Abstract
Individuals with autism spectrum disorder (ASD) often have difficulty with social-emotional cues. This study examined the neural, behavioral, and autonomic correlates of emotional face processing in adolescents with ASD and typical development (TD) using eye-tracking and event-related potentials (ERPs) across two different paradigms. Scanning of faces was similar across groups in the first task, but the second task found that face-sensitive ERPs varied with emotional expressions only in TD. Further, ASD showed enhanced neural responding to non-social stimuli. In TD only, attention to eyes during eye-tracking related to faster face-sensitive ERPs in a separate task; in ASD, a significant positive association was found between autonomic activity and attention to mouths. Overall, ASD showed an atypical pattern of emotional face processing, with reduced neural differentiation between emotions and a reduced relationship between gaze behavior and neural processing of faces.
Similar content being viewed by others
References
Anderson, C. J., & Colombo, J. (2009). Larger tonic pupil size in young children with autism spectrum disorder. Developmental Psychobiology, 51, 207–211.
Ashwin, E., Ashwin, C., Rhydderch, D., Howells, J., & Baron-Cohen, S. (2009). Eagle-eyed visual acuity: An experimental investigation of enhanced perception in autism. Biological Psychiatry, 65, 17–21.
Ashwin, C., Chapman, E., Colle, L., & Baron-Cohen, S. (2006). Impaired recognition of negative basic emotions in autism: A test of the amygdala theory. Social Neuroscience, 1, 349–363.
Bal, E., Harden, E., Lamb, D., Vaughan Van Hecke, A., Denver, J. W., & Porges, S. W. (2010). Emotion recognition in children with autism spectrum disorders: Relations to eye gaze and autonomic state. Journal of Autism and Developmental Disorders, 40, 358–370.
Baron-Cohen, S., Wheelwright, S., & Jolliffe, T. (1997). Is there a “language of the eyes”? Evidence from normal adults, and adults with autism or Asperger Syndrome. Visual Cognition, 4, 311–331.
Batty, M., & Taylor, M. J. (2003). Early processing of the six basic facial emotional expressions. Cognitive Brain Research, 17, 613–620.
Bentin, S., Allison, T., Puce, A., Perez, E., & McCarthy, G. (1996). Electrophysiological studies of face perception in humans. Journal of Cognitive Neuroscience, 8, 551–565.
Berument, S., Rutter, M., Lord, C., Pickles, A., & Bailey, A. (1999). Autism screening questionnaire: Diagnostic validity. British Journal of Psychiatry, 175, 444–451.
Bradley, M. M., Miccoli, L., Escrig, M. A., & Lang, P. J. (2008). The pupil as a measure of emotional arousal and autonomic activation. Psychophysiology, 45, 602–607.
Cassia, V., Kuefner, D., Westerlund, A., & Nelson, C. (2006). A behavioural and ERP investigation of 3-month-olds’ face preferences. Neuropsychologia, 44, 2113–2125.
Celani, G., Battacchi, M. W., & Arcidiacono, L. (1999). The understanding of emotional meaning of facial expressions in people with autism. Journal of Autism and Developmental Disorders, 29, 57–66.
Critchley, H. D., Daly, E. M., Bullmore, E. T., Williams, S. C., Van Amelsvoort, T., Robertson, D. M., et al. (2000). The functional neuroanatomy of social behaviour: Changes in cerebral blood flow when people with autistic disorder process facial expressions. Brain: A. Journal of Neurology, 123, 2203–2212.
Dalton, K. M., Nacewicz, B. M., Alexander, A. L., & Davidson, R. J. (2007). Gaze-fixation, brain activation, and amygdala volume in unaffected siblings of individuals with autism. Biological Psychiatry, 61, 512–520.
Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., et al. (2005). Gaze-fixation and the neural circuity of face processing in autism. Nature Reviews Neuroscience, 8, 519–526.
Dawson, G., Carver, L., Meltzoff, A. N., Panagiotides, H., McPartland, J., & Webb, S. J. (2002). Neural correlates of face and object recognition in young children with autism spectrum disorder, developmental delay, and typical development. Child Development, 73, 700–717.
Dawson, G., Webb, S. J., Carver, L., Panagiotides, H., & McPartland, J. (2004). Young children with autism show atypical brain responses to fearful versus neutral facial expressions of emotion. Developmental Science, 7, 340–359.
de Wit, T. C., Falck-Ytter, T., & von Hofsten, C. (2008). Young children with autism spectrum disorder look differently at positive versus negative emotional faces. Research in Autism Spectrum Disorders, 2, 651–659.
Ekman, P., & Friesen, W. V. (1976). Pictures of facial affect. Palo Alto, CA: Consulting Psychologists Press.
Hall, G. B. C., Szechtman, H., & Nahmias, C. (2003). Enhanced salience and emotion recognition in autism: A PET study. American Journal of Psychiatry, 160, 1439–1441.
Heinze, H. J., Luck, S. J., Mangun, G. R., & Hillyard, S. A. (1990). Visual event-related potentials index focused attention within bilateral stimulus arrays, I: Evidence for early selection. Electroencephalography and Clinical Neurophysiology, 75, 511–527.
Hileman, C. M., Henderson, H., Mundy, P., Newell, L., & Mark, J. (2011). Developmental and individual differences on the P1 and N170 ERP components in children with and without autism. Developmental Neuropsychology, 36, 214–236.
Hirstein, W., Iverson, P., & Ramachandran, V. S. (2001). Autonomic responses of autistic children to people and objects. Proceedings of the Royal Society of London B, 268, 1883–1888.
Itier, R. J., & Batty, M. (2009). Neural bases of eye and gaze processing: The core of social cognition. Neuroscience and Biobehavioral Reviews, 33, 843–863.
Itier, R. J., & Taylor, M. J. (2002). Inversion and contrast polarity reversal affect both encoding and recognition processes of unfamiliar faces: A repetition study using ERPs. Neuroimage, 15, 353–372.
Itier, R. J., & Taylor, M. J. (2004). N170 or N1? Spatiotemporal differences between object and face processing using ERPs. Cerebral Cortex, 14, 132–142.
Jeste, S. S., & Nelson, C. A. (2009). Event related potentials in the understanding of autism spectrum disorders: An analytical review. Journal of Autism and Developmental Disorders, 39, 495–510.
Kanwisher, N., McDermott, J., & Chun, M. M. (1997). The fusiform face area: A module in human extra striate cortex specialized for face perception. Journal of Neuroscience, 17, 4302–4311.
Kaufman, A. S., & Kaufman, N. L. (2004). Kaufman Brief Intelligence Test (2nd ed.). Bloomington, MN: Pearson, Inc.
Kemner, C., van Ewijk, L., van Engeland, H., & Hooge, I. (2008). Brief report: Eye movements during visual search tasks indicate enhanced stimulus discriminability in subjects with PDD. Journal of Autism and Developmental Disorders, 38, 553–557.
Laeng, B., Sirois, S., & Gredeback, G. (2012). Pupillometry: A window to the preconscious? Perspectives on Psychological Science, 7, 18–27.
Leppanen, J. M., Moulson, M. C., Vogel-Farley, V. K., & Nelson, C. A. (2007). An ERP study of emotional face processing in the adult and infant brain. Child Development, 78, 232–245.
Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2002). Autism Diagnostic Observation Schedule: ADOS: Manual. Los Angeles, CA: Western Psychological Services.
Luck, S. J., Heinze, H. J., Mangun, G. R., & Hillyard, S. A. (1990). Visual event-related potentials index focused attention within bilateral stimulus arrays, II: Functional dissociation of P1 and N1 components. Electroencephalography and Clinical Neurophysiology, 75, 528–542.
Manjaly, Z. M., Bruning, N., Neufang, S., Stephan, K. E., Brieber, S., Marshall, J. C., et al. (2007). Neurophysiological correlates of relatively enhanced local visual search in autistic adolescents. Neuroimage, 35, 283–291.
McCleery, J. P., Askshoomoff, N., Dobkins, K. R., & Carver, L. J. (2009). Atypical face versus object processing and hemispheric asymmetries in 10-month-old infants at risk for autism. Biological Psychiatry, 66, 950–957.
McPartland, J., Dawson, G., Webb, S. J., Panagiotides, H., & Carver, L. J. (2004). Event related brain potentials reveal anomalies in temporal processing of faces in autism spectrum disorder. Journal of Child Psychology and Psychiatry, 45, 1235–1245.
McPartland, J. C., Webb, S. J., Keehn, B., & Dawson, G. (2011). Patterns of visual attention to faces and objects in autism spectrum disorder. Journal of Autism and Developmental Disorders, 41, 148–157.
Mottron, L., Dawson, M., & Soulieres, I. (2009). Enhanced perception in savant syndrome: Patterns, structure and creativity. Philosophical Transactions of the Royal Society B, 364, 1385–1391.
Nelson, C. A., & de Haan, M. (1996). Neural correlates of infants’ visual responsiveness to facial expressions of emotion. Developmental Psychobiology, 29, 577–595.
Nelson, C. A., & McCleery, J. P. (2008). Use of event-related potentials in the study of typical and atypical development. Journal of American Academy of Child and Adolescent Psychiatry, 47, 1252–1261.
Noland, J. S., Reznick, J. S., Stone, W. L., Walden, T., & Sheridan, E. H. (2010). Better working memory for non-social targets in infant siblings of children with Autism Spectrum Disorder. Developmental Science, 13, 244–251.
Ogai, M., Matsumoto, H., Suzuki, K., Ozawa, F., Fukudu, R., Uchiyama, I., et al. (2003). fMRI study of recognition of facial expressions in high-functioning autistic patients. NeuroReport, 14, 559–563.
Pelphrey, K. A., Sasson, N. J., Reznick, J., Paul, G., Goldman, B. D., & Piven, J. (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders, 32, 249–261.
Pierce, K., Muller, R. A., Ambrose, J., Allen, G., & Courchesne, E. (2001). Face processing occurs outside the fusiform ‘face area’ in autism: Evidence from functional MRI. Brain, 124, 2059–2073.
Porter, G., Troscianki, T., & Gilchrist, I. D. (2007). Effort during visual search and counting: Insights from pupillometry. Quarterly Journal of Experimental Psychology, 60, 211–229.
Rossignol, M., Philippot, P., Douilliez, C., Crommelinck, M., & Campanella, S. (2005). The perception of fearful and happy facial expression is modulated by anxiety: An event-related potential study. Neuroscience Letters, 377, 115–120.
Rossion, B., Delvenne, J. F., Debatisse, D., Goffaux, V., Bruyer, R., Crommelinck, M., et al. (1999). Spatio-temporal localization of the face inversion effect: An event related potentials study. Biological Psychology, 50, 173–189.
Rutherford, M. D., & Towns, A. M. (2008). Scan path differences and similarities during emotion perception in those with and without autism spectrum disorders. Journal of Autism and Developmental Disorders, 38, 1371–1381.
Sawyer, A. C. P., Williamson, P., & Young, R. L. (2012). Can gaze avoidance explain why individuals with Asperger’s syndrome can’t recognize emotions from facial expressions? Journal of Autism and Developmental Disorders, 42, 606–618.
Schoen, S. A., Miller, L. J., Brett-Green, B., & Hepburn, S. L. (2008). Psychophysiology of children with autism spectrum disorder. Research in Autism Spectrum Disorders, 2, 417–429.
Siegle, G. J., Steinhauer, S. R., Carter, C. S., Ramel, W., & Thase, M. E. (2003). Do the seconds turn into hours? Relationships between sustained pupil dilation in response to emotional information and self-reported rumination. Cognitive Therapy and Research, 27, 365–383.
Siegle, G. J., Steinhauer, S. R., & Thase, M. E. (2004). Pupillary assessment and computational modeling of the stroop task in depression. International Journal of Psychophysiology, 52, 63–76.
Soulieres, I., Dawson, M., Samson, F., Barbeau, E. B., Sahyoun, C., Strangman, G. E., et al. (2009). Enhanced visual processing contributes to matrix reasoning in autism. Human Brain Mapping, 30, 4082–4107.
Tottenham, N., Tanaka, J., Leon, A., McCarry, T., Nurse, M., Hare, T., et al. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168, 242–249.
Vaughn Van Hecke, A., Lebow, J., Bal, E., Lamb, D., Harden, E., Kramer, A., et al. (2009). Electroencephalogram and heart rate regulation to familiar and unfamiliar people in children with autism spectrum disorders. Child Development, 80, 1118–1133.
Webb, S. J., Dawson, G., Bernier, R., & Panagiotides, H. (2006). ERP evidence of atypical face processing in young children with autism. Journal of Autism and Developmental Disorders, 36, 881–890.
Webb, S. J., Jones, E. J. H., Merkle, K., Murias, M., Greenson, J., Richards, T., et al. (2010). Response to familiar faces, newly familiar faces, and novel faces as assessed by ERPs is intact in adults with autism spectrum disorders. International Journal of Psychophysiology, 77, 106–117.
Webb, S. J., Merkle, K., Murias, M., Richards, T., Aylward, E., & Dawson, G. (2009). ERP responses differentiate inverted but not upright face processing in adults with ASD. Social, Cognitive & Affective Neuroscience. doi:10.1093/scan/nsp002.
Wong, T. K. W., Fung, P. C. W., Chua, S. E., & McAlonan, G. M. (2008). Abnormal spatiotemporal processing of emotional facial expressions in childhood autism: Dipole source analysis of event-related potentials. European Journal of Neuroscience, 28, 407–416.
Acknowledgments
This research was made possible by a grant from the Autism Consortium for a multi-site, multi-modal study (in collaboration with Boston University, Massachusetts Institute of Technology, and Massachusetts General Hospital). We would like to thank our many collaborators across sites who contributed to study conception and design, including John Gabrieli, Robert Joseph, Nancy Kanwisher, Tal Kenet, Pawan Sinha, and Helen Tager-Flusberg. This work was conducted in accordance with the ethical standards of the APA and all the authors concur with the contents of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wagner, J.B., Hirsch, S.B., Vogel-Farley, V.K. et al. Eye-Tracking, Autonomic, and Electrophysiological Correlates of Emotional Face Processing in Adolescents with Autism Spectrum Disorder. J Autism Dev Disord 43, 188–199 (2013). https://doi.org/10.1007/s10803-012-1565-1
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-012-1565-1