Attention does not modulate neural responses to social stimuli in autism spectrum disorders

We investigated whether individuals with autism spectrum disorders (ASD) would show attentional modulation for social (face) and non-social (house) stimuli. Sixteen individuals with ASD and 16 matched control participants completed a task in which pairs of face and house stimuli were present on every trial, with one of the pairs randomly assigned to attended locations and the other to unattended locations. Both mass-univariate (SPM) and region of interest analyses suggested that responses to houses were modulated by attention in both groups, but that only the control participants demonstrated attentional modulation of face-selective regions. Thus, the participants with ASD demonstrated a lack of attentional modulation which was particularly evident for the social stimulus. Analyses of effective connectivity indicated that these results were due to a failure of attention to modulate connectivity between extrastriate areas and V1. We discuss how these results may suggest a mechanism to explain the reduced salience of social stimuli in ASD.

[1]  L Cipolotti,et al.  Fractionation of visual memory: agency detection and its impairment in autism , 2002, Neuropsychologia.

[2]  F. Happé Autism: cognitive deficit or cognitive style? , 1999, Trends in Cognitive Sciences.

[3]  Leslie G. Ungerleider,et al.  Neuroimaging Studies of Attention: From Modulation of Sensory Processing to Top-Down Control , 2003, The Journal of Neuroscience.

[4]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe , 1989, The Journal of comparative neurology.

[5]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

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

[7]  E. Hill Executive dysfunction in autism , 2004, Trends in Cognitive Sciences.

[8]  Veikko Jousmäki,et al.  Abnormal activation of face processing systems at early and intermediate latency in individuals with autism spectrum disorder: a magnetoencephalographic study , 2005, The European journal of neuroscience.

[9]  Chris Moore,et al.  The development of attention and joint attention in children with autism , 2001 .

[10]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[11]  Leslie G. Ungerleider,et al.  The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  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.

[13]  P. Skudlarski,et al.  The role of the fusiform face area in social cognition: implications for the pathobiology of autism. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[15]  J. Burack,et al.  Selective attention deficits in persons with autism: preliminary evidence of an inefficient attentional lens. , 1994, Journal of abnormal psychology.

[16]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[17]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[18]  C. Lord,et al.  Austism diagnostic observation schedule: A standardized observation of communicative and social behavior , 1989, Journal of autism and developmental disorders.

[19]  M. Corbetta,et al.  A PET study of visuospatial attention , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[20]  Karl J. Friston,et al.  Voxel based morphometry of 465 normal adult human brains , 2000, NeuroImage.

[21]  Leslie G. Ungerleider,et al.  Projections from inferior temporal cortex to prefrontal cortex via the uncinate fascicle in rhesus monkeys , 2004, Experimental Brain Research.

[22]  Alberto Beltramello,et al.  A comparison between the accuracy of voxel‐based morphometry and hippocampal volumetry in Alzheimer's disease , 2004, Journal of magnetic resonance imaging : JMRI.

[23]  R. Dolan,et al.  Effects of Attention and Emotion on Face Processing in the Human Brain An Event-Related fMRI Study , 2001, Neuron.

[24]  Karl J. Friston,et al.  Event‐related f MRI , 1997, Human brain mapping.

[25]  G. Baird,et al.  The frequency and distribution of spontaneous attention shifts between social and nonsocial stimuli in autistic, typically developing, and nonautistic developmentally delayed infants. , 1998, Journal of child psychology and psychiatry, and allied disciplines.

[26]  C D Frith,et al.  Space-based and object-based visual attention: shared and specific neural domains. , 1997, Brain : a journal of neurology.

[27]  S. Baron-Cohen,et al.  The Autism-Spectrum Quotient (AQ): Evidence from Asperger Syndrome/High-Functioning Autism, Malesand Females, Scientists and Mathematicians , 2001, Journal of autism and developmental disorders.

[28]  C. Frith What do imaging studies tell us about the neural basis of autism? , 2003, Novartis Foundation symposium.

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

[30]  R. Dolan,et al.  Contrast polarity and face recognition in the human fusiform gyrus , 1999, Nature Neuroscience.

[31]  F. Volkmar,et al.  Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. , 2002, Archives of general psychiatry.

[32]  E. Courchesne,et al.  Face processing occurs outside the fusiform 'face area' in autism: evidence from functional MRI. , 2001, Brain : a journal of neurology.

[33]  K. Nakayama,et al.  Binocular Rivalry and Visual Awareness in Human Extrastriate Cortex , 1998, Neuron.

[34]  J. Russell Autism as an executive disorder , 1997 .

[35]  G. Dawson,et al.  Early social attention impairments in autism: social orienting, joint attention, and attention to distress. , 2004, Developmental psychology.

[36]  J Townsend,et al.  Impairment in shifting attention in autistic and cerebellar patients. , 1994, Behavioral neuroscience.

[37]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[38]  M. Belmonte,et al.  Abnormal Attention in Autism Shown by Steady-State Visual Evoked Potentials , 2000 .

[39]  Geraldine Dawson,et al.  Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. , 2002, Child development.

[40]  A. Dale,et al.  The Representation of Illusory and Real Contours in Human Cortical Visual Areas Revealed by Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[41]  Christopher F. Chabris,et al.  Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces , 2004, NeuroImage.

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

[43]  Karl J. Friston,et al.  Attentional modulation of effective connectivity from V2 to V5/MT in humans. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[44]  Susan E. Bryson,et al.  Visual-spatial orienting in autism , 1996, Journal of autism and developmental disorders.

[45]  Richard S. J. Frackowiak,et al.  Functional localization of the system for visuospatial attention using positron emission tomography. , 1997, Brain : a journal of neurology.

[46]  E. Courchesne,et al.  The brain response to personally familiar faces in autism: findings of fusiform activity and beyond. , 2004, Brain : a journal of neurology.

[47]  R. Desimone,et al.  Neural mechanisms of selective visual attention. , 1995, Annual review of neuroscience.

[48]  J. Boucher,et al.  Unfamiliar face recognition in relatively able autistic children. , 1992, Journal of child psychology and psychiatry, and allied disciplines.

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

[50]  Uta Frith,et al.  Theory of mind , 2001, Current Biology.

[51]  N. Kanwisher,et al.  Covert visual attention modulates face-specific activity in the human fusiform gyrus: fMRI study. , 1998, Journal of neurophysiology.

[52]  Karl J. Friston,et al.  Cerebral Asymmetry and the Effects of Sex and Handedness on Brain Structure: A Voxel-Based Morphometric Analysis of 465 Normal Adult Human Brains , 2001, NeuroImage.