Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome.

BACKGROUND Recognition of individual faces is an integral part of both interpersonal interactions and successful functioning within a social group. Therefore, it is of considerable interest that individuals with autism and related conditions have selective deficits in face recognition (sparing nonface object recognition). METHOD We used functional magnetic resonance imaging (fMRI) to study face and subordinate-level object perception in 14 high-functioning individuals with autism or Asperger syndrome (the autism group), in comparison with 2 groups of matched normal controls (normal control group ] [NC1] and normal control group 2 [NC2]) (n = 14 for each). Regions of interest (ROIs) were defined in NC1 and then applied in comparisons between NC2 and the autism group. Regions of interest were also defined in NC2 and then applied to comparisons between NC1 and the autism group as a replication study. RESULTS In the first set of comparisons, we found significant task x group interactions for the size of activation in the right fusiform gyrus (FG) and right inferior temporal gyri (ITG). Post hoc analyses showed that during face (but not object) discrimination, the autism group had significantly greater activation than controls in the right ITG and less activation of the right FG. The replication study showed again that the autism group used the ITG significantly more for processing faces than the control groups, but for these analyses, the effect was now on the left side. Greater ITG activation was the pattern found in both control groups during object processing. CONCLUSIONS Individuals with autism spectrum disorders demonstrate a pattern of brain activity during face discrimination that is consistent with feature-based strategies that are more typical of nonface object perception.

[1]  M. Tarr,et al.  Activation of the middle fusiform 'face area' increases with expertise in recognizing novel objects , 1999, Nature Neuroscience.

[2]  Leslie G. Ungerleider,et al.  The Effect of Face Inversion on Activity in Human Neural Systems for Face and Object Perception , 1999, Neuron.

[3]  C. Feinstein,et al.  Memory for Faces in Children with Autism , 1998 .

[4]  A. Meltzoff,et al.  Neuropsychological correlates of early symptoms of autism. , 1998, Child development.

[5]  M. D’Esposito,et al.  An Area within Human Ventral Cortex Sensitive to “Building” Stimuli Evidence and Implications , 1998, Neuron.

[6]  Heinrich H Bülthoff,et al.  Image-based object recognition in man, monkey and machine , 1998, Cognition.

[7]  M. Farah,et al.  What is "special" about face perception? , 1998, Psychological review.

[8]  R. Adolphs,et al.  The human amygdala in social judgment , 1998, Nature.

[9]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

[10]  Daniel R. Weinberger,et al.  Neonatal lesions of the medial temporal lobe disrupt prefrontal cortical regulation of striatal dopamine , 1998, Nature.

[11]  Faces, Animals, and Animals with Obscured Faces Elicit Similar fMRI Activation in the Ventral Object Vision Pathway , 1998, NeuroImage.

[12]  R T Constable,et al.  Quantifying and comparing region-of-interest activation patterns in functional brain MR imaging: methodology considerations. , 1998, Magnetic resonance imaging.

[13]  J A Frank,et al.  Altered development of prefrontal neurons in rhesus monkeys with neonatal mesial temporo-limbic lesions: a proton magnetic resonance spectroscopic imaging study. , 1997, Cerebral cortex.

[14]  Karl J. Friston,et al.  How the brain learns to see objects and faces in an impoverished context , 1997, Nature.

[15]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

[16]  L. Mottron,et al.  Visual agnosia with bilateral temporo‐occipital brain lesions in a child with autistic disorder: a case study , 1997, Developmental medicine and child neurology.

[17]  M. Raichle,et al.  Anatomic Localization and Quantitative Analysis of Gradient Refocused Echo-Planar fMRI Susceptibility Artifacts , 1997, NeuroImage.

[18]  M. Tarr,et al.  Levels of categorization in visual recognition studied using functional magnetic resonance imaging , 1997, Current Biology.

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

[20]  M. Tarr,et al.  Becoming a “Greeble” Expert: Exploring Mechanisms for Face Recognition , 1997, Vision Research.

[21]  Charles L. Wilson,et al.  Single Neuron Activity in Human Hippocampus and Amygdala during Recognition of Faces and Objects , 1997, Neuron.

[22]  C. Moorehead All rights reserved , 1997 .

[23]  J. Mazziotta,et al.  A Locus in Human Extrastriate Cortex for Visual Shape Analysis , 1997, Journal of Cognitive Neuroscience.

[24]  S. Rauch,et al.  Response and Habituation of the Human Amygdala during Visual Processing of Facial Expression , 1996, Neuron.

[25]  U. Frith,et al.  Cognitive explanations of autism , 1996, Acta paediatrica (Oslo, Norway : 1992). Supplement.

[26]  J. Haxby,et al.  Functional Magnetic Resonance Imaging of Human Visual Cortex during Face Matching: A Comparison with Positron Emission Tomography , 1996, NeuroImage.

[27]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[28]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

[29]  F. Volkmar,et al.  Validity and neuropsychological characterization of Asperger syndrome: convergence with nonverbal learning disabilities syndrome. , 1995, Journal of child psychology and psychiatry, and allied disciplines.

[30]  T. Allison,et al.  Face-sensitive regions in human extrastriate cortex studied by functional MRI. , 1995, Journal of neurophysiology.

[31]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Daniel L. Schacter,et al.  Brain regions associated with retrieval of structurally coherent visual information , 1995, Nature.

[33]  Hisao Nishijo,et al.  Amygdala role in conditioned associative learning , 1995, Progress in Neurobiology.

[34]  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.

[35]  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.

[36]  D. Bishop,et al.  Face perception in children with autism and Asperger's syndrome. , 1994, Journal of child psychology and psychiatry, and allied disciplines.

[37]  G. Dawson,et al.  Early recognition of children with autism: A study of first birthday home videotapes , 1994, Journal of autism and developmental disorders.

[38]  J. Bachevalier Medial temporal lobe structures and autism: A review of clinical and experimental findings , 1994, Neuropsychologia.

[39]  Commentary on “a new series of slides depicting facial expressions of affect” by Mazurski and Bond (1993) , 1994 .

[40]  L. Mottron,et al.  A Study of Perceptual Analysis in a High-Level Autistic Subject with Exceptional Graphic Abilities , 1993, Brain and Cognition.

[41]  L. Brothers,et al.  Mesial temporal neurons in the macaque monkey with responses selective for aspects of social stimuli , 1993, Behavioural Brain Research.

[42]  J. Aggleton The contribution of the amygdala to normal and abnormal emotional states , 1993, Trends in Neurosciences.

[43]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

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

[45]  J. Sattler Assessment of Children , 1992 .

[46]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[47]  W. Singer,et al.  Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. , 1992, Science.

[48]  Leslie G. Ungerleider,et al.  Lesions of inferior temporal area TE in infant monkeys alter cortico-amygdalar projections. , 1991, Neuroreport.

[49]  Mark H. Johnson,et al.  CONSPEC and CONLERN: a two-process theory of infant face recognition. , 1991, Psychological review.

[50]  Martha J. Farah,et al.  Cognitive Neuropsychology: Patterns of Co-occurrence Among the Associative Agnosias: Implications for Visual Object Representation , 1991 .

[51]  H. Nicholson,et al.  Autistic children's ability to interpret faces: a research note. , 1989, Journal of child psychology and psychiatry, and allied disciplines.

[52]  F. Volkmar,et al.  Facial perception in autism. , 1989, Journal of child psychology and psychiatry, and allied disciplines.

[53]  Mark Braverman,et al.  Affect comprehension in children with pervasive developmental disorders , 1989, Journal of autism and developmental disorders.

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

[55]  T. Valentine Upside-down faces: a review of the effect of inversion upon face recognition. , 1988, British journal of psychology.

[56]  A. Lee,et al.  What's in a face? The case of autism. , 1988, British journal of psychology.

[57]  M. Wiznitzer,et al.  AIDS and the Nervous System , 1988, Neurology.

[58]  D. Gaffan,et al.  Disconnection of the amygdala from visual association cortex impairs visual reward-association learning in monkeys , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  J. Sattler Assessment of children, 3rd ed. , 1988 .

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

[61]  S. Carey,et al.  Why faces are and are not special: an effect of expertise. , 1986, Journal of experimental psychology. General.

[62]  A R Damasio,et al.  A neurological model for childhood autism. , 1978, Archives of neurology.

[63]  T. Langdell,et al.  Recognition of faces: an approach to the study of autism. , 1978, Journal of child psychology and psychiatry, and allied disciplines.

[64]  H. D. Steklis,et al.  A neural substrate for affiliative behavior in nonhuman primates. , 1976, Brain, behavior and evolution.

[65]  P. Ekman,et al.  Unmasking the face : a guide to recognizing emotions from facial clues , 1975 .

[66]  David Wechsler,et al.  Manual for the Wechsler intelligence scale for children , 1974 .

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

[68]  G. Sackett Monkeys Reared in Isolation with Pictures as Visual Input: Evidence for an Innate Releasing Mechanism , 1966, Science.

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

[70]  Karl H. Pribram,et al.  Influence of amygdalectomy on social behavior in monkeys. , 1954, Journal of comparative and physiological psychology.