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Impaired Recognition of Negative Facial Expressions is Partly Related to Facial Perception Deficits in Adolescents with High-Functioning Autism Spectrum Disorder

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Abstract

Accumulating studies have reported facial emotion recognition or facial perception impairments in autism spectrum disorder (ASD). To clarify the specificity of the emotion recognition impairment, this study examined the relationships between facial emotion recognition and facial perception abilities in ASD. Twenty-two adolescents with high-functioning ASD (20 males) and 22 typically developing (TD) adolescents (16 males) aged 11–18 years undertook a facial emotion labeling task and a facial perception test. We found that adolescents with ASD had deficits in recognizing negative facial expressions, which correlated with both facial perception deficits and severity of social impairment. In addition, the emotion recognition deficits remained after adjusting for facial perception performance. Thus, our findings suggest an emotion-specific impairment in facial emotion recognition in ASD.

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References

  • Adolphs, R. (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12(2), 169–177.

    PubMed  Google Scholar 

  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington: American Psychiatric Publishing.

    Google Scholar 

  • Annaz, D., Karmiloff-Smith, A., Johnson, M. H., & Thomas, M. S. (2009). A cross-syndrome study of the development of holistic face recognition in children with autism, Down syndrome, and Williams syndrome. Journal of Experimental Child Psychology, 102(4), 456–486.

    PubMed  Google Scholar 

  • 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(3–4), 349–363.

    PubMed  Google Scholar 

  • Bachevalier, J., & Loveland, K. A. (2006). The orbitofrontal–amygdala circuit and self-regulation of social–emotional behavior in autism. Neuroscience & Biobehavioral Reviews, 30(1), 97–117.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Batty, M., & Taylor, M. J. (2003). Early processing of the six basic facial emotional expressions. Cognitive Brain Research, 17(3), 613–620.

    PubMed  Google Scholar 

  • Benton, A. L., Sivan, A. B., Hamsher, K., Varney, N. R., & Spreen, O. (1994). Contributions to neuropsychological assessment: A clinical manual (2nd ed.). New York: Oxford University Press.

    Google Scholar 

  • Calvo, M. G., & Lundqvist, D. (2008). Facial expressions of emotion (KDEF): Identification under different display-duration conditions. Behavior Research Methods, 40(1), 109–115.

    Google Scholar 

  • Cohen, J. (1973). Eta-squared and partial eta-squared in fixed factor ANOVA designs. Educational and Psychological Measurement, 33(1), 107–112.

    Google Scholar 

  • Cohen J. (1988). Statistical power analysis for the behavioral sciences. New York, NY: Routledge Academic.

    Google Scholar 

  • Constantino, J. N., & Gruber, C. P. (2012). Social responsiveness scale (SRS). Torrance: Western Psychological Services.

    Google Scholar 

  • Dawson, G., Toth, K., Abbott, R., Osterling, J., Munson, J., Estes, A., & Liaw, J. (2004). Early social attention impairments in autism: social orienting, joint attention, and attention to distress. Developmental Psychology, 40(2), 271–283.

    PubMed  Google Scholar 

  • Eack, S. M., Mazefsky, C. A., & Minshew, N. J. (2015). Misinterpretation of facial expressions of emotion in verbal adults with autism spectrum disorder. Autism, 19(3), 308–315.

    PubMed  Google Scholar 

  • Ekman, P. (1992). An argument for basic emotions. Cognition & Emotion, 6(3–4), 169–200.

    Google Scholar 

  • Enticott, P. G., Kennedy, H. A., Johnston, P. J., Rinehart, N. J., Tonge, B. J., Taffe, J. R., & Fitzgerald, P. B. (2014). Emotion recognition of static and dynamic faces in autism spectrum disorder. Cognition and Emotion, 28(6), 1110–1118.

    PubMed  Google Scholar 

  • Falkmer, T., Anderson, K., Falkmer, M., & Horlin, C. (2013). Diagnostic procedures in autism spectrum disorders: A systematic literature review. European Child & Adolescent Psychiatry, 22(6), 329–340.

    Google Scholar 

  • Fein, D., Barton, M., Eigsti, I. M., Kelley, E., Naigles, L., Schultz, R. T., … Troyb, E. (2013). Optimal outcome in individuals with a history of autism. Journal of Child Psychology and Psychiatry, 54(2), 195–205.

    PubMed  Google Scholar 

  • Garman, H. D., Spaulding, C. J., Webb, S. J., Mikami, A. Y., Morris, J. P., & Lerner, M. D. (2016). Wanting it too much: An inverse relation between social motivation and facial emotion recognition in autism spectrum disorder. Child Psychiatry & Human Development, 47(6), 890–902.

    Google Scholar 

  • Goeleven, E., De Raedt, R., Leyman, L., & Verschuere, B. (2008). The Karolinska directed emotional faces: A validation study. Cognition and Emotion, 22(6), 1094–1118.

    Google Scholar 

  • Griffiths, S., Jarrold, C., Penton-Voak, I. S., Woods, A. T., Skinner, A. L., & Munafò, M. R. (2017). Impaired recognition of basic emotions from facial expressions in young people with autism spectrum disorder: Assessing the importance of expression intensity. Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s10803-017-3091-7.

    Article  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Hooker, C., & Park, S. (2002). Emotion processing and its relationship to social functioning in schizophrenia patients. Psychiatry Research, 112(1), 41–50.

    PubMed  Google Scholar 

  • Humphreys, K., Minshew, N., Leonard, G. L., & Behrmann, M. (2007). A fine-grained analysis of facial expression processing in high-functioning adults with autism. Neuropsychologia, 45(4), 685–695.

    PubMed  Google Scholar 

  • Izard, C., Fine, S., Schultz, D., Mostow, A., Ackerman, B., & Youngstrom, E. (2001). Emotion knowledge as a predictor of social behavior and academic competence in children at risk. Psychological Science, 12(1), 18–23.

    PubMed  Google Scholar 

  • Jones, C. R., Pickles, A., Falcaro, M., Marsden, A. J., Happé, F., Scott, S. K., … Simonoff, E. (2011). A multimodal approach to emotion recognition ability in autism spectrum disorders. Journal of Child Psychology and Psychiatry, 52(3), 275–285.

    PubMed  Google Scholar 

  • Just, M. A., Keller, T. A., Malave, V. L., Kana, R. K., & Varma, S. (2012). Autism as a neural systems disorder: A theory of frontal-posterior underconnectivity. Neuroscience & Biobehavioral Reviews, 36(4), 1292–1313.

    Google Scholar 

  • Kennedy, D. P., & Adolphs, R. (2012). Perception of emotions from facial expressions in high-functioning adults with autism. Neuropsychologia, 50(14), 3313–3319.

    PubMed  PubMed Central  Google Scholar 

  • Keppel G. (1991). Design and analysis: A researcher’s handbook. Englewood Cliffs, NJ: Prentice Hall.

    Google Scholar 

  • Kuusikko, S., Haapsamo, H., Jansson-Verkasalo, E., Hurtig, T., Mattila, M. L., Ebeling, H., … Moilanen, I. (2009). Emotion recognition in children and adolescents with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39(6), 938–945.

    PubMed  Google Scholar 

  • Lord, C., Rutter, M., & Le Couteur, A. (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(5), 659–685.

    PubMed  Google Scholar 

  • Lundqvist, D., Flykt, A., & Öhman, A. (1998). The Karolinska directed emotional faces (KDEF). CD ROM from Department of Clinical Neuroscience, Psychology section, Karolinska Institutet, ISBN 91-630-7164-9.

  • Mandal, M. K., Tandon, S. C., & Asthana, H. S. (1991). Right brain damage impairs recognition of negative emotions. Cortex, 27(2), 247–253.

    PubMed  Google Scholar 

  • 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(2), 148–157.

    PubMed  PubMed Central  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Picci, G., & Scherf, K. S. (2016). From caregivers to peers: Puberty shapes human face perception. Psychological Science, 27(11), 1461–1473

    Google Scholar 

  • Philip, R. C. M., Whalley, H. C., Stanfield, A. C., Sprengelmeyer, R., Santos, I. M., Young, A. W., … Hall, J. (2010). Deficits in facial, body movement and vocal emotional processing in autism spectrum disorders. Psychological Medicine, 40(11), 1919–1929.

    PubMed  Google Scholar 

  • Renneberg, B., Heyn, K., Gebhard, R., & Bachmann, S. (2005). Facial expression of emotions in borderline personality disorder and depression. Journal of Behavior Therapy and Experimental Psychiatry, 36(3), 183–196.

    PubMed  Google Scholar 

  • Sachse, M., Schlitt, S., Hainz, D., Ciaramidaro, A., Walter, H., Poustka, F., … Freitag, C. M. (2016). Facial emotion recognition in paranoid schizophrenia and autism spectrum disorder. Schizophrenia Research, 159 (2), 509–514.

    Google Scholar 

  • Schultz, R. T. (2005). Developmental deficits in social perception in autism: the role of the amygdala and fusiform face area. International Journal of Developmental Neuroscience, 23(2–3), 125–141.

    PubMed  Google Scholar 

  • Uljarevic, M., & Hamilton, A. (2013). Recognition of emotions in autism: A formal meta-analysis. Journal of Autism and Developmental Disorders, 43(7), 1517–1526.

    PubMed  Google Scholar 

  • Veale, J. F. (2014). Edinburgh handedness inventory–short form: A revised version based on confirmatory factor analysis. Laterality: Asymmetries of Body, Brain and Cognition, 19(2), 164–177.

    Google Scholar 

  • Vetter, N. C., Drauschke, M., Thieme, J., & Altgassen, M. (2018). Adolescent basic facial emotion recognition is not influenced by puberty or own-age bias. Frontiers in Psychology, 9, 956.

    PubMed  PubMed Central  Google Scholar 

  • Wagner, H. L. (1993). On measuring performance in category judgment studies of nonverbal behavior. Journal of Nonverbal Behavior, 17(1), 3–28.

    Google Scholar 

  • Wallace, S., Coleman, M., & Bailey, A. (2008). Face and object processing in autism spectrum disorders. Autism Research, 1(1), 43–51.

    PubMed  Google Scholar 

  • Wechsler, D. (2010). Wechsler Intelligence Scale for Children (4th ed.). Hong Kong: King-May Psychological Assessment.

    Google Scholar 

  • Weigelt, S., Koldewyn, K., & Kanwisher, N. (2012). Face identity recognition in autism spectrum disorders: A review of behavioral studies. Neuroscience & Biobehavioral Reviews, 36(3), 1060–1084.

    Google Scholar 

  • Wolf, J. M., Tanaka, J. W., Klaiman, C., Cockburn, J., Herlihy, L., Brown, C., … Schultz, R. T. (2008). Specific impairment of face-processing abilities in children with autism spectrum disorder using the Let’s Face It! skills battery. Autism Research, 1(6), 329–340.

    PubMed  PubMed Central  Google Scholar 

  • Yeung, M. K., Han, Y. M., Sze, S. L., & Chan, A. S. (2014). Altered right frontal cortical connectivity during facial emotion recognition in children with autism spectrum disorders. Research in Autism Spectrum Disorders, 8(11), 1567–1577.

    Google Scholar 

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Acknowledgments

The authors would like to thank Buddhist Tai Hung College, Chi Lin Buddhist Secondary School, Heep Hong Society, New Life Psychiatric Rehabilitation Association, City of Love, and Parents’ Association of Pre-school Handicapped Children for their assistance in subject recruitment. Appreciation is extended to all adolescents and parents who participated in this research project.

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MY contributed to the conceptualization of the study. MY and TL contributed to the subject recruitment and data collection. MY undertook the data analysis and prepared the initial draft of the manuscript. MY, TL, and AC significantly contributed to the later versions of the manuscript, and read and approved the final version of the manuscript.

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Correspondence to Agnes S. Chan.

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Yeung, M.K., Lee, T.L. & Chan, A.S. Impaired Recognition of Negative Facial Expressions is Partly Related to Facial Perception Deficits in Adolescents with High-Functioning Autism Spectrum Disorder. J Autism Dev Disord 50, 1596–1606 (2020). https://doi.org/10.1007/s10803-019-03915-3

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