Abstract
Children with autism spectrum disorder (ASD) have high levels of anxiety. It is unclear whether they exhibit threat-related attentional biases commensurate with anxiety disorders as manifest in non-ASD populations, such as facilitated attention toward, and difficulties disengaging engaging from, threatening stimuli. Ninety children, 45 cognitively able with ASD and 45 age, perceptual-IQ, and gender matched typically developing children, aged 7–12 years, were administered a visual dot probe task using threatening facial pictures. Parent-reported anxiety symptoms were also collected. Children with ASD showed similarly high levels of anxiety compared with normative data from an anxiety disordered sample. Children with ASD had higher levels of parent-reported anxiety but did not show differences in disengaging from, or facilitated attention toward, threatening facial stimuli compared with typically developing children. In contrast to previously published studies of anxious children, in this study there were no differences in attentional biases in children with ASD meeting clinical cutoff for anxiety and those who did not. There were no correlations between attentional biases and anxiety symptoms and no gender differences. These findings indicate the cognitive mechanisms underlying anxiety in cognitively able children with ASD could differ from those commonly found in anxious children which may have implications for both understanding the aetiology of anxiety in ASD and for anxiety interventions
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References
Adolphs, R. (1999). Social cognition and the human brain. Trends in Cognitive Sciences, 3(12), 469–479.
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders, IV-TR. Washington, DC: American Psychiatric Association.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders 5. Washington, DC: American Psychiatric Association.
Ames, C., & Fletcher-Watson, S. (2010). A review of methods in the study of attention in autism. Developmental Review, 30(1), 52–73.
Amir, N., Elias, J., Klumpp, H., & Przeworski, A. (2003). Attentional bias to threat in social phobia: Facilitated processing of threat or difficulty disengaging attention from threat? Behaviour Research and Therapy, 41(11), 1325–1335.
Bar-Haim, Y., Lamy, D., Pergamin, L., Bakermans-Kranenburg, M. J., & van Ijzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133(1), 1–24. doi:10.1037/0033-2909.133.1.1.
Bar-Haim, Y., Shulman, C., Lamy, D., & Reuveni, A. (2006). Attention to eyes and mouth in high-functioning children with autism. Journal of Autism and Developmental Disorders, 36(1), 131–137. doi:10.1007/s10803-005-0046-1.
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(3), 311–331. doi:10.1080/713756761.
Braverman, M., Fein, D., Lucci, D., & Waterhouse, L. (1989). Affect comprehension in children with pervasive developmental disorders. Journal of Autism and Developmental Disorders, 19(2), 301–316.
Chalfant, A. M., Rapee, R., & Carroll, L. (2007). Treating anxiety disorders in children with high functioning autism spectrum disorders: A controlled trial. Journal of Autism and Developmental Disorders, 37(10), 1842–1857.
Cisler, J. M., & Koster, E. H. (2010). Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. Clinical Psychology Review, 30(2), 203–216. doi:10.1016/j.cpr.2009.11.003.
Constantino, J. N. (2002). The social responsiveness scale. Los Angeles: Western Psychological Services.
Constantino, J. N., Davis, S. A., Todd, R. D., Schindler, M. K., Gross, M. M., Brophy, S. L., & Reich, W. (2003). Validation of a brief quantitative measure of autistic traits: Comparison of the social responsiveness scale with the autism diagnostic interview-revised. Journal of Autism and Developmental Disorders, 33(4), 427–433.
Dalton, K. M., Nacewicz, B. M., Johnstone, T., Schaefer, H. S., Gernsbacher, M. A., Goldsmith, H. H., & Davidson, R. J. (2005). Gaze fixation and the neural circuitry of face processing in autism. Nature Neuroscience, 8(4), 519–526. doi:10.1038/nn1421.
Farrugia, S., & Hudson, J. (2006). Anxiety in adolescents with Asperger syndrome: Negative thoughts, behavioral problems, and life interference. Focus on Autism and Other Developmental Disabilities, 21(1), 25–35. doi:10.1177/10883576060210010401.
Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G* Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175–191.
Fombonne, E. (2003). Epidemiological surveys of autism and other pervasive developmental disorders: An update. Journal of Autism and Developmental Disorders, 33(4), 365–382. doi:10.1023/A:1025054610557.
Georgiou, G. A., Bleakley, C., Hayward, J., Russo, R., Dutton, K., Eltiti, S., & Fox, E. (2005). Focusing on fear: Attentional disengagement from emotional faces. Visual Cognition, 12(1), 145–158. doi:10.1080/13506280444000076.
Ghaziuddin, M. (2002). Asperger syndrome: Associated psychiatric and medical conditions. Focus on Autism and Other Developmental Disabilities, 17(3), 138–144. doi:10.1177/10883576020170030301.
Hallett, V., Lecavalier, L., Sukhodolsky, D. G., Cipriano, N., Aman, M. G., McCracken, J. T., & Hollander, E. (2013). Exploring the manifestations of anxiety in children with autism spectrum disorders. Journal of Autism and Developmental Disorders, 43(10), 2341–2352.
Happe, F., & Frith, U. (2006). The weak coherence account: Detail-focused cognitive style in autism spectrum disorders. Journal of Autism and Developmental Disorders, 36(1), 5–25. doi:10.1007/s10803-005-0039-0.
Hollocks, M. J., Ozsivadjian, A., Matthews, C. E., Howlin, P., & Simonoff, E. (2013). The relationship between attentional bias and anxiety in children and adolescents with autism spectrum disorders. Autism Research, 6(4), 237–247.
Hughes, C., & Russell, J. (1993). Autistic children’s difficulty with mental disengagement from an object: Its implications for theories of autism. Developmental Psychology, 29(3), 498–510. doi:10.1037/0012-1649.29.3.498.
Kerns, C. M., & Kendall, P. C. (2012). The presentation and classification of anxiety in autism spectrum disorder. Clinical Psychology: Science and Practice, 19(4), 323–347.
Kleinhans, N. M., Richards, T., Weaver, K., Johnson, L. C., Greenson, J., Dawson, G., & Aylward, E. (2010). Association between amygdala response to emotional faces and social anxiety in autism spectrum disorders. Neuropsychologia, 48(12), 3665–3670. doi:10.1016/j.neuropsychologia.2010.07.022.
Koster, E. H., Crombez, G., Verschuere, B., & De Houwer, J. (2004). Selective attention to threat in the dot probe paradigm: Differentiating vigilance and difficulty to disengage. Behaviour Research and Therapy, 42(10), 1183–1192. doi:10.1016/j.brat.2003.08.001.
Lang, R., Regester, A., Lauderdale, S., Ashbaugh, K., & Haring, A. (2010). Treatment of anxiety in autism spectrum disorders using cognitive behaviour therapy: A systematic review. Developmental Neurorehabilitation,. doi:10.3109/17518420903236288.
Lecavalier, L. (2006). Behavioral and emotional problems in young people with pervasive developmental disorders: Relative prevalence, effects of subject characteristics, and empirical classification. Journal of Autism and Developmental Disorders,. doi:10.1007/s10803-006-0147-5.
Legerstee, J. S., Tulen, J. H., Kallen, V. L., Dieleman, G. C., Treffers, P. D., Verhulst, F. C., & Utens, E. M. (2009). Threat-related selective attention predicts treatment success in childhood anxiety disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 48(2), 196–205. doi:10.1097/CHI.0b013e31819176e4.
MacLeod, C., Mathews, A., & Tata, P. (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology, 95(1), 15–20.
Mogg, K., & Bradley, B. P. (1999). Some methodological issues in assessing attentional biases for threatening faces in anxiety: A replication study using a modified version of the probe detection task. Behaviour Research and Therapy, 37(6), 595–604.
Mogg, K., Philippot, P., & Bradley, B. P. (2004). Selective attention to angry faces in clinical social phobia. Journal of Abnormal Psychology, 113(1), 160–165. doi:10.1037/0021-843x.113.1.160.
Monk, C. S., Weng, S. J., Wiggins, J. L., Kurapati, N., Louro, H. M. C., Carrasco, M., & Lord, C. (2010). Neural circuitry of emotional face processing in autism spectrum disorders. Journal of Psychiatry and Neuroscience, 35(2), 105–114. doi:10.1503/jpn.090085.
Moree, B. N., & Davis, T. E. (2010). Cognitive-behavioral therapy for anxiety in children diagnosed with autism spectrum disorders: Modification trends. Research in Autism Spectrum Disorders, 4(3), 346–354.
Musa, C., Lepine, J. P., Clark, D. M., Mansell, W., & Ehlers, A. (2003). Selective attention in social phobia and the moderating effect of a concurrent depressive disorder. Behaviour Research and Therapy, 41(9), 1043–1054.
Nauta, M. H., Scholing, A., Rapee, R. M., Abbott, M., Spence, S. H., & Waters, A. (2004). A parent-report measure of children’s anxiety: Psychometric properties and comparison with child-report in a clinic and normal sample. Behaviour Research and Therapy, 42(7), 813–839. doi:10.1016/S0005-7967%2803%2900200-6.
Ozonoff, S., Pennington, B. F., & Rogers, S. J. (1990). Are there emotion perception deficits in young autistic children? Journal of Child Psychology and Psychiatry, 31(3), 343–361.
Pine, D. S., Mogg, K., Bradley, B. P., Montgomery, L., Monk, C. S., McClure, E., & Kaufman, J. (2005). Attention bias to threat in maltreated children: Implications for vulnerability to stress-related psychopathology. American Journal of Psychiatry, 162(2), 291–296. doi:10.1176/appi.ajp.162.2.291.
Puliafico, A. C., & Kendall, P. C. (2006). Threat-related attentional bias in anxious youth: A review. Clinical Child and Family Psychology Review, 9(3–4), 162–180. doi:10.1007/s10567-006-0009-x.
Roy, A. K., Vasa, R. A., Bruck, M., Mogg, K., Bradley, B. P., Sweeney, M., & Pine, D. S. (2008). Attention bias toward threat in pediatric anxiety disorders. Journal of the American Academy of Child and Adolescent Psychiatry, 47(10), 1189–1196. doi:10.1097/CHI.0b013e3181825ace.
Russell, E., & Sofronoff, K. (2005). Anxiety and social worries in children with Asperger syndrome. Australian and New Zealand Journal of Psychiatry, 39(7), 633–638.
Sacrey, L.-A. R., Armstrong, V. L., Bryson, S. E., & Zwaigenbaum, L. (2014). Impairments to visual disengagement in autism spectrum disorder: A review of experimental studies from infancy to adulthood. Neuroscience and Biobehavioral Reviews, 47, 559–577.
Salemink, E., van den Hout, M. A., & Kindt, M. (2007). Selective attention and threat: Quick orienting versus slow disengagement and two versions of the dot probe task. Behaviour Research and Therapy, 45(3), 607–615. doi:10.1016/j.brat.2006.04.004.
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. doi:10.1097/CHI.0b013e318179964f.
Solomon, M., Miller, M., Taylor, S., Hinshaw, S., & Carter, C. S. (2011). Autism symptoms and internalizing psychopathology in girls and boys with autism spectrum disorders. Journal of Autism and Developmental Disorders,. doi:10.1007/s10803-011-1215-z.
Spence, S. H. (1998). A measure of anxiety symptoms among children. Behaviour Research and Therapy, 36(5), 545–566. doi:10.1016/S0005-7967%2898%2900034-5.
Spence, S. H., Barrett, P. M., & Turner, C. M. (2003). Psychometric properties of the Spence Children’s Anxiety Scale with young adolescents. Journal of Anxiety Disorders, 17(6), 605–625.
Storch, E. A., Ehrenreich May, J., Wood, J. J., Jones, A. M., De Nadai, A. S., Lewin, A. B., & Murphy, T. K. (2012). Multiple informant agreement on the anxiety disorders interview schedule in youth with autism spectrum disorders. Journal of Child and Adolescent Psychopharmacology, 22(4), 292–299.
Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Hare, T. A., & Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168(3), 242–249. doi:10.1016/j.psychres.2008.05.006.
Waterhouse, L., Fein, D., & Modahl, C. (1996). Neurofunctional mechanisms in autism. Psychological Review, 103(3), 457–489.
Waters, A. M., Wharton, T. A., Zimmer-Gembeck, M. J., & Craske, M. G. (2008). Threat-based cognitive biases in anxious children: Comparison with non-anxious children before and after cognitive behavioural treatment. Behaviour Research and Therapy, 46(3), 358–374. doi:10.1016/j.brat.2008.01.002.
Watts, S., & Weems, C. (2006). Associations among selective attention, memory bias, cognitive errors and symptoms of anxiety in youth. Journal of Abnormal Child Psychology, 34(6), 838–849. doi:10.1007/s10802-006-9066-3.
Wechsler, D. (1999). Wechsler abbreviated scale of intelligence (WASI). San Antonio, TX: Harcourt Assessment.
Wechsler, D. (2005). WISC—IV Australian administration and scoring manual. Harcourt Assessment.
White, S. W., Oswald, D. P., Ollendick, T. H., & Scahill, L. (2009). Anxiety in children and adolescents with autism spectrum disorders. Clinical Psychology Review, 29(3), 216–229.
Wong, N., Beidel, D. C., Sarver, D. E., & Sims, V. (2012). Facial emotion recognition in children with high functioning autism and children with social phobia. Child Psychiatry and Human Development, 43(5), 775–794. doi:10.1007/s10578-012-0296-z.
Wood, J. J., & Gadow, K. D. (2010). Exploring the nature and function of anxiety in youth with autism spectrum disorders. Clinical Psychology: Science and Practice, 17(4), 281–292.
Acknowledgments
We wish to thank all of the families who generously participated in this research. We also wish to thank Prof. Susan Spence for providing additional information from the Nauta et al (2004) study to facilitate our group comparisons.
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May, T., Cornish, K. & Rinehart, N.J. Mechanisms of Anxiety Related Attentional Biases in Children with Autism Spectrum Disorder. J Autism Dev Disord 45, 3339–3350 (2015). https://doi.org/10.1007/s10803-015-2500-z
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DOI: https://doi.org/10.1007/s10803-015-2500-z