Neural correlates of pragmatic language comprehension in autism spectrum disorders.

Difficulties with pragmatic aspects of communication are universal across individuals with autism spectrum disorders (ASDs). Here we focused on an aspect of pragmatic language comprehension that is relevant to social interaction in daily life: the integration of speaker characteristics inferred from the voice with the content of a message. Using functional magnetic resonance imaging (fMRI), we examined the neural correlates of the integration of voice-based inferences about the speaker's age, gender or social background, and sentence content in adults with ASD and matched control participants. Relative to the control group, the ASD group showed increased activation in right inferior frontal gyrus (RIFG; Brodmann area 47) for speaker-incongruent sentences compared to speaker-congruent sentences. Given that both groups performed behaviourally at a similar level on a debriefing interview outside the scanner, the increased activation in RIFG for the ASD group was interpreted as being compensatory in nature. It presumably reflects spill-over processing from the language dominant left hemisphere due to higher task demands faced by the participants with ASD when integrating speaker characteristics and the content of a spoken sentence. Furthermore, only the control group showed decreased activation for speaker-incongruent relative to speaker-congruent sentences in right ventral medial prefrontal cortex (vMPFC; Brodmann area 10), including right anterior cingulate cortex (ACC; Brodmann area 24/32). Since vMPFC is involved in self-referential processing related to judgments and inferences about self and others, the absence of such a modulation in vMPFC activation in the ASD group possibly points to atypical default self-referential mental activity in ASD. Our results show that in ASD compensatory mechanisms are necessary in implicit, low-level inferential processes in spoken language understanding. This indicates that pragmatic language problems in ASD are not restricted to high-level inferential processes, but encompass the most basic aspects of pragmatic language processing.

[1]  C. Zuker,et al.  Independent Anchoring and Assembly Mechanisms of INAD Signaling Complexes in Drosophila Photoreceptors , 2001, The Journal of Neuroscience.

[2]  Peter Hagoort,et al.  When Elephants Fly: Differential Sensitivity of Right and Left Inferior Frontal Gyri to Discourse and World Knowledge , 2009, Journal of Cognitive Neuroscience.

[3]  U. Frith,et al.  Can autistic children predict behavior by social stereotypes? , 2007, Current Biology.

[4]  P. Hagoort,et al.  Integration of Word Meaning and World Knowledge in Language Comprehension , 2004, Science.

[5]  W. Kintsch,et al.  Strategies of discourse comprehension , 1983 .

[6]  K. Amunts,et al.  Brodmann's Areas 17 and 18 Brought into Stereotaxic Space—Where and How Variable? , 2000, NeuroImage.

[7]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[8]  M. Corbetta,et al.  Top-down modulation of early sensory cortex , 1996, NeuroImage.

[9]  Jordan Grafman,et al.  A thoroughly modern gage , 1999 .

[10]  U. Frith,et al.  An islet of social ability in Asperger Syndrome: Judging social attributes from faces , 2006, Brain and Cognition.

[11]  Phillip J. Holcomb,et al.  Making sense of discourse: An fMRI study of causal inferencing across sentences , 2006, NeuroImage.

[12]  D. Wechsler Manual for the Wechsler Adult Intelligence Scale. , 1955 .

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

[14]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[15]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[16]  Jason P. Mitchell,et al.  Dissociable Medial Prefrontal Contributions to Judgments of Similar and Dissimilar Others , 2006, Neuron.

[17]  Peter Hagoort,et al.  Beyond the sentence given , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[18]  C. N. Macrae,et al.  Finding the Self? An Event-Related fMRI Study , 2002, Journal of Cognitive Neuroscience.

[19]  Rolf A. Zwaan,et al.  Situation models in language comprehension and memory. , 1998, Psychological bulletin.

[20]  F. Volkmar,et al.  Handbook of Autism and Pervasive Developmental Disorders , 1987 .

[21]  M. Kutas,et al.  Semantic integration in reading: engagement of the right hemisphere during discourse processing. , 1999, Brain : a journal of neurology.

[22]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[23]  D. Poeppel,et al.  Towards a functional neuroanatomy of speech perception , 2000, Trends in Cognitive Sciences.

[24]  I. Noens,et al.  Captured by details: sense-making, language and communication in autism. , 2005, Journal of communication disorders.

[25]  F. Happé Communicative competence and theory of mind in autism: A test of relevance theory , 1993, Cognition.

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

[27]  Karl J. Friston,et al.  Functional Imaging Studies of Neuropsychological Patients: Applications and Limitations , 2002, Neurocase.

[28]  Jean-Baptiste Poline,et al.  Perception of complex sounds: abnormal pattern of cortical activation in autism. , 2003, The American journal of psychiatry.

[29]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[30]  Jason P. Mitchell,et al.  Repetition suppression of ventromedial prefrontal activity during judgments of self and others , 2008, Proceedings of the National Academy of Sciences.

[31]  Remco J. Renken,et al.  Semantic ambiguity processing in sentence context: Evidence from event-related fMRI , 2007, NeuroImage.

[32]  Peter Hagoort,et al.  UvA-DARE (Digital Academic Repository) Unification of speaker and meaning in language comprehension: an fMRI study , 2022 .

[33]  R. Hu Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) , 2003 .

[34]  R. Müller,et al.  Brain Mapping of Language and Auditory Perception in High-Functioning Autistic Adults: A PET Study , 1999, Journal of autism and developmental disorders.

[35]  K. Zilles,et al.  Mind Reading: Neural Mechanisms of Theory of Mind and Self-Perspective , 2001, NeuroImage.

[36]  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.

[37]  Pascal Belin,et al.  Abnormal cortical voice processing in autism , 2004, Nature Neuroscience.

[38]  M. Greicius,et al.  Default-Mode Activity during a Passive Sensory Task: Uncoupled from Deactivation but Impacting Activation , 2004, Journal of Cognitive Neuroscience.

[39]  M. Dapretto,et al.  Neural basis of irony comprehension in children with autism: the role of prosody and context. , 2006, Brain : a journal of neurology.

[40]  Michael S. Gaffrey,et al.  Erratum to “Atypical participation of visual cortex during word processing in autism: An fMRI study of semantic decision” [Neuropsychologia 45 (2007) 1672–1684] , 2007, Neuropsychologia.

[41]  Matthew H. Davis,et al.  The neural mechanisms of speech comprehension: fMRI studies of semantic ambiguity. , 2005, Cerebral cortex.

[42]  Marcel Adam Just,et al.  Theory of Mind disruption and recruitment of the right hemisphere during narrative comprehension in autism , 2008, Neuropsychologia.

[43]  J. Grafman,et al.  Ventromedial Prefrontal Cortex Lesions in Humans Eliminate Implicit Gender Stereotyping , 2001, The Journal of Neuroscience.

[44]  Evelyn C. Ferstl,et al.  Emotional and Temporal Aspects of Situation Model Processing during Text Comprehension: An Event-Related fMRI Study , 2005, Journal of Cognitive Neuroscience.

[45]  C. Chabris,et al.  Brain activation during semantic processing in autism spectrum disorders via functional magnetic resonance imaging , 2006, Brain and Cognition.

[46]  Michael S. Gaffrey,et al.  A typical participation of visual cortex during word processing in autism: An fMRI study of semantic decision , 2007, Neuropsychologia.

[47]  G. Fink,et al.  Neural correlates of the first-person-perspective , 2003, Trends in Cognitive Sciences.

[48]  Denis Dooley,et al.  Atlas of the Human Brain. , 1971 .

[49]  S. Bookheimer,et al.  Form and Content Dissociating Syntax and Semantics in Sentence Comprehension , 1999, Neuron.

[50]  H. Tager-Flusberg,et al.  Identifying neurocognitive phenotypes in autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[51]  M. Just,et al.  Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. , 2004, Brain : a journal of neurology.

[52]  G. Shulman,et al.  Medial prefrontal cortex and self-referential mental activity: Relation to a default mode of brain function , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[53]  C. Neil Macrae,et al.  The Link between Social Cognition and Self-referential Thought in the Medial Prefrontal Cortex , 2005, Journal of Cognitive Neuroscience.

[54]  Jiang Xu,et al.  Language in context: emergent features of word, sentence, and narrative comprehension , 2005, NeuroImage.

[55]  Roel M. Willems,et al.  When language meets action: the neural integration of gesture and speech. , 2007, Cerebral cortex.

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

[57]  D. Poeppel,et al.  The cortical organization of speech processing , 2007, Nature Reviews Neuroscience.

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

[59]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[60]  Michael S. Gaffrey,et al.  Atypical [corrected] participation of visual cortex during word processing in autism: an fMRI study of semantic decision. , 2007, Neuropsychologia.

[61]  M. Iacoboni Failure to deactivate in autism: the co-constitution of self and other , 2006, Trends in Cognitive Sciences.

[62]  Sally Ozonoff,et al.  An Exploration of Right-Hemisphere Contributions to the Pragmatic Impairments of Autism , 1996, Brain and Language.

[63]  P. Hagoort On Broca, brain, and binding: a new framework , 2005, Trends in Cognitive Sciences.

[64]  Daniel P. Kennedy,et al.  Failing to deactivate: resting functional abnormalities in autism. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[65]  Rhea Paul,et al.  Language and communication in autism , 2005 .

[66]  D. A. Robertson,et al.  Functional Neuroanatomy of the Cognitive Process of Mapping During Discourse Comprehension , 2000, Psychological science.