Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity.

The brain activation of a group of high-functioning autistic participants was measured using functional MRI during sentence comprehension and the results compared with those of a Verbal IQ-matched control group. The groups differed in the distribution of activation in two of the key language areas. The autism group produced reliably more activation than the control group in Wernicke's (left laterosuperior temporal) area and reliably less activation than the control group in Broca's (left inferior frontal gyrus) area. Furthermore, the functional connectivity, i.e. the degree of synchronization or correlation of the time series of the activation, between the various participating cortical areas was consistently lower for the autistic than the control participants. These findings suggest that the neural basis of disordered language in autism entails a lower degree of information integration and synchronization across the large-scale cortical network for language processing. The article presents a theoretical account of the findings, related to neurobiological foundations of underconnectivity in autism.

[1]  August B. Hollingshead,et al.  Two Factor Index of Social Position , 1957 .

[2]  A. Luria Higher Cortical Functions in Man , 1980, Springer US.

[3]  S. Baron-Cohen,et al.  Does the autistic child have a “theory of mind” ? , 1985, Cognition.

[4]  B Horwitz,et al.  The cerebral metabolic landscape in autism. Intercorrelations of regional glucose utilization. , 1988, Archives of neurology.

[5]  U. Frrrh Autism: explaining the enigma , 1989 .

[6]  M. Posner,et al.  Positron Emission Tomographic Studies of the Processing of Singe Words , 1989, Journal of Cognitive Neuroscience.

[7]  M M Mesulam,et al.  Large‐scale neurocognitive networks and distributed processing for attention, language, and memory , 1990, Annals of neurology.

[8]  S. Petersen,et al.  Activation of extrastriate and frontal cortical areas by visual words and word-like stimuli. , 1990, Science.

[9]  Karl J. Friston,et al.  The cortical localization of the lexicons. Positron emission tomography evidence. , 1992, Brain : a journal of neurology.

[10]  A. Galaburda,et al.  Human Cerebral Cortex: Localization, Parcellation, and Morphometry with Magnetic Resonance Imaging , 1992, Journal of Cognitive Neuroscience.

[11]  N. Minshew,et al.  Age differences in academic achievement in high-functioning autistic individuals. , 1994, Journal of clinical and experimental neuropsychology.

[12]  Karl J. Friston Functional and effective connectivity in neuroimaging: A synthesis , 1994 .

[13]  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.

[14]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[15]  Y. Samson,et al.  Delayed maturation of the frontal cortex in childhood autism. , 1995, The American journal of psychiatry.

[16]  N. Makris,et al.  MRI-Based Topographic Parcellation of Human Neocortex: An Anatomically Specified Method with Estimate of Reliability , 1996, Journal of Cognitive Neuroscience.

[17]  M. Just,et al.  Brain Activation Modulated by Sentence Comprehension , 1996, Science.

[18]  N. Minshew,et al.  Neuropsychologic functioning in autism: Profile of a complex information processing disorder , 1997, Journal of the International Neuropsychological Society.

[19]  J. Fiez Phonology, Semantics, and the Role of the Left Inferior Prefrontal Cortex , 2022 .

[20]  David Caplan,et al.  Effects of Syntactic Structure and Propositional Number on Patterns of Regional Cerebral Blood Flow , 1998, Journal of Cognitive Neuroscience.

[21]  B. Horwitz,et al.  Functional connectivity of the angular gyrus in normal reading and dyslexia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[22]  S. Petersen,et al.  Neuroimaging studies of word reading. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  J. Desmond,et al.  The role of left prefrontal cortex in language and memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  R. Müller,et al.  Language organization in patients with early and lateleft-hemisphere lesion: a pet study , 1999, Neuropsychologia.

[25]  G. Waters,et al.  PET Studies of Syntactic Processing with Auditory Sentence Presentation , 1999, NeuroImage.

[26]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

[27]  D. Shankweiler,et al.  An Event-related Neuroimaging Study Distinguishing Form and Content in Sentence Processing , 2000, Journal of Cognitive Neuroscience.

[28]  B. Leventhal,et al.  The Autism Diagnostic Observation Schedule—Generic: A Standard Measure of Social and Communication Deficits Associated with the Spectrum of Autism , 2000, Journal of autism and developmental disorders.

[29]  J. Barth,et al.  The Halstead-Reitan Neuropsychological Test Battery. , 2000 .

[30]  A. Friederici,et al.  Auditory Language Comprehension: An Event-Related fMRI Study on the Processing of Syntactic and Lexical Information , 2000, Brain and Language.

[31]  F. Volkmar,et al.  Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. , 2000, Archives of general psychiatry.

[32]  M. Just,et al.  Interdependence of Nonoverlapping Cortical Systems in Dual Cognitive Tasks , 2001, NeuroImage.

[33]  M. Just,et al.  The neural bases of sentence comprehension: a fMRI examination of syntactic and lexical processing. , 2001, Cerebral cortex.

[34]  Erica B. Michael,et al.  fMRI investigation of sentence comprehension by eye and by ear: Modality fingerprints on cognitive processes , 2001, Human brain mapping.

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

[36]  David A. Ziegler,et al.  Abnormal asymmetry in language association cortex in autism , 2002, Annals 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]  F. Rösler,et al.  Brain Activation Modulated by the Comprehension of Normal and Pseudo-word Sentences of Different Processing Demands: A Functional Magnetic Resonance Imaging Study , 2002, NeuroImage.

[39]  N. Minshew,et al.  Effects of age on brain volume and head circumference in autism , 2002, Neurology.

[40]  Karl J. Friston,et al.  Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations , 2002, Biological Psychiatry.

[41]  S. Bookheimer Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. , 2002, Annual review of neuroscience.

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

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

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

[45]  T. Horbach,et al.  No Influence of Surgical Stress on Postoperative Leptin Gene Expression in Different Adipose Tissues and Soluble Leptin Receptor Plasma Levels , 2003, Hormone Research in Paediatrics.

[46]  Sharlene D. Newman,et al.  Imagery in sentence comprehension: an fMRI study , 2004, NeuroImage.