The role of the fusiform face area in social cognition: implications for the pathobiology of autism.

A region in the lateral aspect of the fusiform gyrus (FG) is more engaged by human faces than any other category of image. It has come to be known as the 'fusiform face area' (FFA). The origin and extent of this specialization is currently a topic of great interest and debate. This is of special relevance to autism, because recent studies have shown that the FFA is hypoactive to faces in this disorder. In two linked functional magnetic resonance imaging (fMRI) studies of healthy young adults, we show here that the FFA is engaged by a social attribution task (SAT) involving perception of human-like interactions among three simple geometric shapes. The amygdala, temporal pole, medial prefrontal cortex, inferolateral frontal cortex and superior temporal sulci were also significantly engaged. Activation of the FFA to a task without faces challenges the received view that the FFA is restricted in its activities to the perception of faces. We speculate that abstract semantic information associated with faces is encoded in the FG region and retrieved for social computations. From this perspective, the literature on hypoactivation of the FFA in autism may be interpreted as a reflection of a core social cognitive mechanism underlying the disorder.

[1]  N. Kanwisher,et al.  How Distributed Is Visual Category Information in Human Occipito-Temporal Cortex? An fMRI Study , 2002, Neuron.

[2]  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.

[3]  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.

[4]  Alex Martin,et al.  Experience-dependent modulation of category-related cortical activity. , 2002, Cerebral cortex.

[5]  Isabel Gauthier,et al.  Social interest and the development of cortical face specialization: what autism teaches us about face processing. , 2002, Developmental psychobiology.

[6]  J. O'Doherty,et al.  Automatic and intentional brain responses during evaluation of trustworthiness of faces , 2002, Nature Neuroscience.

[7]  P. Cavanagh,et al.  Attention Response Functions Characterizing Brain Areas Using fMRI Activation during Parametric Variations of Attentional Load , 2001, Neuron.

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

[9]  A. Ishai,et al.  Distributed and Overlapping Representations of Faces and Objects in Ventral Temporal Cortex , 2001, Science.

[10]  N. Kanwisher,et al.  The Human Body , 2001 .

[11]  P. Sinha,et al.  Functional neuroanatomy of biological motion perception in humans , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[12]  T Yamamoto,et al.  Selective impairment of facial recognition due to a haematoma restricted to the right fusiform and lateral occipital region , 2001, Journal of neurology, neurosurgery, and psychiatry.

[13]  S. Bölte,et al.  Alterations of face processing strategies in autism: A fMRI study , 2001, NeuroImage.

[14]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[15]  B. Bertenthal,et al.  Does Perception of Biological Motion Rely on Specific Brain Regions? , 2001, NeuroImage.

[16]  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.

[17]  J. J. Ryan,et al.  Wechsler Adult Intelligence Scale-III , 2001 .

[18]  R. Adolphs,et al.  The human amygdala in social judgement , 2000 .

[19]  H. Critchley,et al.  The functional neuroanatomy of social behaviour: changes in cerebral blood flow when people with autistic disorder process facial expressions. , 2000, Brain : a journal of neurology.

[20]  A. Klin Attributing social meaning to ambiguous visual stimuli in higher-functioning autism and Asperger syndrome: The Social Attribution Task. , 2000, Journal of child psychology and psychiatry, and allied disciplines.

[21]  C. Frith,et al.  Movement and Mind: A Functional Imaging Study of Perception and Interpretation of Complex Intentional Movement Patterns , 2000, NeuroImage.

[22]  M. Tarr,et al.  FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise , 2000, Nature Neuroscience.

[23]  N. Kanwisher Domain specificity in face perception , 2000, Nature Neuroscience.

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

[25]  Dermot M. Bowler,et al.  Attribution of Mechanical and Social Causality to Animated Displays by Children with Autism , 2000 .

[26]  E. Bullmore,et al.  The amygdala theory of autism , 2000, Neuroscience & Biobehavioral Reviews.

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

[28]  I. Gauthier,et al.  Expertise for cars and birds recruits brain areas involved in face recognition , 2000, Nature Neuroscience.

[29]  C. Frith,et al.  Reading the mind in cartoons and stories: an fMRI study of ‘theory of mind’ in verbal and nonverbal tasks , 2000, Neuropsychologia.

[30]  Leslie G. Ungerleider,et al.  Object-form topology in the ventral temporal lobe Response to I. Gauthier (2000) , 2000, Trends in Cognitive Sciences.

[31]  U. Frith,et al.  Do triangles play tricks? Attribution of mental states to animated shapes in normal and abnormal development , 2000 .

[32]  Michael Davis,et al.  The amygdala , 2000, Current Biology.

[33]  J. Haxby,et al.  Distinct representations of eye gaze and identity in the distributed human neural system for face perception , 2000, Nature Neuroscience.

[34]  F. Volkmar,et al.  A Normed Study of Face Recognition in Autism and Related Disorders , 1999, Journal of autism and developmental disorders.

[35]  C. Frith,et al.  Interacting minds--a biological basis. , 1999, Science.

[36]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

[37]  Leslie G. Ungerleider,et al.  Distributed representation of objects in the human ventral visual pathway. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  T. Allison,et al.  Electrophysiological studies of human face perception. I: Potentials generated in occipitotemporal cortex by face and non-face stimuli. , 1999, Cerebral cortex.

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

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

[41]  John C. Gore,et al.  ROC Analysis of Statistical Methods Used in Functional MRI: Individual Subjects , 1999, NeuroImage.

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

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

[44]  R. Dolan,et al.  Conscious and unconscious emotional learning in the human amygdala , 1998, Nature.

[45]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[46]  Donna B. Pincus,et al.  Distinguishing Lies from Jokes: Theory of Mind Deficits and Discourse Interpretation in Right Hemisphere Brain-Damaged Patients , 1998, Brain and Language.

[47]  S. Rauch,et al.  Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge , 1998, The Journal of Neuroscience.

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

[49]  M. Ernst,et al.  Low medial prefrontal dopaminergic activity in autistic children , 1997, The Lancet.

[50]  M S Buchsbaum,et al.  Anterior cingulate gyrus volume and glucose metabolism in autistic disorder. , 1997, The American journal of psychiatry.

[51]  R. Lane,et al.  Neuroanatomical correlates of happiness, sadness, and disgust. , 1997, The American journal of psychiatry.

[52]  Karl J. Friston,et al.  Neuroanatomical correlates of externally and internally generated human emotion. , 1997, The American journal of psychiatry.

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

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

[55]  Alan C. Evans,et al.  Specific Involvement of Human Parietal Systems and the Amygdala in the Perception of Biological Motion , 1996, The Journal of Neuroscience.

[56]  E. Rolls,et al.  Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage , 1996, Neuropsychologia.

[57]  Michael Siegal,et al.  Theory of Mind and Pragmatic Understanding Following Right Hemisphere Damage , 1996, Brain and Language.

[58]  T. Robbins,et al.  Dissociation in prefrontal cortex of affective and attentional shifts , 1996, Nature.

[59]  A. Damasio,et al.  Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. , 1996, Cerebral cortex.

[60]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[61]  S. Carmichael,et al.  Networks related to the orbital and medial prefrontal cortex; a substrate for emotional behavior? , 1996, Progress in brain research.

[62]  J. Price,et al.  Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys , 1995, The Journal of comparative neurology.

[63]  Richard S. J. Frackowiak,et al.  Other minds in the brain: a functional imaging study of “theory of mind” in story comprehension , 1995, Cognition.

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

[65]  M. Hallett,et al.  Modeling other minds , 1995, Neuroreport.

[66]  Edmund T. Rolls,et al.  A theory of emotion and consciousness, and its application to understanding the neural basis of emotion. , 1995 .

[67]  T. Naidich,et al.  Limbic connections. , 1995, AJNR. American journal of neuroradiology.

[68]  IIse Kracke,et al.  DEVELOPMENTAL PROSOPAGNOSIA IN ASPERGER SYNDROME: PRESENTATION AND DISCUSSION OF AN INDIVIDUAL CASE , 1994, Developmental medicine and child neurology.

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

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

[71]  E. Lauterbach The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction , 1993 .

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

[73]  P. Mundy,et al.  Empathy and cognition in high-functioning children with autism. , 1992, Child development.

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

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

[76]  A. Damasio,et al.  Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli , 1990, Behavioural Brain Research.

[77]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[78]  S. Folstein,et al.  Recognition and expression of emotional cues by autistic and normal adults. , 1989, Journal of child psychology and psychiatry, and allied disciplines.

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

[80]  R. P. Hobson,et al.  Emotion recognition in autism: coordinating faces and voices , 1988, Psychological Medicine.

[81]  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.

[82]  Mortimer Mishkin,et al.  Visual recognition impairment follows ventromedial but not dorsolateral prefrontal lesions in monkeys , 1986, Behavioural Brain Research.

[83]  D. Amaral,et al.  Amygdalo‐cortical projections in the monkey (Macaca fascicularis) , 1984, The Journal of comparative neurology.

[84]  J. Eccles The emotional brain. , 1980, Bulletin et memoires de l'Academie royale de medecine de Belgique.

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

[86]  R. Myers,et al.  Loss of social group affinity following prefrontal lesions in free-ranging macaques. , 1973, Brain research.

[87]  J. A. McDonald,et al.  Orality, Preference Behavior, and Reinforcement Value of Nonfood Object in Monkeys with Orbital Frontal Lesions , 1969, Science.

[88]  H. Laborit,et al.  [Experimental study]. , 1958, Bulletin mensuel - Societe de medecine militaire francaise.

[89]  F. Heider,et al.  An experimental study of apparent behavior , 1944 .