Emotional attribution in high-functioning individuals with autistic spectrum disorder: A functional imaging study
Abstract
Objective To determine whether expertise in the attribution of emotion from basic facial expressions in high-functioning individuals with autistic spectrum disorder (ASD) is supported by the amygdala, fusiform, and prefrontal regions of interest (ROI) and is comparable to that of typically developing individuals.Method Functional magnetic resonance imaging scans were acquired from 14 males with ASD and 10 matched adolescent controls while performing emotion match (EM) (perceptual), emotion label (EL) (linguistic), and control tasks. Accuracy, response time, and average activation were measured for each ROI.Results There was no significant difference in accuracy, response time, or ROI activation between groups performing the EL task. The ASD group was as accurate as the control group performing the EM task but had a significantly longer response time and lower average fusiform activation.Conclusions Expertise in the attribution of emotion from basic facial expressions was task-dependent in the high-functioning ASD group. The hypothesis that the high-functioning ASD group would be less expert and would have reduced fusiform activation was supported in the perceptual task but not the linguistic task. The reduced fusiform activation in the perceptual task was not explained by reduced expertise; it is therefore concluded that reduced fusiform activation is associated with the diagnosis of ASD.
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Three studies, those of Ogai et al. (2003), Pierce et al. (2004) and Piggot et al. (2004), failed to find any significant differences in amygdala activation for the ASD samples compared to controls.
“However, three studies, those of Ogai et al. (2003), Pierce et al. (2004) and Piggot et al. (2004), failed to find any significant differences in amygdala activation for the ASD samples compared to controls.”
From Vision in autism spectrum disorders (2009) · cites this paper as Piggot et al. (2004)
Cites
The assessment and analysis of handedness: The Edinburgh inventory
Oldfield, R. C. (1971) · Neuropsychologia · doi:10.1016/0028-3932(71)90067-4 · Cited by 35,900 · see citing works
Lord, C., Rutter, M., & Le Couteur, A. (1994) · Journal of Autism and Developmental Disorders · doi:10.1007/bf02172145 · Cited by 9,065 · see citing works
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
Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Leventhal, B. L., DiLavore, P. C., Pickles, A., & Rutter, M. (2000) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1005592401947 · Cited by 7,520 · see citing works
Frith, C., & Frith, U. (2005) · Current Biology · doi:10.1016/j.cub.2005.08.041 · Cited by 3,494 · see citing works
Baron‐Cohen, S., Jolliffe, T., Mortimore, C., & Robertson, M. (1997) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1997.tb01599.x · Cited by 1,970 · see citing works
The neurobiology of social cognition
Adolphs, R. (2001) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00202-6 · Cited by 1,432 · see citing works
Expertise for cars and birds recruits brain areas involved in face recognition
Gauthier, I., Skudlarski, P., Gore, J. C., & Anderson, A. W. (2000) · Nature Neuroscience · doi:10.1038/72140 · Cited by 1,418 · cited 1× · see citing works
“The FA, often termed the fusiform “face” area, is considered a key area for processing faces and other visual percepts for which there is expertise (Gauthier et al., 2000).”
BackgroundLesions of the human amygdala impair enhanced perception of emotionally salient events
Anderson, A. K., & Phelps, E. A. (2001) · Nature · doi:10.1038/35077083 · Cited by 1,335 · see citing works
Social intelligence in the normal and autistic brain: An fMRI study
Baron‐Cohen, S., Ring, H. A., Wheelwright, S., Bullmore, E. T., Brammer, M. J., Simmons, A., & Williams, S. C. R. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00621.x · Cited by 1,320 · see citing works
Early recognition of children with autism: a study of first birthday home videotapes
Osterling, J., & Dawson, G. (1994) · Journal of Autism and Developmental Disorders · doi:10.1007/bf02172225 · Cited by 1,290 · see citing works
Modulating emotional responses: effects of a neocortical network on the limbic system
Hariri, A. R., Bookheimer, S. Y., & Mazziotta, J. C. (2000) · NeuroReport · doi:10.1097/00001756-200001170-00009 · Cited by 1,277 · see citing works
Self-citationBaron-Cohen, S., Ring, H. A., Bullmore, E. T., Wheelwright, S., Ashwin, C., & Williams, S. C. R. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00011-7 · Cited by 1,130 · see citing works
Face-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
The human amygdala in social judgment
Adolphs, R., Tranel, D., & Damasio, A. R. (1998) · Nature · doi:10.1038/30982 · Cited by 1,125 · see citing works
Children with Autism Fail to Orient to Naturally Occurring Social Stimuli
Dawson, G., Meltzoff, A. N., Osterling, J., Rinaldi, J., & Brown, E. (1998) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1026043926488 · Cited by 1,065 · see citing works
Social Intelligence in the Normal and Autistic Brain: An fMRI Study
Baron‐Cohen, S., RING, H. A., Wheelwright, S. J., Bullmore, E. T., Brammer, M. J., Simmons, A., & Williams, S. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3077.003.0028 · Cited by 1,044 · 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
Puce, A., Allison, T., Asgari, M., Gore, J. C., & McCarthy, G. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-16-05205.1996 · Cited by 987 · cited 2× · see citing works
“In typically developing individuals, the fusiform area (FA) has been associated with the perceptual processing of faces (Clark et al., 1996; Kanwisher et al., 1997; McCarthy et al., 1997; Puce et al., 1996; Tarr and Gauthier, 2000) and with the attribution of emotion from basic facial expressions (Critchley et al.”
BackgroundFace 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
The Human Amygdala in Social Judgment
Adolphs, R., Tranel, D., & Damásio, A. R. (2002) · The MIT Press eBooks · doi:10.7551/mitpress/3077.003.0027 · Cited by 882 · see citing works
The functional neuroanatomy of social behaviour
Critchley, H. D., Daly, E. M., Bullmore, E. T., Williams, S. C. R., Van Amelsvoort, T., Robertson, D. M., Rowe, A., Phillips, M., McAlonan, G., Howlin, P., et al. (2000) · Brain · doi:10.1093/brain/123.11.2203 · Cited by 816 · see citing works
The frontal lobes are necessary for `theory of mind'
Stuss, D. T. (2001) · Brain · doi:10.1093/brain/124.2.279 · Cited by 660 · see citing works
FFA: a flexible fusiform area for subordinate-level visual processing automatized by expertise
Tarr, M. J., & Gauthier, L. (2000) · Nature Neuroscience · doi:10.1038/77666 · Cited by 645 · 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
‘Theory of mind’ in the brain. Evidence from a PET scan study of Asperger syndrome
Happe, F. G. E., Ehlers, S., Fletcher, P. C., Uta Frith, A., Johansson, M., Gillberg, C., Dolan, R. J., Frackowiak, R. S. J., & Frith, C. (1996) · Neuroreport · doi:10.1097/00001756-199612200-00040 · Cited by 577 · see citing works
A Developmental fMRI Study of the Stroop Color-Word Task
Adleman, N. E., Menon, V., Blasey, C. M., White, C. D., Warsofsky, I. S., Glover, G. H., & Reiss, A. L. (2002) · NeuroImage · doi:10.1006/nimg.2001.1046 · Cited by 569 · see citing works
Self-citationValenza, E., Simion, F., Cassia, V. M., & Umiltà, C. A. (1996) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037//0096-1523.22.4.892 · Cited by 538 · see citing works
Self‐navigated spiral fMRI: Interleaved versus single‐shot
Glover, G. H., & Lai, S. (1998) · Magnetic Resonance in Medicine · doi:10.1002/mrm.1910390305 · Cited by 476 · see citing works
Amygdala response to facial expressions in children and adults.
Thomas, K. M., Drevets, W. C., Whalen, P. J., Eccard, C. H., Dahl, R. E., Ryan, N. D., & Casey, B. J. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(00)01066-0 · Cited by 470 · see citing works
Defining and quantifying the social phenotype in autism
Klin, A., Jones, W., Schultz, R., Volkmar, F., & Cohen, D. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.6.895 · Cited by 467 · see citing works
Recognition of Mental State Terms
Baron‐Cohen, S., RING, H. A., Moriarty, J., Schmitz, B., Costa, D. C., & Ell, P. J. (1994) · The British Journal of Psychiatry · doi:10.1192/bjp.165.5.640 · Cited by 441 · see citing works
Grelotti, D. J., Gauthier, L., & Schultz, R. T. (2002) · Developmental Psychobiology · doi:10.1002/dev.10028 · Cited by 386 · see citing works
Are there Emotion Perception Deficits in Young Autistic Children?
Ozonoff, S. J., Pennington, B. F., & Rogers, S. J. (1990) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1990.tb01574.x · Cited by 335 · see citing works
Valenza, E., Simion, F., Cassia, V. M., et al. (1996) · Journal of Experimental Psychology Human Perception & Performance · doi:10.1037/0096-1523.22.4.892 · Cited by 324 · see citing works
The Recognition of Facial Expressions in the First Two Years of Life: Mechanisms of Development
Nelson, C. A. (1987) · Child Development · doi:10.2307/1130530 · Cited by 306 · 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
Recognition and Expression of Emotional Cues by Autistic and Normal Adults
Macdonald, H., Rutter, M. L., Howlin, P., Rios, P., Conteur, A. L., Evered, C., & Folstein, S. E. (1989) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1989.tb00288.x · Cited by 253 · see citing works
Autistic Children's Knowledge of Thinking and Feeling States in Other People
Prior, M. R., Dahlstrom, B., & Squires, T. (1990) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.1990.tb00799.x · Cited by 249 · see citing works
Increased social fear and decreased fear of objects in monkeys with neonatal amygdala lesions
Prather, M. D., Lavenex, P., Mauldin-Jourdain, M. L., Mason, W. A., Capitanio, J. P., Mendoza, S. P., & Amaral, D. G. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00445-6 · Cited by 248 · 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
Do children with autism recognise surprise? A research note
Baron‐Cohen, S., Spitz, A., & Cross, P. (1993) · Cognition & Emotion · doi:10.1080/02699939308409202 · Cited by 208 · see citing works
The Awkward Moments Test: A Naturalistic Measure of Social Understanding in Autism
Heavey, L., Phillips, W., Baron-Cohen, S., & Rutter, M. (2000) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1005544518785 · Cited by 207 · see citing works
Affect comprehension in children with pervasive developmental disorders
Braverman, M., Fein, D., Lucci, D., & Waterhouse, L. (1989) · Journal of Autism and Developmental Disorders · doi:10.1007/bf02211848 · Cited by 183 · see citing works
Brain Activations in Schizophrenia During a Graded Memory Task Studied With Functional Neuroimaging
Fletcher, P. C., McKenna, P. J., Frith, C., Grasby, P. M., Friston, K. J., & Dolan, R. J. (1998) · Archives of General Psychiatry · doi:10.1001/archpsyc.55.11.1001 · Cited by 172 · see citing works
Advanced Theory of Mind in High-Functioning Adults with Autism
Kleinman, J. M., Marciano, P. L., & Ault, R. L. (2001) · Journal of Autism and Developmental Disorders · doi:10.1023/a:1005657512379 · Cited by 157 · see citing works
Hamann, S. B., Stefanacci, L., Squire, L. R., Adolphs, R., Tranel, D., Damásio, H., & Damásio, A. R. (1996) · Nature · doi:10.1038/379497a0 · Cited by 149 · see citing works
McCusker, T. (1993) · Datamation · Cited by 121 · see citing works
`Theory of mind' and the prefrontal cortex
Shallice, T. (2001) · Brain · doi:10.1093/brain/124.2.247 · Cited by 88 · see citing works
Xiong (1999) · doi:10.1002/(sici)1097-0193(1999)8:2/3
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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Schultz, R. T. (2005) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.12.012 · Cited by 1,071 · see citing works
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
Cui, X., Bryant, D. M., & Reiss, A. L. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.09.003 · Cited by 807 · see citing works
Self-citationVision 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
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Assaf, M., Jagannathan, K., Calhoun, V. D., Miller, L., Stevens, M. C., Sahl, R., O'Boyle, J. G., Schultz, R. T., & Pearlson, G. D. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.05.067 · Cited by 680 · see citing works
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Varghese, M., Keshav, N., Jacot-Descombes, S., Warda, T., Wicinski, B., Dickstein, D. L., Harony-Nicolas, H., De Rubeis, S., Drapeau, E., Buxbaum, J. D., et al. (2017) · Acta Neuropathologica · doi:10.1007/s00401-017-1736-4 · Cited by 536 · see citing works
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Kleinhans, N. M., Richards, T., Sterling, L., Stegbauer, K. C., Mahurin, R., Johnson, L. C., Greenson, J., Dawson, G., & Aylward, E. (2008) · Brain · doi:10.1093/brain/awm334 · Cited by 498 · see citing works
Koshino, H., Kana, R. K., Keller, T. A., Cherkassky, V. L., Minshew, N. J., & Just, M. A. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm054 · Cited by 436 · see citing works
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Grelotti, D. J., Klin, A. J., Gauthier, I., Skudlarski, P., Cohen, D. J., Gore, J. C., Volkmar, F. R., & Schultz, R. T. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.06.015 · Cited by 254 · see citing works
White, S. W., Mazefsky, C. A., Dichter, G. S., Chiu, P. H., Richey, J. A., & Ollendick, T. H. (2014) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2014.05.012 · Cited by 252 · see citing works
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Wang, A. T., Lee, S. S., Sigman, M., & Dapretto, M. (2007) · Archives of General Psychiatry · doi:10.1001/archpsyc.64.6.698 · Cited by 227 · see citing works
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- Authors
- Piggot, J., Kwon, H., Mobbs, D., Blasey, C., Lotspeich, L., Menon, V., Bookheimer, S., & Reiss, A. L.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Piggot, Judith
- Venue
- Journal of the American Academy of Child & Adolescent Psychiatry
- Publisher
- Elsevier BV
- Published
- 2004-04
- Volume
- 43
- Issue
- 4
- Pages
- 473-480
- ISSN
- 0890-8567 (ISSN-L)
- OpenAlex
- W2064755515
- Cited by
- 201
- References
- 52
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 4 · 2023: 2 · 2022: 7 · 2021: 12 · 2020: 4 · 2019: 7 · 2018: 6 · 2017: 11 · 2016: 6 · 2015: 12 · 2014: 19 · 2013: 18 · 2012: 12
- FWCI
- 4.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of the American Academy of Child & Adolescent Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion)
- Funders
- NIH (MH01142, MH50047, HD31715, MH64708)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Keywords
- autism spectrum disorder, high-functioning autism, facial emotion recognition, emotional attribution, fusiform gyrus, amygdala, prefrontal cortex, emotion perception, emotion labeling, reaction time (psychology)
- MeSH terms
- Adolescent, Amygdala, Analysis of Variance, Autistic Disorder, Cerebral Cortex, Child, Emotions, Facial Expression, Humans, Magnetic Resonance Imaging, Male, Psycholinguistics, Social Perception, Case-Control Studies
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