Abstract
Despite evidence suggesting differences in early event-related potential (ERP) responses to social emotional stimuli, little is known about later stage ERP contributions to social emotional processing in individuals with autism spectrum disorder (ASD). Adults with and without ASD completed a facial emotion recognition task involving stimuli that varied by emotional intensity while electroencephalograms were recorded. Principal components analysis was used to examine P300 and late positive potential (LPP) modulation by emotional intensity. Results indicated that greater ASD symptomatology evinced heightened P300 to high relative to low intensity faces, then heightened LPP to low relative to high intensity faces. Findings suggest that adults with greater ASD symptomatology may demonstrate a lag in engagement in elaborative processing of low intensity faces.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders. Arlington. https://doi.org/10.1176/appi.books.9780890425596.744053.
Ashwin, C., Baron-Cohen, S., Wheelwright, S., O’Riordan, M., & Bullmore, E. T. (2007). Differential activation of the amygdala and the “social brain” during fearful face-processing in Asperger syndrome. Neuropsychologia,45(1), 2–14. https://doi.org/10.1016/j.neuropsychologia.2006.04.014.
Bal, E., Harden, E., Lamb, D., Van Hecke, A. V., 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(3), 358–370. https://doi.org/10.1007/s10803-009-0884-3.
Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & Clubley, E. (2001). The autism spectrum quotient: Evidence from Asperger syndrome/high functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders,31(1), 5–17. https://doi.org/10.1023/A:1005653411471.
Batty, M., Meaux, E., Wittemeyer, K., Rogé, B., & Taylor, M. J. (2011). Early processing of emotional faces in children with autism: An event-related potential study. Journal of Experimental Child Psychology,109(4), 430–444. https://doi.org/10.1016/j.jecp.2011.02.001.
Benning, S. D., Kovac, M., Campbell, A., Miller, S., Hanna, E. K., Damiano, C. R., et al. (2016). Late positive potential ERP responses to social and nonsocial stimuli in youth with autism spectrum disorder. Journal of Autism and Developmental Disorders,46(June), 3068–3077. https://doi.org/10.1007/s10803-016-2845-y.
Bishop, S. L., & Seltzer, M. M. (2012). Self-reported autism symptoms in adults with autism spectrum disorders. Journal of Autism and Developmental Disorders,42(11), 2354–2363. https://doi.org/10.1007/s10803-012-1483-2.
Blair, R. J. R., & Cipolotti, L. (2000). Impaired social response reversal: A case of “acquired sociopathy”. Brain,123(6), 1122–1141. https://doi.org/10.1093/brain/123.6.1122.
Blau, V. C., Maurer, U., Tottenham, N., & McCandliss, B. D. (2007). The face-specific N170 component is modulated by emotional facial expression. Behavioral and Brain Functions: BBF,3, 7. https://doi.org/10.1186/1744-9081-3-7.
Boraston, Z. L., Corden, B., Miles, L. K., Skuse, D. H., & Blakemore, S. J. (2008). Brief report: Perception of genuine and posed smiles by individuals with autism. Journal of Autism and Developmental Disorders,38(3), 574–580. https://doi.org/10.1007/s10803-007-0421-1.
Centers for Disease Control and Prevention. (2011). Autism spectrum disorder (ASD) data & statistics. Retrieved March 17, 2017 from https://www.cdc.gov/ncbddd/autism/data.html.
Cohen, S., Masyn, K., Mastergeorge, A., & Hessl, D. (2015). Psychophysiological responses to emotional stimuli in children and adolescents with autism and fragile × syndrome. Journal of Clinical Child & Adolescent Psychology,44(2), 250–263. https://doi.org/10.1080/15374416.2013.843462.Psychophysiological.
Cohen, J., & Polich, J. (1997). On the number of trials needed for P300. International Journal of Psychophysiology,25, 249–255.
Constantino, J. N. (2011). The quantitative nature of autistic social impairment. Pediatric Research,69(5), 1–17. https://doi.org/10.1203/PDR.0b013e318212ec6e.The.
Constantino, J. N., Gruber, C. P., Davis, S., Hayes, S., Passanante, N., & Przybeck, T. (2004). The factor structure of autistic traits. Journal of Child Psychology and Psychiatry,45(4), 719–726. https://doi.org/10.1111/j.1469-7610.2004.00266.x.
Corden, B., Chilvers, R., & Skuse, D. (2008). Avoidance of emotionally arousing stimuli predicts social-perceptual impairment in Asperger’s syndrome. Neuropsychologia,46(1), 137–147. https://doi.org/10.1016/j.neuropsychologia.2007.08.005.
Cui, T., Wang, P. P., Liu, S., & Zhang, X. (2017). P300 amplitude and latency in autism spectrum disorder: A meta-analysis. European Child and Adolescent Psychiatry,26(2), 177–190. https://doi.org/10.1007/s00787-016-0880-z.
Deeley, Q., Daly, E. M., Surguladze, S., Page, L., Toal, F., Robertson, D., et al. (2007). An event related functional magnetic resonance imaging study of facial emotion processing in Asperger syndrome. Biological Psychiatry,62(3), 207–217. https://doi.org/10.1016/j.biopsych.2006.09.037.
Donchin, E., & Coles, M. G. H. (1988). Is the P300 component a manifestation of context updating? Behavioral and Brain Sciences,11(03), 357. https://doi.org/10.1017/S0140525X00058027.
Eisenbarth, H., & Alpers, G. W. (2011). Happy mouth and sad eyes: Scanning emotional facial expressions. Emotion,11(4), 860–865. https://doi.org/10.1037/a0022758.
Ekman, P., Friesen, W. V., & Ellsworth, P. (2013). Emotion in the human face: Guidelines for research and an integration of findings. New York: Elsevier.
Faja, S., Dawson, G., Aylward, E., Wijsman, E. M., & Webb, J. (2016). Early event-related potentials to emotional faces differ for adults with autism spectrum disorder and by serotonin transporter genotype. Clinical Neurophysiology,127(6), 2436–2447. https://doi.org/10.1016/j.clinph.2016.02.022.Early.
Ferri, J., Weinberg, A., & Hajcak, G. (2012). I see people: The presence of human faces impacts the processing of complex emotional stimuli. Social Neuroscience,7(4), 436–443. https://doi.org/10.1080/17470919.2012.680492.
Foti, D., Hajcak, G., & Dien, J. (2009). Differentiating neural responses to emotional pictures: Evidence from temporal-spatial PCA. Psychophysiology,46(3), 521–530. https://doi.org/10.1111/j.1469-8986.2009.00796.x.
Gepner, B., Deruelle, C., & Grynfeltt, S. (2001). Motion and Emotion: A Novel Approach to the Study of Face Processing by Young Autistic Children. Journal of Autism and Developmental Disorders,31(1), 37–45. https://doi.org/10.1023/A:1005609629218.
Gratton, G., Coles, M. G. H., & Donchin, E. (1983). A new method for off-line removal of ocular artifact. Electroencephalography and Clinical Neurophysiology,55(4), 468–484.
Greimel, E., Schulte-Rüther, M., Kamp-Becker, I., Remschmidt, H., Herpertz-Dahlmann, B., & Konrad, K. (2014). Impairment in face processing in autism spectrum disorder: A developmental perspective. Journal of Neural Transmission,121(9), 1171–1181. https://doi.org/10.1007/s00702-014-1206-2.
Hajcak, G., Dunning, J. P., & Foti, D. (2009). Motivated and controlled attention to emotion: Time-course of the late positive potential. Clinical Neurophysiology,120(3), 505–510. https://doi.org/10.1016/j.clinph.2008.11.028.
Hanley, J. A., Negassa, A., deB Edwardes, M. D., & Forrester, J. E. (2003). Statistical analysis of correlated data using generalized estimating equations: An orientation. American Journal of Epidemiology,157(4), 364–375. https://doi.org/10.1093/aje/kwf215.
Harms, M. B., Martin, A., & Wallace, G. L. (2010). Facial emotion recognition in autism spectrum disorders: A review of behavioral and neuroimaging studies. Neuropsychology Review,20(3), 290–322. https://doi.org/10.1007/s11065-010-9138-6.
Hernandez, N., Metzger, A., Magné, R., Frederique, B.-B., Roux, S., Barthelemy, C., et al. (2009). Exploration of core features of a human face by healthy and autistic adults analyzed by visual scanning. Neuropsychologia,47(4), 1004–1012. https://doi.org/10.1016/j.neuropsychologia.2008.10.023.
Hileman, C. M., Henderson, H., Mundy, P., Newell, L., & Jaime, M. (2011). Developmental and individual differences on the P1 and N170 ERP components in children with and without autism. Developmental Neuropsychology,36(2), 214–236. https://doi.org/10.1080/87565641.2010.549870.
Hirstein, W., Iversen, P., & Ramachandran, V. S. (2001). Autonomic responses of autistic children to people and objects. Proceedings of the Royal Society B: Biological Sciences,268(1479), 1883–1888. https://doi.org/10.1098/rspb.2001.1724.
Hubert, B. E., Wicker, B., Monfardini, E., & Deruelle, C. (2009). Electrodermal reactivity to emotion processing in adults with autistic spectrum disorders. Autism,13(1), 9–19. https://doi.org/10.1177/1362361308091649.
Humphreys, K., Minshew, N., Leonard, G. L., & Behrmann, M. (2006). A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia,45(4), 685–695. https://doi.org/10.1016/j.neuropsychologia.2006.08.003.
Jemel, B., Mottron, L., & Dawson, M. (2006). Impaired face processing in autism: Fact or artifact? Journal of Autism and Developmental Disorders,36(1), 91–106. https://doi.org/10.1007/s10803-005-0050-5.
Kang, E., Keifer, C. M., Levy, E. J., Foss-Feig, J. H., McPartland, J. C., & Lerner, M. D. (2017). Atypicality of the N170 event-related potential in autism spectrum disorder: A meta-analysis. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging,59(1), 30–38.
Kaufman, A. S., & Kaufman, N. L. (2004). Kaufman brief intelligence test. New York: Wiley.
Keil, A., Bradley, M. M., Hauk, O., Rockstroh, B., Elbert, T., & Lang, P. J. (2002). Large-scale neural correlates of affective picture processing. Psychophysiology,39(5), 641–649.
Kirchner, J. C., Hatri, A., Heekeren, H. R., & Dziobek, I. (2011). Autistic symptomatology, face processing abilities, and eye fixation patterns. Journal of Autism and Developmental Disorders,41(2), 158–167. https://doi.org/10.1017/S0048577202394162.
Kleinhans, N. M., Johnson, L. C., Richards, T., Mahurin, R., Greenson, J., Dawson, G., et al. (2009). Reduced neural habituation in the amygdala and social impairments in autism spectrum disorders. American Journal of Psychiatry,166(4), 467–475. https://doi.org/10.1176/appi.ajp.2008.07101681.
Kohls, G., Chevallier, C., Troiani, V., & Schultz, R. T. (2012). Social “wanting” dysfunction in autism: Neurobiological underpinnings and treatment implications. Journal of Neurodevelopmental Disorders,4(1), 10. https://doi.org/10.1186/1866-1955-4-10.
Kujawa, A., Weinberg, A., Hajcak, G., & Klein, D. N. (2013). Differentiating event‐related potential components sensitive to emotion in middle childhood: Evidence from temporal–spatial PCA. Developmental Psychobiology,55(5), 539–550. https://doi.org/10.1086/498510.Parasitic. NIH Public Access.
Lerner, M. D., McPartland, J. C., & Morris, J. P. (2013). Multimodal emotion processing in autism spectrum disorders: An event-related potential study. Developmental Cognitive Neuroscience,3(1), 11–21. https://doi.org/10.1016/j.dcn.2012.08.005.
Little, L. (2002). Middle-class mothers’ perceptions of peer and sibling victimization among children with Asperger’s syndrome and nonverbal learning disorders. Issues in Comprehensive Pediatric Nursing,25, 43–57. https://doi.org/10.1097/00005721-200211000-00010.
Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2012). Autism diagnostic observation schedule-second edition (ADOS-2). Los Angeles, CA: Western Psychological Services.
Lozier, L. M., VanMeter, J. W., & Marsh, A. A. (2014). Impairments in facial affect recognition associated with autism spectrum disorders: A meta-analysis. Development and Psychopathology,26(4), 1–13. https://doi.org/10.1017/S0954579414000479.
Luckhardt, C., Kröger, A., Cholemkery, H., Bender, S., & Freitag, C. M. (2017). Neural correlates of explicit versus implicit facial emotion processing in ASD. Journal of Autism and Developmental Disorders,47(7), 1944–1955. https://doi.org/10.1007/s10803-017-3141-1.
Ming, X., Julu, P. O. O., Brimacombe, M., Connor, S., & Daniels, M. L. (2005). Reduced cardiac parasympathetic activity in children with autism. Brain and Development,27(7), 509–516. https://doi.org/10.1016/j.braindev.2005.01.003.
Mini, A., Palomba, D., Angrilli, A., & Bravi, S. (1996). Emotional information processing and visual evoked brain potentials. Perceptual and Motor Skills,83(1), 143–152. https://doi.org/10.2466/pms.1996.83.1.143.
Moran, T. P., Jendrusina, A. A., & Moser, J. S. (2013). The psychometric properties of the late positive potential during emotion processing and regulation. Brain Research,1516(April), 66–75. https://doi.org/10.1016/j.brainres.2013.04.018.
Neumann, D., Spezio, M. L., Piven, J., & Adolphs, R. (2006). Looking you in the mouth: Abnormal gaze in autism resulting from impaired top-down modulation of visual attention. Social Cognitive and Affective Neuroscience,1(3), 194–202. https://doi.org/10.1093/scan/nsl030.
Nowicki, S. (2004). Manual for the receptive tests of the diagnostic analysis of nonverbal accuracy (Vol. 2). Atlanta, GA: Emory University.
O’Connor, K., Hamm, J. P., & Kirk, I. J. (2005). The neurophysiological correlates of face processing in adults and children with Asperger’s syndrome. Brain and Cognition,59(1), 82–95. https://doi.org/10.1016/j.bandc.2005.05.004.
Pelphrey, K. A., Sasson, N. J., Reznick, J. S., Paul, G., Goldman, B. D., & Piven, J. (2002). Visual scanning of faces in autism. Journal of Autism and Developmental Disorders,32(4), 249–261.
Rhodes, M. G., & Anastasi, J. S. (2012). The own-age bias in face recognition: A meta-analytic and theoretical review. Psychological Bulletin,138(1), 146–174. https://doi.org/10.1037/a0025750.
Riby, D. M., Whittle, L., & Doherty-Sneddon, G. (2012). Physiological reactivity to faces via live and video-mediated communication in typical and atypical development. Journal of Clinical and Experimental Neuropsychology,34(4), 385–395. https://doi.org/10.1080/13803395.2011.645019.
Robinson, E., Munir, K., Munafò, M. R., Hughes, M., Mccormick, M., & Koenen, K. C. (2011). The stability of autistic traits in the general population: Further evidence for a continuum of impairment. Journal of the American Academy of Child and Adolescent Psychiatry,50(4), 376–384. https://doi.org/10.1016/j.jaac.2011.01.005.The.
Rump, K. M., Giovannelli, J. L., Minshew, N. J., & Strauss, M. S. (2009). The development of emotion recognition in individuals with autism. Child Development,80(5), 1434–1447. https://doi.org/10.1111/j.1467-8624.2009.01343.x.The.
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(7), 1371–1381. https://doi.org/10.1007/s10803-007-0525-7.
Simonoff, E., Pickles, A., Charman, T., Chandler, S., Loucas, T., & Baird, G. (2008). Psychiatric disorders in children with autism spectrum disorders: Prevalence, comorbidity, and associated factors in a population-derived sample. Journal of the American Academy of Child and Adolescent Psychiatry,47(8), 921–929. https://doi.org/10.1097/CHI.0b013e318179964f.
Spezio, M. L., Adolphs, R., Hurley, R. S. E., & Piven, J. (2007). Abnormal use of facial information in high-functioning autism. Journal of Autism and Developmental Disorders,37(5), 929–939. https://doi.org/10.1007/s10803-006-0232-9.
Steiger, J. H. (1980). Tests for comparing elements of a correlation matrix. Psychological Bulletin,87(2), 245–251.
Trevisan, D. A., & Birmingham, E. (2016). Are emotion recognition abilities related to everyday social functioning in ASD? A meta-analysis. Research in Autism Spectrum Disorders,32, 24–42. https://doi.org/10.1016/j.rasd.2016.08.004.
Tye, C., Battaglia, M., Bertoletti, E., Ashwood, K. L., Azadi, B., Asherson, P., et al. (2014). Altered neurophysiological responses to emotional faces discriminate children with ASD, ADHD and ASD + ADHD. Biological Psychology,103, 125–134. https://doi.org/10.1016/j.biopsycho.2014.08.013.
Uljarevic, M., & Hamilton, A. (2013). Recognition of emotions in autism: A formal meta-analysis. Journal of Autism and Developmental Disorders,43(7), 1517–1526. https://doi.org/10.1007/s10803-012-1695-5.
Van Roekel, E., Scholte, R. H. J., & Didden, R. (2010). Bullying among adolescents with autism spectrum disorders: Prevalence and perception. Journal of Autism and Developmental Disorders,40(1), 63–73. https://doi.org/10.1007/s10803-009-0832-2.
Van Strien, J. W., De Sonneville, L. M. J., & Franken, I. H. A. (2010). The late positive potential and explicit versus implicit processing of facial valence. NeuroReport,21(9), 656–661. https://doi.org/10.1097/WNR.0b013e32833ab89e.
Webb, S. J., Merkle, K., Murias, M., Richards, T., Aylward, E., & Dawson, G. (2012). ERP responses differentiate inverted but not upright face processing in adults with ASD. Social Cognitive and Affective Neuroscience,7(5), 578–587. https://doi.org/10.1093/scan/nsp002.
Webb, S. J., Neuhaus, E., & Faja, S. (2017). Face perception and learning in autism spectrum disorders. The Quarterly Journal of Experimental Psychology,70(5), 970–986. https://doi.org/10.1080/17470218.2016.1151059.
Wheatley, T., Weinberg, A., Looser, C., Moran, T., & Hajcak, G. (2011). Mind perception: Real but not artificial faces sustain neural activity beyond the N170/VPP. PLoS ONE,6(3), 1–7. https://doi.org/10.1371/journal.pone.0017960.
Woodbury-Smith, M. R., Robinson, J., Wheelwright, S., & Baron-Cohen, S. (2005). Screening adults for Asperger syndrome using the AQ: A preliminary study of its diagnostic validity in clinical practice. Journal of Autism and Developmental Disorders,35(3), 331–335. https://doi.org/10.1007/s10803-005-3300-7.
Acknowledgments
This work was supported by the Alan Alda Fund for Communication.
Funding
This study was funded by the Alan Alda Fund for Communication.
Author information
Authors and Affiliations
Contributions
Author Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by all authors. All authors read and approved the final manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
Cara Keifer, Kathryn Hauschild, Brady Nelson, Greg Hajcak, and Matthew Lerner declare that they have no conflicts of interest.
Ethical Approval
All procedures performed in the studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.
Informed Consent
Informed consent was obtained from all individual participants included in this study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Keifer, C.M., Hauschild, K.M., Nelson, B.D. et al. Differences in the Late Positive Potential and P300 to Emotional Faces in Individuals with Autism Spectrum Disorder. J Autism Dev Disord 49, 5009–5022 (2019). https://doi.org/10.1007/s10803-019-04207-6
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10803-019-04207-6