Abnormal activation of face processing systems at early and intermediate latency in individuals with autism spectrum disorder: A magnetoencephalographic study
Abstract
The neurological basis of developmental psychopathology in autism is a matter of intense debate. Magnetoencephalography (MEG) was used to study the neuronal responses associated with the processing of faces in 12 able adults with autism spectrum disorders (ASD), performing image categorization and image identification tasks. The neuromagnetic data were analysed using nonparametric time-series analysis and equivalent current dipole estimation. Comparison data were obtained from 22 normally developing adults. In individuals with ASD, the neural responses to images of faces, observed in right extrastriate cortices at approximately 145 ms after stimulus onset, were significantly weaker, less lateralized and less affected by stimulus repetition than in control subjects. Early latency (30-60 ms) responses to face images, over right anterior temporal regions, differed significantly between the two subject groups in the image identification task. No such difference was observed for images of mugs or meaningless geometrical patterns. These findings suggest that, during the course of development in individuals with ASD, the cortical activity associated with the processing of human faces assumes a different-from-normal localization in extrastriate brain regions. This abnormal localization may be associated with unusual, but nevertheless face-specific, fast processing pathways.
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To date there is one published MEG study of neural responses in ASD populations to faces.
“To date there is one published MEG study of neural responses in ASD populations to faces (Bailey, Braeutigam, Jousmäki, & Swithenby, 2005).”
From Vision in autism spectrum disorders (2009) · cites this paper as Bailey et al., 2005
Cites
The fusiform face area: a module in human extrastriate cortex specialized for face perception
Kanwisher, N., McDermott, J., & Chun, M. M. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-11-04302.1997 · Cited by 7,738 · see citing works
The distributed human neural system for face perception
Haxby, J. V., Hoffman, E. A., & Gobbini, M. I. (2000) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(00)01482-0 · Cited by 4,891 · see citing works
Baron‐Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00715 · Cited by 4,555 · cited 2× · see citing works
“…to judge complex mental states from the eyes is the core face processing deficit in individuals on the autistic spectrum (Adolphs et al., 2001; Baron-Cohen et al., 2001), there are also reports of impairments in identity recognition (Klin et al., 1999) and in the ability to judge eye gaze…”
BackgroundBaron‐Cohen, S., Wheelwright, S. J., Hill, J., Raste, Y., & Plumb, I. (2001) · PubMed · Cited by 4,313 · see citing works
Electrophysiological Studies of Face Perception in Humans
Shlomo Bentin, A., Allison, T., Puce, A., Perez, E., & McCarthy, G. (1996) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1996.8.6.551 · Cited by 3,081 · see citing works
Autism as a strongly genetic disorder: evidence from a British twin study
Bailey, A., Le Couteur, A., Gottesman, I., Bolton, P., Simonoff, E., Yuzda, E., & Rutter, M. (1995) · Psychological Medicine · doi:10.1017/s0033291700028099 · Cited by 2,461 · see citing works
Self-citationFace-specific processing in the human fusiform gyrus
McCarthy, G., Puce, A., Gore, J. C., & Allison, T. (1997) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1997.9.5.605 · Cited by 1,127 · see citing works
A clinicopathological study of autism
Bailey, A. (1998) · Brain · doi:10.1093/brain/121.5.889 · Cited by 1,083 · see citing works
Self-citationHaxby, J., Horwitz, B., Ungerleider, L. G., Maisog, J. M., Pietrini, P., & Grady, C. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06336.1994 · Cited by 1,065 · see citing works
Schultz, R. T., Gauthier, I., Klin, A., Fulbright, R. K., Anderson, A. W., Volkmar, F., Skudlarski, P., Lacadie, C., Cohen, D. J., & Gore, J. C. (2000) · Archives of General Psychiatry · doi:10.1001/archpsyc.57.4.331 · Cited by 1,000 · see citing works
Face processing occurs outside the fusiform ‘face area’ in autism: evidence from functional MRI
Pierce, K. (2001) · Brain · doi:10.1093/brain/124.10.2059 · Cited by 898 · see citing works
Visual attention mediated by biased competition in extrastriate visual cortex
Desimone, R. (1998) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.1998.0280 · Cited by 696 · see citing works
Stages of processing in face perception: an MEG study
Jia Liu, B., Harris, A. M., & Kanwisher, N. (2002) · Nature Neuroscience · doi:10.1038/nn909 · Cited by 683 · see citing works
Abnormal Processing of Social Information from Faces in Autism
Adolphs, R., Sears, L. L., & Piven, J. (2001) · Journal of Cognitive Neuroscience · doi:10.1162/089892901564289 · Cited by 590 · see citing works
Neuropathology of Infantile Autism
Kemper, T. L., & Bauman, M. (1998) · Journal of Neuropathology and Experimental Neurology · doi:10.1097/00005072-199807000-00001 · Cited by 585 · see citing works
Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism
Howard, M. A., Cowell, P. E., Boucher, J., Broks, P., Mayes, A. R., Farrant, A., & Roberts, N. P. (2000) · Neuroreport · doi:10.1097/00001756-200009110-00020 · Cited by 479 · see citing works
The role of the fusiform face area in social cognition: implications for the pathobiology of autism
Schultz, R. T., Grelotti, D. J., Klin, A., Kleinman, J., Van der Gaag, C., Marois, R., & Skudlarski, P. (2003) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2002.1208 · Cited by 469 · see citing works
Covert Visual Attention Modulates Face-Specific Activity in the Human Fusiform Gyrus: fMRI Study
Wojciulik, E., Kanwisher, N., & Driver, J. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.3.1574 · Cited by 451 · see citing works
The brain response to personally familiar faces in autism: Findings of fusiform activity and beyond
Pierce, K. (2004) · Brain · doi:10.1093/brain/awh289 · Cited by 432 · see citing works
Puce, A. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.5.445 · Cited by 422 · see citing works
A Normed Study of Face Recognition in Autism and Related Disorders
Klin, A., Sparrow, S. S., de Bildt, A. A., Cicchetti, D. V., Cohen, D. J., & Volkmar, F. R. (1999) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1022299920240 · Cited by 408 · see citing works
How Does the Brain Process Upright and Inverted Faces?
Rossion, B., & Gauthier, L. (2002) · Behavioral and Cognitive Neuroscience Reviews · doi:10.1177/1534582302001001004 · Cited by 386 · see citing works
122-channel squid instrument for investigating the magnetic signals from the human brain
Ahonen, A., Hämäläinen, M., Kajola, M., Knuutila, J., Laine, P., Lounasmaa, O. V., Parkkonen, L. T., Simola, J., & Tesche, C. D. (1993) · Physica Scripta · doi:10.1088/0031-8949/1993/t49a/033 · Cited by 365 · see citing works
Halgren, E., Baudena, P., Heit, G., Clarke, M., & Marinković, K. (1994) · Journal of Physiology-Paris · doi:10.1016/0928-4257(94)90092-2 · Cited by 360 · see citing works
Activation of the fusiform gyrus when individuals with autism spectrum disorder view faces
Hadjikhani, N. K., Joseph, R. M., Snyder, J., Chabris, C. F., Clark, J., Steele, S. D., McGrath, L. M., Vangel, M. G., Aharon, I., Feczko, E., et al. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.03.025 · Cited by 350 · see citing works
Can Face Recognition Really be Dissociated from Object Recognition?
Gauthier, L., Behrmann, M., & Tarr, M. J. (1999) · Journal of Cognitive Neuroscience · doi:10.1162/089892999563472 · Cited by 319 · see citing works
THE AUTISTIC CHILD'S APPRAISAL OF EXPRESSIONS OF EMOTION: A FURTHER STUDY
Hobson, R. P. (1986) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1986.tb00191.x · Cited by 313 · see citing works
Courchesne, E., Townsend, J., & Saitoh, O. (1994) · Neurology · doi:10.1212/wnl.44.2.214 · Cited by 296 · see citing works
Verbal Bias in Recognition of Facial Emotions in Children with Asperger Syndrome
Grossman, J. B., Klin, A. J., Carter, A. S., & Volkmar, F. R. (2000) · Journal of Child Psychology and Psychiatry · doi:10.1111/1469-7610.00621 · Cited by 285 · see citing works
THE SALIENCE OF FACIAL EXPRESSION FOR AUTISTIC CHILDREN
Weeks, S. J., & Hobson, R. P. (1987) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1987.tb00658.x · Cited by 272 · see citing works
Clark, V. P., Keil, K., Maisog, J. M., Courtney, S. M., Ungerleider, L. G., & Haxby, J. V. (1996) · NeuroImage · doi:10.1006/nimg.1996.0025 · Cited by 234 · see citing works
Phillips, W., Baron‐Cohen, S., & Rutter, M. L. (1992) · Development and Psychopathology · doi:10.1017/s0954579400000845 · Cited by 209 · see citing works
Clinical and Macroscopic Correlates of Minicolumnar Pathology in Autism
Casanova, M. F., Buxhoeveden, D. P., & Brown, C. (2002) · Journal of Child Neurology · doi:10.1177/088307380201700908 · Cited by 190 · see citing works
B�tzel, K., & Gr�sser, O. J. (1989) · Experimental Brain Research · doi:10.1007/bf00274992 · Cited by 179 · see citing works
Hello and goodbye: a study of social engagement in autism
Hobson, R. P., & Lee, A. (1998) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1026088531558 · Cited by 174 · see citing works
Begleiter, H., Bernice Porjesz, A., & Wang, W. (1995) · Electroencephalography and Clinical Neurophysiology · doi:10.1016/0013-4694(94)00240-l · Cited by 174 · see citing works
Evidence for rapid face recognition from human scalp and intracranial electrodes
Seeck, M., Michel, C. M., Mainwaring, N. R., Cosgrove, R. G., Blume, H. W., Ives, J. R., Landis, T., & Schomer, D. L. (1997) · Neuroreport · doi:10.1097/00001756-199708180-00021 · Cited by 158 · see citing works
Face-specific responses from the human inferior occipito-temporal cortex
Sams, M. E., Hietanen, J. K., Hari, R., Ilmoniemi, R. J., & Lounasmaa, O. V. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00419-8 · Cited by 147 · see citing works
Eye contact does not facilitate detection in children with autism
Senju, A., Yaguchi, K., Tojo, Y., & Hasegawa, T. (2003) · Cognition · doi:10.1016/s0010-0277(03)00081-7 · Cited by 138 · see citing works
Campanella, S., Hanoteau, C., Dépy, D., Rossion, B., Bruyer, R., Crommelinck, M., & Guérit, J. M. (2000) · Psychophysiology · doi:10.1111/1469-8986.3760796 · Cited by 133 · see citing works
Face and shape repetition effects in humans
George, N., Jemel, B., Fiori, N., & Renault, B. (1997) · Neuroreport · doi:10.1097/00001756-199704140-00019 · Cited by 88 · see citing works
Neural processing of human faces: a magnetoencephalographic study
Swithenby, S., Bailey, A. J., Bräutigam, S., Josephs, O., Jousmäki, V., & Tesche, C. D. (1998) · Experimental Brain Research · doi:10.1007/s002210050306 · Cited by 65 · see citing works
Self-citationTask-dependent early latency (30???60 ms) visual processing of human faces and other objects
Braeutigam, S., Bailey, A. J., & Swithenby, S. (2001) · Neuroreport · doi:10.1097/00001756-200105250-00046 · Cited by 65 · see citing works
Self-citationMagnetoencephalographic evidence of early processing of direction of gaze in humans
Taylor, M. J., George, N., & Ducorps, A. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)02378-3 · Cited by 62 · see citing works
Wavelengths and energy levels of the 4d95s-4d95ptransition array of Xe IX
van Kampen, P., Hallin, R., Heijkenskjöld, F., Langereis, A., Larsson, M., NORDLING, C., Nyström, B., O’Sullivan, G., & Wännström, A. (1994) · Physica Scripta · doi:10.1088/0031-8949/49/2/010 · Cited by 53 · see citing works
Evoked potential evidence for human brain mechanisms that respond to single, fixated faces
Jeffreys, D. A., Tukmachi, E. S. A., & Rockley, G. (1992) · Experimental Brain Research · doi:10.1007/bf00231669 · Cited by 50 · see citing works
Shami, S. A., & Rasmuson, M. (1994) · Human Heredity · doi:10.1159/000154220 · Cited by 28 · see citing works
The role of the fusiform face area in social cognition ; implications for the pathology of autism
Schultz, R. T. (2003) · Medical Entomology and Zoology · Cited by 1 · see citing works
Activation of Broca's area by syntactic processing under conditions of concurrent articulation
Caplan, D., Alpert, N., Waters, G., & Olivieri, A. (2000) · Human Brain Mapping · doi:10.1002/(sici)1097-0193(200002)9:2
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Harms, M. B., Martin, A., & Wallace, G. L. (2010) · Neuropsychology Review · doi:10.1007/s11065-010-9138-6 · Cited by 1,028 · see citing works
Tager‐Flusberg, H., & Kasari, C. (2013) · Autism Research · doi:10.1002/aur.1329 · Cited by 985 · see citing works
Johnson, M. H. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1766 · Cited by 969 · see citing works
Vision in autism spectrum disorders
Simmons, D. R., Robertson, A. E., McKay, L. S., Toal, E., McAleer, P., & Pollick, F. E. (2009) · Vision Research · doi:10.1016/j.visres.2009.08.005 · Cited by 827 · see citing works
The eye contact effect: mechanisms and development
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Seeing it differently: visual processing in autism
BEHRMANN, M., THOMAS, C., & HUMPHREYS, K. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.05.001 · Cited by 469 · see citing works
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Senju, A., & Johnson, M. H. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.06.001 · Cited by 454 · see citing works
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Anderson, J. S., Druzgal, T. J., Froehlich, A., DuBray, M. B., Lange, N., Alexander, A. L., Abildskov, T., Nielsen, J. A., Cariello, A. N., Cooperrider, J. R., et al. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq190 · Cited by 438 · see citing works
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Khan, S., Gramfort, A., Shetty, N. R., Kitzbichler, M. G., Ganesan, S., Moran, J. M., Lee, S. M., Gabrieli, J. D. E., Tager-Flusberg, H. B., Joseph, R. M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1214533110 · Cited by 303 · see citing works
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Jemel, B., Mottron, L., & Dawson, M. (2006) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-005-0050-5 · Cited by 246 · see citing works
McCleery, J. P., Akshoomoff, N., Dobkins, K. R., & Carver, L. J. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.07.031 · Cited by 155 · see citing works
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Spencer, M. D., Holt, R. J., Chura, L. R., Suckling, J., Calder, A. J., Bullmore, E. T., & Baron-Cohen, S. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.18 · Cited by 92 · see citing works
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- Authors
- Bailey, A. J., Braeutigam, S., Jousmäki, V., & Swithenby, S. J.
- Affiliations
- University of London (GB)
- The Open University (GB)
- Corresponding author
- Bailey, Anthony J.
- Venue
- European Journal of Neuroscience
- Publisher
- Wiley
- Published
- 2005-05
- Volume
- 21
- Issue
- 9
- Pages
- 2575-2585
- ISSN
- 0953-816X (ISSN-L)
- 1460-9568
- OpenAlex
- W2041715523
- Cited by
- 86
- References
- 49
- Citations by year
- 2026: 1 · 2024: 3 · 2023: 4 · 2022: 1 · 2021: 2 · 2020: 3 · 2019: 1 · 2018: 5 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 4 · 2013: 7 · 2012: 5
- FWCI
- 3.79
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Open Research Online (The Open University) (submittedVersion)
- Funders
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- autism spectrum disorder, face processing, face perception, extrastriate cortex, right hemisphere lateralization, anterior temporal cortex, developmental psychopathology, face identification, magnetoencephalography
- MeSH terms
- Adult, Autistic Disorder, Evoked Potentials, Visual, Face, Female, Humans, Male, Middle Aged, Pattern Recognition, Visual, Photic Stimulation, Reaction Time, Magnetoencephalography
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