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Frontal contributions to face processing differences in autism: Evidence from fMRI of inverted face processing

  • SUSAN Y. BOOKHEIMER (a1) (a2), A. TING WANG (a3), ASHLEY SCOTT (a1), MARIAN SIGMAN (a1) (a2) and MIRELLA DAPRETTO (a1)...
Abstract
Abstract

Functional neuroimaging studies of face processing deficits in autism have typically focused on visual processing regions, such as the fusiform face area (FFA), which have shown reduced activity in autism spectrum disorders (ASD), though inconsistently. We recently reported reduced activity in the inferior frontal region in ASD, implicating impaired mirror-neuron systems during face processing. In the present study, we used fMRI during a face processing task in which subjects had to match faces presented in the upright versus inverted position. Typically developing (TD) children showed a classic behavioral inversion effect, increased reaction time for inverted faces, while this effect was significantly reduced in ASD subjects. The fMRI data showed similar responses in the fusiform face area for ASD and TD children, with both groups demonstrating increased activation for inverted faces. However, the groups did differ in several brain regions implicated in social cognition, particularly prefrontal cortex and amygdala. These data suggest that the behavioral differences in processing upright versus inverted faces for TD children are related not to visual information processing but to the social significance of the stimuli. Our results are consistent with other recent studies implicating frontal and limbic dysfunction during face processing in autism. (JINS, 2008, 14, 922–932.)

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Copyright
Corresponding author
Correspondence and reprint requests to: Susan Y. Bookheimer, Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, 760 Westwood Plaza, Los Angeles, CA 90095. E-mail: sbook@ucla.edu
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G.K. Aguirre , R. Singh , & M. D'Esposito (1999). Stimulus inversion and the responses of face and object-sensitive cortical areas. Neuroreport, 10, 189194.

C. Ashwin , S. Wheelwright , & S. Baron-Cohen (2006). Finding a face in the crowd: Testing the anger superiority effect in Asperger Syndrome. Brain and Cognition, 61, 7895.

J.J. Barton , R.L. Hefter , M.V. Cherkasova , & D.S. Manoach (2007). Investigations of face expertise in the social developmental disorders. Neurology, 69, 860870.

J. Barton , J. Keenan , & T. Bass (2001). Discrimination of spatial relations and features in faces: Effects of inversion and viewing duration. British Journal of Psychology, 92, 527549.

M. Behrmann , G. Avidan , G.L. Leonard , R. Kimchi , B. Luna , K. Humphreys , & N. Minshew (2006). Configural processing in autism and its relationship to face processing. Neuropsychologia, 44, 110129.

S.K. Berument , M. Rutter , C. Lord , A. Pickles , & A. Bailey (1999). Autism screening questionnaire: Diagnostic validity. British Journal of Psychiatry, 175, 444451.

A.C. Burggren , G.W. Small , F.W. Sabb , & S.Y. Bookheimer (2002). Specificity of brain activation patterns in people at genetic risk for Alzheimer's disease. American Journal of Geriatric Psychiatry, 10, 4451.

R. Campbell , K. Lawrence , W. Mandy , C. Mitra , L. Jeyakuma , & D. Skuse (2006). Meanings in motion and faces: Developmental associations between the processing of intention from geometrical animations and gaze detection accuracy. Development and Psychopathology, 18, 99118.

L. Carr , M. Iacoboni , M.C. Dubeau , J.J. Mazziotta , & G.L. Lenzi (2003). Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proceedings of the National Academy of Science of the United States of America, 100, 54975502.

K. Chawarska , A. Klin , & F. Volkmar (2003). Automatic attention cueing through eye movement in 2-year-old children with autism. Child Development, 74, 11081122.

M. Dapretto , M.S. Davies , J.H. Pfeifer , A.A. Scott , M. Sigman , S.Y. Bookheimer , & M. Iacoboni (2006). Understanding emotions in others: Mirror neuron dysfunction in children with autism spectrum disorders. Nature Neuroscience, 9, 2830.

L.M. Dunn & L.M. Dunn (1997). Peabody Picture Vocabulary Test: III. Circle Pines, MN: American Guidance Service.

P. Ekman & W. Friesen (1976). Measuring facial movement. Environmental Psychology and Nonverbal Behavior, 1, 5675.

M. Farah , P. McMullen , & M. Meyer (1991). Can recognition of living things be selectively impaired? Neuropsychologia, 29, 185193.

M.J. Farah , J.W. Tanaka , & H.M. Drain (1995a). What causes the face inversion effect? Journal of Experimental Psychology. Human Perception and Performance, 21, 628634.

M.J. Farah , K.D. Wilson , H.M. Drain , & J.R. Tanaka (1995b). The inverted face inversion effect in prosopagnosia: Evidence for mandatory, face-specific perceptual mechanisms. Vision Research, 35, 20892093.

A. Freire , K. Lee , & L.A. Symons (2000). The face-inversion effect as a deficit in the encoding of configural information: Direct evidence. Perception, 29, 159170.

U. Frith (2007). The social brain? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 362, 671678.

N. Hadjikhani , R.M. Joseph , J. Snyder , C.F. Chabris , J. Clark , S. Steele , L. McGrath , M. Vangel , I. Aharon , E. Feczko , G.J. Harris , & H. Tager-Flusberg (2004). Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces. Neuroimage, 22, 11411150.

N. Hadjikhani , R.M. Joseph , J. Snyder , & H. Tager-Flusberg (2006). Anatomical differences in the mirror neuron system and social cognition network in autism. Cerebral Cortex, 16, 12761282.

N. Hadjikhani , R.M. Joseph , J. Snyder , & H. Tager-Flusberg (2007). Abnormal activation of the social brain during face perception in autism. Human Brain Mapping, 28, 441449.

F. Happe & U. Frith (2006). The weak coherence account: Detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36, 525.

J.V. Haxby , L.G. Ungerleider , V.P. Clark , J.L. Schouten , E.A. Hoffman , & A. Martin (1999). The effect of face inversion on activity in human neural systems for face and object perception. Neuron, 22, 189199.

R.P. Hobson , J. Ouston , & A. Lee (1988). What's in a face? The case of autism. British Journal of Psychology, 79(Pt 4), 441453.

M. Iacoboni (2005). Neural mechanisms of imitation. Current Opinion in Neurobiology, 15, 632637.

M. Iacoboni & M. Dapretto (2006). The mirror neuron system and the consequences of its dysfunction. Nature Reviews. Neuroscience, 7, 942951.

A. Klin , W. Jones , R. Schultz , F. Volkmar , & D. Cohen (2002). Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry, 59, 809816.

J.K. Kroger , F.W. Sabb , C. Fales , S.Y. Bookheimer , M.S. Cohen , & K.J. Holyoak (2002). Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: A parametric study of relational complexity. Cerebral Cortex, 12, 477485.

C. Lord , S. Risi , L. Lambrecht , E.H. Cook Jr., B.L. Leventhal , P.C. DiLavore , A. Pickles , & M. Rutter (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30, 205223.

C. Lord , M. Rutter , & A. Le Couteur (1994). Autism Diagnostic Interview-Revised: A revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659685.

L. Mottron , S. Belleville , & E. Menard (1999). Local bias in autistic subjects as evidenced by graphic tasks: Perceptual hierarchization or working memory deficit? Journal of Child Psychology and Psychiatry, and Allied Disciplines, 40, 743755.

E. Pellicano , L. Jeffery , D. Burr , & G. Rhodes (2007). Abnormal adaptive face-coding mechanisms in children with autism spectrum disorder. Current Biology, 17, 15081512.

K.A. Pelphrey , J.P. Morris , & G. McCarthy (2005). Neural basis of eye gaze processing deficits in autism. Brain, 128(Pt 5), 10381048.

K.A. Pelphrey , J.P. Morris , G. McCarthy , & K.S. Labar (2007). Perception of dynamic changes in facial affect and identity in autism. Social Cognitive and Affective Neuroscience, 2, 140149.

K. Pierce , F. Haist , F. Sedaghat , & E. Courchesne (2004). The brain response to personally familiar faces in autism: Findings of fusiform activity and beyond. Brain, 127(Pt 12), 27032716.

K. Pierce , R.A. Muller , J. Ambrose , G. Allen , & E. Courchesne (2001). Face processing occurs outside the fusiform ‘face area’ in autism: Evidence from functional MRI. Brain, 124(Pt 10), 20592073.

J. Piggot , H. Kwon , D. Mobbs , C. Blasey , L. Lotspeich , V. Menon , S. Bookheimer , & A.L. Reiss (2004). Emotional attribution in high-functioning individuals with autistic spectrum disorder: A functional imaging study. Journal of the American Academy of Child and Adolescent Psychiatry, 43, 473480.

M.E. Raichle , A.M. MacLeod , A.Z. Snyder , W.J. Powers , D.A. Gusnard , & G.L. Shulman (2001). A default mode of brain function. Proceedings of the National Academy of Sciences of the United States of America, 98, 676682.

M.E. Raichle & A.Z. Snyder (2007). A default mode of brain function: A brief history of an evolving idea. Neuroimage, 37, 10831090; discussion 1097–1099.

F.E. Rose , A.J. Lincoln , Z. Lai , M. Ene , Y.M. Searcy , & U. Bellugi (2007). Orientation and affective expression effects on face recognition in Williams syndrome and autism. Journal of Autism and Developmental Disorders, 37, 513522.

R.T. Schultz , I. Gauthier , A. Klin , R.K. Fulbright , A.W. Anderson , F. Volkmar , P. Skudlarski , C. Lacadie , D.J. Cohen , & J.C. Gore (2000). Abnormal ventral temporal cortical activity during face discrimination among individuals with autism and Asperger syndrome. Archives of General Psychiatry, 57, 331340.

J. Talairach & P. Tournoux (1988). Co-Planar Stereotaxic Atlas of the Human Brain. New York: Thieme Medical Publishers.

J.P. Teunisse & B. de Gelder (2003). Face processing in adolescents with autistic disorder: The inversion and composite effects. Brain and Cognition, 52, 285294.

A.T. Wang , M. Dapretto , A.R. Hariri , M. Sigman , & S.Y. Bookheimer (2004). Neural correlates of facial affect processing in children and adolescents with autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 43, 481490.

D. Wechler (1991). Wechler Intelligence Scale for Children–Third Edition. San Antonio, TX: The Psychological Corporation.

R. Woods , S. Grafton , C. Holmes , S. Cherry , & J. Mazziotta (1998). Automated image registration: I. General methods and intrasubject, intramodality validation. Journal of Computer Assisted Tomography, 22, 141154.

R.K. Yin (1969). Looking at upside-down faces. Journal of Experimental Psychology, 81, 141145.

G. Yovel & N. Kanwisher (2004). Face perception: Domain specific, not process specific. Neuron, 44, 889898.

G. Yovel & N. Kanwisher (2005). The neural basis of the behavioral face-inversion effect. Current Biology, 15, 22562262.

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