.

[9]  P. Gloor The Temporal Lobe and Limbic System , 1997 .

[10]  L. Kanner Autistic disturbances of affective contact. , 1968, Acta paedopsychiatrica.

[11]  D. Treadwell-Deering,et al.  The Biology of Autistic Syndromes , 2002 .

[12]  Paul D Griffiths,et al.  Association of tuberous sclerosis of temporal lobes with autism and atypical autism , 1997, The Lancet.

[13]  N. Minshew,et al.  Corpus callosum size in autism , 2000, Neurology.

[14]  S Arndt,et al.  No Difference in Hippocampus Volume Detected on Magnetic Resonance Imaging in Autistic Individuals , 1998, Journal of autism and developmental disorders.

[15]  D. Josse,et al.  Echelle de développement psychomoteur de la première enfance Brunet-Lézine , 1997 .

[16]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[17]  A. Mayes,et al.  Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism , 2000, Neuroreport.

[18]  S. Kuperman,et al.  Cerebellar structure in autism. , 1987, American journal of diseases of children.

[19]  Arthur W Toga,et al.  Cortical sulcal maps in autism. , 2003, Cerebral cortex.

[20]  G. Rizzolatti,et al.  Neurophysiological mechanisms underlying the understanding and imitation of action , 2001, Nature Reviews Neuroscience.

[21]  D. Pandya,et al.  Efferent cortical connections of multimodal cortex of the superior temporal sulcus in the rhesus monkey , 1992, The Journal of comparative neurology.

[22]  S. Folstein,et al.  Magnetic resonance imaging in autism: measurement of the cerebellum, pons, and fourth ventricle , 1992, Biological Psychiatry.

[23]  Ruth A. Carper,et al.  Unusual brain growth patterns in early life in patients with autistic disorder , 2001, Neurology.

[24]  Andrew E. Switala,et al.  Minicolumnar pathology in autism , 2002, Neurology.

[25]  J. Piven,et al.  An MRI study of the corpus callosum and cerebellum in mentally retarded autistic individuals. , 1999, The Journal of neuropsychiatry and clinical neurosciences.

[26]  N. Minshew,et al.  MRI volumes of amygdala and hippocampus in non–mentally retarded autistic adolescents and adults , 1999, Neurology.

[27]  D. Pandya,et al.  Parietal, temporal, and occipita projections to cortex of the superior temporal sulcus in the rhesus monkey: A retrograde tracer study , 1994, The Journal of comparative neurology.

[28]  J Fermanian,et al.  Validation of the Revised Behavior Summarized Evaluation Scale , 1997, Journal of autism and developmental disorders.

[29]  D. Perrett,et al.  Imitation, mirror neurons and autism , 2001, Neuroscience & Biobehavioral Reviews.

[30]  J. Piven,et al.  Structural and functional magnetic resonance imaging of autism , 2002, International Journal of Developmental Neuroscience.

[31]  I C Gillberg,et al.  Autistic Syndrome with Onset at Age 31 Years: Herpes Encephalitis as a Possible Model for Childhood Autism , 1991, Developmental medicine and child neurology.

[32]  E Courchesne,et al.  Cross‐sectional area of the posterior hippocampus in autistic patients with cerebellar and corpus callosum abnormalitiGs , 1995, Neurology.

[33]  M S Buchsbaum,et al.  Limbic circuitry in patients with autism spectrum disorders studied with positron emission tomography and magnetic resonance imaging. , 2000, The American journal of psychiatry.

[34]  Ruth A. Carper,et al.  Evidence of brain overgrowth in the first year of life in autism. , 2003, JAMA.

[35]  Richard S. J. Frackowiak,et al.  ‘Theory of mind’ in the brain. Evidence from a PET scan study of Asperger syndrome , 1996, Neuroreport.

[36]  E. Courchesne,et al.  Reduced size of corpus callosum in autism. , 1995, Archives of neurology.

[37]  C. Frith,et al.  Autism, Asperger syndrome and brain mechanisms for the attribution of mental states to animated shapes. , 2002, Brain : a journal of neurology.

[38]  J B Poline,et al.  Temporal lobe dysfunction in childhood autism: a PET study. Positron emission tomography. , 2000, The American journal of psychiatry.

[39]  T. Allison,et al.  Social perception from visual cues: role of the STS region , 2000, Trends in Cognitive Sciences.

[40]  J. Decety,et al.  From the perception of action to the understanding of intention , 2001, Nature reviews. Neuroscience.

[41]  U. Frith Mind Blindness and the Brain in Autism , 2001, Neuron.

[42]  A. Couteur,et al.  Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders , 1994, Journal of autism and developmental disorders.

[43]  Karl J. Friston,et al.  The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. , 1999, Neuroreport.

[44]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[45]  E. Courchesne,et al.  Hypoplasia of cerebellar vermal lobules VI and VII in autism. , 1988, The New England journal of medicine.

[46]  J. K. Hietanen,et al.  A comparison of visual responses to object- and ego-motion in the macaque superior temporal polysensory area , 1996, Experimental Brain Research.

[47]  G. Dawson,et al.  Brain structural abnormalities in young children with autism spectrum disorder , 2002, Neurology.

[48]  H. Chugani,et al.  Infantile spasms: III. Prognostic implications of bitemporal hypometabolism on positron emission tomography , 1996, Annals of neurology.