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Motivation and Emotion

, Volume 43, Issue 1, pp 191–202 | Cite as

Recognition of facial emotions on human and canine faces in children with and without autism spectrum disorders

  • Denise DavidsonEmail author
  • Elizabeth Hilvert
  • Ieva Misiunaite
  • Katy Kerby
  • Michael Giordano
Original Paper

Abstract

In children with Autism Spectrum Disorders (ASD), it is not clear whether emotion recognition impairments are unique to human faces. In the present study, children with ASD and neurotypical (NT) children were shown photographs of human and canine faces expressing angry, fear, happy, sad, or neutral expressions. Between-group differences showed that children with ASD were less accurate in their overall recognition of emotion on human faces than NT children, whereas the groups did not differ in their recognition of emotion on canine faces. In terms of within-group results, NT children did not differ in their recognition of emotions on human and canine faces, while children with ASD were more accurate in recognizing emotions on canine than on human faces. Although ASD symptomatology was not related to emotion recognition performance, some evidence was found that theory of mind and age were related to emotion recognition in all children.

Keywords

Facial emotion recognition Autism spectrum disorder Basic emotions Theory of mind Human and canine faces 

Notes

Acknowledgements

We wish to thank the children, parents, teachers and staff that made this research possible. Portions of the data were presented at the Society for Research in Child Development 2015 biennial meeting, Philadelphia, PA. Address correspondence regarding this article to Denise Davidson, ddavids@luc.edu.

Compliance with ethical standards

Conflict of interest

The authors report no conflict of interest.

Ethical approval

All procedures performed in the study were approved, and in accordance with, the ethical standards at the host university.

References

  1. American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th edn.). Arlington: American Psychiatric Publishing.Google Scholar
  2. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th edn.). Arlington: American Psychiatric Publishing.CrossRefGoogle Scholar
  3. 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, 2–14.  https://doi.org/10.1016/j.neuropsychologia.2006.04.014.CrossRefGoogle Scholar
  4. Baglio, G., Blasi, V., Intra, F., Castelli, I., Massaro, D., Baglio, F., Valle, A. … Marchetti, A. (2016). Social competence in children with borderline intellectual functioning: Delayed development of theory of mind across all complexity levels. Frontiers in Psychology, 7, 1–10.  https://doi.org/10.3389/fpsyg.2016.01604.Google Scholar
  5. 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.  https://doi.org/10.1007/s10803-009-0884-3.CrossRefGoogle Scholar
  6. Baron-Cohen, S., O’Riordan, M., Stone, V., Jones, R., & Plaisted, K. (1999). Recognition of faux pas by normally developing children and children with Asperger syndrome or high-functioning autism. Journal of Autism and Developmental Disorders, 29, 407–418.CrossRefGoogle Scholar
  7. Baron-Cohen, S., Spitz, A., & Cross, P. (1993). Can children with autism recognize surprise? Cognition and Emotion, 7, 507–516.CrossRefGoogle Scholar
  8. Bloom, T., & Friedman, H. (2013). Classifying dogs’ (canis familiaris) facial expressions from photographs. Behavioural Processes, 96, 1–10.  https://doi.org/10.1016/j.beproc.2013.02.010.CrossRefGoogle Scholar
  9. Bölte, S., Westerwald, E., Holtmann, M., Freitag, C., & Poustka, F. (2011). Autistic traits and autism spectrum disorders: The clinical validity of two measures presuming a continuum of social communication skills. Journal of Autism and Developmental Disorders, 41, 66–72.  https://doi.org/10.1007/s10803-010-1024-9.CrossRefGoogle Scholar
  10. Bolwig, N. (1964). Facial expression in primates with remarks on parallel development in certain carnivores (a preliminary report on work in progress). Behaviour, 22, 167–192.  https://doi.org/10.1163/156853964X00012.CrossRefGoogle Scholar
  11. Boraston, Z., Blakemore, S. J., Chilvers, R., & Skuse, D. (2007). Impaired sadness recognition is linked to social interaction deficit in autism. Neuropsychologia, 45, 1501–1510.  https://doi.org/10.1016/j.neuropsychologia.2006.11.010.CrossRefGoogle Scholar
  12. Bornstein, M. H., & Arterbery, M. E. (2003). Recognition, discrimination, and categorization of smiling by 5-month-old infants. Developmental Science, 6, 585–589.  https://doi.org/10.1111/1467-7687.00314.CrossRefGoogle Scholar
  13. Brosnan, M., Johnson, H., Grawmeyer, B., Chapman, E., & Benton, L. (2015). Emotion recognition in animated compared to human stimuli in adolescents with autism spectrum disorder. Journal of Autism and Developmental Disorders, 45, 1785–1796.  https://doi.org/10.1007/s10803-014-2338-9.CrossRefGoogle Scholar
  14. Camras, L. A., Fatani, S., Fraumeni, B., & Shuster, M. (2016). The development of facial expressions: Current perspectives on infant emotions. In L. F. Barrett, M. Lewis & J. M. Haviland-Jones (Eds.), Handbook of emotions (4th edn., pp. 255–271). New York: Guilford.Google Scholar
  15. Carlisle, G. K. (2014). Pet dog ownership decisions for parents of children with autism spectrum disorder. Journal of Pediatric Nursing, 29, 114–123.  https://doi.org/10.1016/j.pedn.2013.09.005.CrossRefGoogle Scholar
  16. Carlisle, G. K. (2015). The social skills and attachment to dogs of children with autism spectrum disorder. Journal of Autism and Developmental Disorders, 45, 1137–1145.  https://doi.org/10.1007/s10803-014-2267-7.CrossRefGoogle Scholar
  17. Celani, G. (2002). Human beings, animals, and inanimate objects: What do people with autism like? Autism, 6, 93–102.  https://doi.org/10.1177/1362361302006001007.CrossRefGoogle Scholar
  18. Chandler, S., Charman, T., Baird, G., Simonoff, E., & Loucas, T. (2007). Validation of the Social Communication Questionnaire in a population cohort of children with autism spectrum disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 46, 1324–1332.  https://doi.org/10.1097/chi.0b013e31812f7d8d.CrossRefGoogle Scholar
  19. Collin, L., Bindra, J., Raju, M., Gillberg, C., & Minnis, H. (2013). Facial emotion recognition in child psychiatry: A systematic review. Research in Developmental Disabilities, 34, 1505–1520.  https://doi.org/10.1016/j.ridd.2013.01.008.CrossRefGoogle Scholar
  20. Constantino, J. N. (2012). Social Responsiveness Scale (2nd ed.). Los Angeles: Western Psychological Services.Google Scholar
  21. Darwin, C. (1872). The expression of the emotions in man and animals. London: Harper Collins.CrossRefGoogle Scholar
  22. Davidson, D., Vanegas, S. B., & Hilvert, E. (2015). Theory of mind and emotion perception in typically developing children. In J. Schlapa (Ed.), Emotional and facial expressions: Recognition, developmental differences and social importance (pp. 25–48). Hauppauge: Nova Science.Google Scholar
  23. Dawson, G., Webb, S. J., & McPartland, J. (2005). Understanding the nature of face processing impairment in autism: Insights from behavioral and electrophysiological studies. Developmental Neuropsychology, 23, 403–424.  https://doi.org/10.1207/s15326942dn2703_6.CrossRefGoogle Scholar
  24. Durand, K., Gallay, M., Seigneuric, A., Robichon, F., & Baudouin, J. Y. (2007). The development of facial emotion recognition: The role of configural information. Journal of Experimental Child Psychology, 97, 14–27.  https://doi.org/10.1016/j.jecp.2006.12.001.CrossRefGoogle Scholar
  25. Dyck, M. J., Piek, J. P., Hay, D., Smith, L., & Hallmayer, J. (2006). Are abilities abnormally interdependent in children with autism? Journal of Clinical Child and Adolescent Psychology, 35, 20–33.  https://doi.org/10.1207/s15374424jccp35013.CrossRefGoogle Scholar
  26. Ekman, P. (2003). Emotions revealed. New York: Times Books.Google Scholar
  27. Evers, K., Steyaert, J., Noens, I., & Wagemans, J. (2015). Reduced recognition of dynamic facial emotional expressions and emotion-specific response bias in children with an autism spectrum disorder. Journal of Autism and Developmental Disorders, 45, 1774–1784.  https://doi.org/10.1007/s10803-014-2337-x.CrossRefGoogle Scholar
  28. Fernandopulle, N. (2011). Measurement of autism: A review of four screening measures. Indian Journal of Psychological Medicine, 33, 5–10.  https://doi.org/10.4103/0253-7176.85389.CrossRefGoogle Scholar
  29. Fox, M. W. (1970). A comparative study of development of facial expressions in canids: Wolf, coyote and foxes. Behaviour, 36, 49–73.  https://doi.org/10.1163/156853970x00042.CrossRefGoogle Scholar
  30. Gross, T. F. (2004). The perception of four basic emotions in human and nonhuman faces by children with autism and other developmental disabilities. Journal of Abnormal Child Psychology, 32, 469–480.  https://doi.org/10.1023/B:JACP.0000037777.17698.01.CrossRefGoogle Scholar
  31. Harms, M. B., Martin, A., & Wallace, G. L. (2010). Facial emotion recognition in autism spectrum disorders: A review of behavioral neuroimaging studies. Neuropsychology Review, 20, 290–322.  https://doi.org/10.1007/s11065-010-9138-6.CrossRefGoogle Scholar
  32. Hebb, D. O. (1946). On the nature of fear. Psychological Review, 53, 259–276.CrossRefGoogle Scholar
  33. Heerey, E., Keltner, D., & Capps, L. M. (2003). Making sense of self-conscious emotion: Linking theory of mind and emotion in children with autism. Emotion, 3, 394–400.  https://doi.org/10.1037/1528-3542.3.4.394.CrossRefGoogle Scholar
  34. Herba, C., & Phillips, M. (2004). Annotation: Development of facial expression recognition from childhood to adolescence: Behavioral and neurological perspectives. Journal of Child Psychology and Psychiatry, 45, 1185–1198.  https://doi.org/10.1111/j.1469-7610.2004.00316.x.CrossRefGoogle Scholar
  35. Herba, C. M., Landau, S., Russell, T., Ecker, C., & Phillips, M. L. (2006). The development of emotion-processing in children: Effects of age, emotion, and intensity. The Journal of Child Psychology and Psychiatry, 47, 1098–1106.  https://doi.org/10.1111/j.1469-7610.2006.01652.x.CrossRefGoogle Scholar
  36. Hess, U., & Thibault, P. (2009). Darwin and emotion expression. American Psychologist, 64, 120–128.  https://doi.org/10.1037/a0013386.CrossRefGoogle Scholar
  37. Individuals with Disabilities Education Act (IDEA), 20 U.S.C. §1400 (2004).Google Scholar
  38. Kuusikko, S., Haapsamo, H., Jansson-Verkasalo, E., Hurtig, T., Mattila, M. L., Ebeling, H., … Molianen, I. (2009). Emotion recognition in children and adolescents with autism spectrum disorders. Journal of Autism and Developmental Disorders, 39, 938–945.  https://doi.org/10.1007/s10803-009-0700-0.CrossRefGoogle Scholar
  39. Lawrence, K., Campbell, R., & Skuse, D. (2015). Age, gender, and puberty influence the development of facial emotion recognition. Frontiers in Psychology, 6, 1–14.  https://doi.org/10.3389/fpsyg.2015.00761.CrossRefGoogle Scholar
  40. Lewis, M., & Sullivan, M. W. (Eds.). (1996). Emotional development in atypical children. Mahwah: Lawrence Erlbaum Associates, Inc.Google Scholar
  41. Lord, C., & Corsello, C. (2005). Diagnostic instruments in autistic spectrum disorders. In F. R. Volkmar, R. Paul, A. Klin & D. Cohen (Eds.), Handbook of autism and pervasive developmental disorders (pp. 730–767). Hoboken: Wiley.Google Scholar
  42. Lozier, L. M., Vanmeter, J. M., & Marsh, A. A. (2014). Impairments in facial affect recognition associated with autism spectrum disorders: A meta-analysis. Development and Psychopathology, 26, 933–945.  https://doi.org/10.1017/S0954579414000479.CrossRefGoogle Scholar
  43. Mitchell, R. L., & Phillips, L. H. (2015). The overlapping relationship between emotion perception and theory of mind. Neuropsychologia, 70, 1–10.  https://doi.org/10.1016/j.neuropsychologia.2015.02.018.CrossRefGoogle Scholar
  44. Nelson, N. L., & Russell, J. A. (2013). Universality revisited. Emotion Review, 5, 8–15.  https://doi.org/10.1177/1754073912457227.CrossRefGoogle Scholar
  45. O’Haire, M. E., McKenzie, S. J., Beck, A. M., & Slaughter, V. (2013). Social behaviors increase in children with autism in the presence of animals compared to toys. PLoS ONE, 8, e57010.  https://doi.org/10.1371/journal.pone.0057010.CrossRefGoogle Scholar
  46. Pearson Education (2018). Qualifications policy. Retrieved from https://www.pearsonclinical.com/psychology/qualifications.html.
  47. Prothmann, A., Ettrich, C., & Prothmann, S. (2009). Preference for, and responsiveness to, people, dogs, and objects in children with autism. Anthrozoös, 22, 161–171.  https://doi.org/10.2752/175303709X434185.CrossRefGoogle Scholar
  48. Rosset, D. B., Rondan, C., Da Fonseca, D., Santos, A., Assouline, B., & Deruelle, C. (2008). Typical emotion processing for cartoon but not for real faces in children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 38, 919–925.  https://doi.org/10.1007/s100803-007-0465-2.CrossRefGoogle Scholar
  49. Rutter, M., Bailey, A., & Lord, C. (2003). The Social Communication Questionnaire. Los Angeles: Western Psychological Services.Google Scholar
  50. Schopler, E., van Bourgondien, M. E., Wellman, G. J., & Love, S. R. (2010). Childhood Autism Rating Scale (2nd ed.). Los Angeles: Western Psychological Services.Google Scholar
  51. Shariff, A. F., & Tracy, J. L. (2011). What are emotion expressions for? Current Directions in Psychological Science, 20, 395–399.  https://doi.org/10.1177/0963721411424739.CrossRefGoogle Scholar
  52. Tanaka, J. W., Wolf, J. M., Klaiman, C., Koenig, K., Cockburn, J., Herlihy, L., … Schultz, R. T. (2012). The perception and identification of facial emotions in individuals with autism spectrum disorders using the Let’s Face It! emotion skills battery. Journal of Child Psychology and Psychiatry, 53, 1259–1267.  https://doi.org/10.1111/j.1469-7610.2012.02571.x.CrossRefGoogle Scholar
  53. Tardiff, C., Lainé, F., Rodriguez, M., & Gepner, B. (2007). Slowing down presentation of facial movements and vocal sounds enhances facial expression recognition and induces facial-vocal imitation in children with autism. Journal of Autism and Developmental Disorders, 37, 1469–1484.  https://doi.org/10.1007/s10803-006-0223-x.CrossRefGoogle Scholar
  54. Tell, D., Davidson, D., & Camras, L. A. (2014). Recognition of emotion from facial expresssions with direct or averted eye gaze and varying expression intensities in children with autism disorder and typically developing children. Autism Research and Treatment.  https://doi.org/10.1155/2014/816137.Google Scholar
  55. Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. M., Marcus, D. J., … Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168, 242–249.  https://doi.org/10.1016/j.psychres.2008.05.006.CrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. Uljarevic, M., & Hamilton, A. (2013). Recognition of emotions in autism: A formal meta-analysis. Journal of Autism and Developmental Disorders, 43, 1517–1526.  https://doi.org/10.1007/s10803-012-1695-5.CrossRefGoogle Scholar
  58. Wallace, G. L., Case, L. K., Harms, M. B., Silvers, J. A., Kenworthy, L., & Martin, A. (2011). Diminished sensitivity to sad facial expressions in high functioning autism spectrum disorders is associated with symptomatology and adaptive functioning. Journal of Autism and Developmental Disorders, 41, 1475–1486.  https://doi.org/10.1007/s10803-010-1170-0.CrossRefGoogle Scholar
  59. Waller, B. M., & Micheletta, J. (2013). Facial expression in nonhuman animals. Emotion Review, 5, 54–59.  https://doi.org/10.1177/1754073912451503.CrossRefGoogle Scholar
  60. Wechsler, D. (2011). Wechsler abbreviated scale of intelligence (2nd edn.). Bloomington: Pearson, Inc.Google Scholar
  61. Weimer, A. A., Sallquist, J., & Bolnick, R. R. (2012). Young children’s emotion comprehension and theory of mind understanding. Early Education and Development, 23, 280–301.  https://doi.org/10.1080/10409289.2010.517694.CrossRefGoogle Scholar
  62. Whyte, E. M., Behrmann, M., Minshew, N. J., Garcia, N. V., & Scherf, K. S. (2016). Animal, but not human, faces engage the distributed face network in adolescents with autism. Developmental Science, 19, 306–317.  https://doi.org/10.1111/desc.12305.CrossRefGoogle Scholar
  63. Widen, S. C., & Russell, J. A. (2013). Children’s recognition of disgust in others. Psychological Bulletin, 139, 271–299.  https://doi.org/10.1037/a0031640.CrossRefGoogle Scholar
  64. Williams, B. T., & Gray, K. M. (2013). The relationship between emotion recognition ability and social skills in young children with autism. Autism, 17, 762–768.  https://doi.org/10.1177/1362361312465355.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Loyola University ChicagoChicagoUSA

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