Abstract
This study assessed visual search abilities, tested through the flicker task, in children diagnosed with autism spectrum disorders (ASDs). Twenty-two children diagnosed with ASD and 22 matched typically developing (TD) children were told to detect changes in objects of central interest or objects of marginal interest (MI) embedded in either emotion-laden (positive or negative) or neutral real-world pictures. The results showed that emotion-laden pictures equally interfered with performance of both ASD and TD children, slowing down reaction times compared with neutral pictures. Children with ASD were faster than TD children, particularly in detecting changes in MI objects, the most difficult condition. However, their performance was less accurate than performance of TD children just when the pictures were negative. These findings suggest that children with ASD have better visual search abilities than TD children only when the search is particularly difficult and requires strong serial search strategies. The emotional–social impairment that is usually considered as a typical feature of ASD seems to be limited to processing of negative emotional information.
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References
Adolphs, R., Baron-Cohen, S., & Tranel, D. (2002). Impaired recognition of social emotions following amygdala damage. Journal of Cognitive Neuroscience, 14(8), 1264–1274.
Adolphs, R., Sears, L., & Piven, J. (2001). Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience, 13, 232–240.
American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders (4th ed., rev.). Washington, DC: American Psychiatric Association.
American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (45th ed.). 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.
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.
Bachevalier, J., & Loveland, K. A. (2006). The orbitofrontal-amygdala circuit and self-regulation of social-emotional behavior in autism. Neuroscience and Biobehavioral Reviews, 30(1), 97–117.
Bacon, A. L., Fein, D., Morris, R., Waterhouse, l., & Allen, D. (1998). The responses of autistic children to the distress of others. Journal of Autism and Developmental Disorders, 28, 129–142.
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.
Batty, M., Meaux, E., Wittemeyer, K., Rogè, 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.
Begeer, S., Rieffe, C., Terwogt, M. M., & Stockmann, L. (2006). Attention to facial emotion expressions in children with autism. Autism, 10, 37–51.
Berger, A., Jones, L., Rothbart, M. K., & Posner, M. I. (2000). Computerized games to study the development of attention in childhood. Behavioral Research Methods, Instruments, & Computers, 32(2), 297–303.
Bölte, S., Feineis-Matthews, S., & Poustka, F. (2008). Brief report: Emotional processing in high-functioning autism—physiological reactivity and affective report. Journal of Autism and Developmental Disorders, 38(4), 776–781.
Bormann-Kischkel, C., Vilsmeier, M., & Baude, B. (1995). The development of emotional concepts in autism. Journal of Child Psychology and Psychiatry, 36, 1243–1259.
Bryson, S. E., Landry, R., Czapinski, P., McConnell, B., Rombough, V., & Wainwright, A. (2004). Autistic spectrum disorders: Causal mechanisms and recent findings on attention and emotion. International Journal of Special Education, 19, 14–22.
Burack, J. A., Joseph, S., Russo, N., Shore, D. I., Porporino, M., & Enns, J. T. (2009). Change detection in naturalistic pictures among children with autism. Journal of Autism and Developmental Disorders, 39(3), 471–479.
Caplovitz, G. P., Fendrich, R., & Hughes, H. C. (2008). Failures to see: Attentive blank stares revealed by change blindness. Consciousness and Cognition, 17, 877–886.
Casey, B. J., Gordon, C. T., Mannheim, G. B., & Rumsey, J. M. (1993). Dysfunctional attention in autistic savants. Journal of Clinical and Experimental Neuropsychology, 5(6), 933–946.
Castelli, F. (2005). Understanding emotions from standardized facial expressions in autism and normal development. Autism, 9, 428–449.
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.
Courchesne, E., Townsend, J., Akshoomoff, N. A., Saitoh, O., Yeung-Courchesne, R., Lincoln, A. J., et al. (1994). Impairment in shifting attention in autistic and cerebellar patients. Behavioral Neuroscience, 108(5), 848–865.
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(3), 340–359.
Elsabbagh, M., Divan, G., Koh, Y. J., Kim, Y. S., Kauchali, S., Marcín, C., et al. (2012). Global prevalence of autism and other pervasive developmental disorders. Autism Research, 5, 160–179.
Fletcher-Watson, S., Collis, J. M., Findlay, J. M., & Leekam, S. R. (2009). The development of change blindness: Children’s attentional priorities whilst viewing naturalistic scenes. Developmental Science, 12(3), 438–445.
Fletcher-Watson, S., Leekam, S. R., Connolly, B., Collis, J. M., Findlay, J. M., McConachie, H., et al. (2012). Attenuation of change blindness in children with autism spectrum disorders. The British Journal of Developmental Psychology, 30(3), 446–458.
Fletcher-Watson, S., Leekam, S. R., Turner, M. A., & Moxon, L. (2006). Do people with autistic spectrum disorder show normal selection for attention? Evidence from change blindness. British Journal of Psychology, 97(4), 537–554.
Frith, U. (1989). Autism: Explaining the enigma. Oxford: Basil Blackwell.
Garnett, M. S., & Attwood, A. J. (1998). The Australian Scale for Asperger’s syndrome. In T. Attwood (Ed.), Asperger’s syndrome. A guide for parents and professionals (pp. 17–19). London: Kingsley.
Ghaziuddin, M., & Gerstein, L. (1996). Pedantic speaking style differentiates autism from Asperger syndrome. Journal of Autism and Developmental Disorders, 26(6), 585–595.
Graham, L. M. (2008). Effect of emotional valence on detection of change. Perceptual and Motor Skills, 107(3), 734–736.
Hall, G. B., Szechtman, H., & Nahmias, C. (2003). Enhanced salience and emotion recognition in Autism: A PET study. American Journal of Psychiatry, 160(8), 1439–1441.
Happé, 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.
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.
Heerey, E. A., Keltner, D., & Capps, L. M. (2003). Making sense of self-conscious emotion: Linking theory of mind and emotion in children with autism. Emotion, 3(4), 394–400.
Henderson, J. M. (2003). Human gaze control during real-world scene perception. Trends in Cognitive Sciences, 7, 498–504.
Hill, E., Berthoz, S., & Frith, U. (2004). Brief report: Cognitive processing of own emotions in individuals with autistic spectrum disorder and in their relatives. Journal of Autism and Developmental Disorders, 34(2), 229–235.
Hughes, C., & Russell, J. (1993). Autistic children’s difficulty with mental disengagement from an object: Its implications for theories of autism. Developmental Psychology, 29, 498–510.
Iarocci, G., & Burack, J. A. (2004). Intact covert orienting to peripheral cues among children with autism. Journal of Autism and Developmental Disorders, 34(3), 257–264.
Jones, C. R., Pickles, A., Falcaro, M., Marsden, A. J., Happé, F., Scott, S. K., et al. (2011). A multimodal approach to emotion recognition ability in autism spectrum disorders. The Journal of Child Psychology and Psychiatry, and Allied Disciplines, 52(3), 275–285.
Joseph, R. M., Keehn, B., Connolly, C., Wolfe, J. M., & Horowits, T. S. (2009). Why is visual search superior in autism spectrum disorder? Developmental Science, 12(6), 1083–1096.
Kennedy, D. P., & Adolphs, R. (2012). Perception of emotions from facial expressions in high-functioning adults with autism. Neuropsychologia, 50(14), 3313–3319.
Kikuchi, Y., Senju, A., Tojo, Y., Osanai, H., & Hasegawa, T. (2009). Faces do not capture special attention in children with autism spectrum disorder: A change blindness study. Child Development, 80(5), 1421–1433.
Landry, R., & Bryson, S. E. (2004). Impaired disengagement of attention in young children with autism. Journal of Child Psychology and Psychiatry and Allied Disciplines, 45(6), 1115–1122.
Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (2008). International affective picture system (IAPS): Affective ratings of pictures and instruction manual. Technical Report A-8. University of Florida, Gainesville, FL.
Law Smith, M. J., Montagne, B., Perrett, D. I., Gill, M., & Gallagher, L. (2010). Detecting subtle facial emotion recognition deficits in high-functioning autism using dynamic stimuli of varying intensities. Neuropsychologia, 48(9), 2777–2781.
Leekam, S. R., Lopez, B., & Moore, C. (2000). Attention and joint attention in preschool children with autism. Developmental Psychology, 36(2), 261–273.
Leekam, S., & Moore, C. (2001). The development of attention and joint attention in children with autism. In J. Burack, T. Charman, N. Yirmiya, & P. Zelazo (Eds.), The development of autism: Perspectives from theory and research. London: Lawrence Erlbaum Associates.
Lord, C., Rutter, M., DiLavore, P., & Risi, S. (1999). Autism diagnostic observation schedule—WPS edition. Los Angeles, CA: Western Psychological Services.
Lord, C., Rutter, M., & LeCouteur, 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, 659–685.
Losh, M., & Capp, L. (2006). Understanding of emotional experience in autism: Insights from the personal accounts of high-functioning children with autism. Developmental Psychology, 42(5), 809–818.
Loveland, K. A., Tunali-Kotoski, B., Chen, Y. R., Ortegon, J., Pearson, D. A., Brelsford, K. A., et al. (1997). Emotion recognition in autism: Verbal and nonverbal information. Journal of Development and Psychopathology, 9, 579–593.
Maccari, L., Casagrande, M., Martella, D., Fuentes, L. J., Anolfo, M., Rosa, C., et al. (2012). Change blindness in children with attention-deficit/hyperactivity disorder: A selective impairment in visual search? Journal of Attention Disorders. doi:10.1177/1087054711433294.
MacDonald, H., Rutter, M., Howlin, P., Rios, P., LeCouteur, A., Evered, C., et al. (1989). Recognition and expression of emotional cues by autistic and normal adults. Journal of Child Psychology and Psychiatry, 30, 865–877.
Maras, K. L., Gaigg, S. B., & Bowler, D. M. (2012). Memory for emotionally arousing events over time in autism spectrum disorder. Emotion, 12(5), 1118–1128.
Marotta, A., Pasini, A., Ruggiero, S., Maccari, L., Rosa, C., Lupiáñez, J., et al. (2013). Inhibition of return in response to eye gaze and peripheral cues in young people with Asperger’s syndrome. Journal of Autism and Developmental Disorders, 43(4), 917–923.
McIntosh, D. N., Reichmann-Decker, A., Winkielman, P., & Wilbarger, P. (2006). When the social mirror breaks: Deficits in automatic, but not voluntary, mimicry of emotional facial expressions in autism. Developmental Science, 9(3), 295–302.
Nacewicz, B. M., Dalton, K. M., Johnstone, T., Long, M. T., McAuliff, E. M., Oakes, T. R., et al. (2006). Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Archives of General Psychiatry, 63(12), 1417–1428.
New, J. J., Schultz, R. T., Wolf, J., Niehaus, J. L., Klin, A., German, T. C., et al. (2010). The scope of social attention deficits in autism: Prioritized orienting to people and animals in static natural scenes. Neuropsychologia, 48(1), 51–59.
Newschaffer, C. J., Croen, L. A., Daniels, J., Giarelli, E., Grether, J. K., Levy, S. E., et al. (2007). The epidemiology of autism spectrum disorders. Annual Review of Public Health, 28, 235–258.
Noterdaeme, M., Wriedt, E., & Höhne, C. (2010). Asperger’s syndrome and high-functioning autism: Language, motor and cognitive profiles. European Child and Adolescent Psychiatry, 19(6), 475–481.
Nuske, H. J., Vivanti, G., & Dissanayake, C. (2013). Are emotion impairments unique to, universal, or specific in autism spectrum disorder? A comprehensive review. Cognition and Emotion, 27(6), 1042–1061.
O’Riordan, M. A. (2004). Superior visual search in adults with autism. Autism, 8, 229–248.
O’Riordan, M. A., Plaisted, K. C., Driver, J., & Baron-Cohen, S. (2001). Superior visual search in autism. Journal of Experimental Psychology: Human Perception and Performance, 27, 719–730.
Pelphrey, K. A., Adolphs, R., & Morris, J. P. (2004). Neuroanatomical substrates of social cognition dysfunction in autism. Mental Retardation and Developmental Disabilities Research Reviews, 10(4), 259–271.
Plaisted, K., O’Riordan, M., & Baron-Cohen, S. (1998). Enhanced visual search for a conjunctive target in autism: A research note. Journal of Child Psychology and Psychiatry and Allied Disciplines, 39, 777–783.
Press, C., Richardson, D., & Bird, G. (2010). Intact imitation of emotional facial actions in autism spectrum conditions. Neuropsychologia, 48(11–3), 3291–3297.
Raven, J. C., Court, J. H., & Raven, J. C. (1990). Manual for Raven’s progressive matrices and vocabulary scales—section 2: Coloured progressive matrices. Oxford: Oxford Psychologists Press.
Raven, J. C., Raven, J. C., & Court, J. H. (1993). Test de Matrices Progressives. Manual. Buenos Aires: Paidós.
Remington, A. M., Swettenham, J. G., & Lavie, N. (2012). Lightening the load: Perceptual load impairs visual detection in typical adults but not in autism. Journal of Abnormal Psychology, 121(2), 544–551.
Rensink, R. A. (2000). Visual search for change: A probe into the nature of attentional processing. Visual Cognition, 7, 345–376.
Rensink, R. A., O’Regan, J. K., & Clark, J. J. (2000). On the failure to detect changes in scenes across brief interruptions. Visual cognition, 7, 127–145.
Rensink, R. A., O’Regan, J. K., & Clark, J. J. (1997). To see or not to see: The need for attention to perceive changes in scenes. Psychological Science, 8, 368–373.
Rieffe, C., Meerum Terwogt, M., & Kotronopoulou, K. (2007). Awareness of single and multiple emotions in high-functioning children with autism. Journal of Autism and Developmental Disorders, 37(3), 455–465.
Schopler, E., Reichler, R., & Rochen Renner, B. (1998). The childhood autism rating scale (CARS). Los Angeles, CA: Western Psychological Service.
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.
Schumann, C. M., & Amaral, D. G. (2006). Stereological analysis of amygdala neuron number in autism. Journal of Neuroscience, 26(29), 7674–7679.
Schumann, C., Barnes, C., Lord, C., & Courchesne, E. (2009). Amygdala enlargement in toddlers with autism related to severity of social and communication impairments. Biological Psychiatry, 66(10), 942–949.
Shalom, D. B., Mostofsky, S. H., Hazlett, R. L., Goldberg, M. C., Landa, R. J., Faran, Y., et al. (2006). Normal physiological emotions but differences in expression of conscious feelings in children with high-functioning autism. Journal of Autism and Developmental Disorders, 36(3), 395–400.
Shore, D. I., Burack, J. A., Miller, D., Joseph, S., & Enns, J. T. (2006). The development of change detection. Developmental Science, 9(5), 490–497.
Sigman, M. D., Kasari, C., Kwon, J., & Yirmiya, N. (1992). Responses to the negative emotions of others by autistic, mentally retarded and normal children. Child Development, 63, 796–807.
Silani, G., Bird, G., Brindley, R., Singer, T., Frith, C., & Frith, U. (2007). Levels of emotional awareness and autism: An fMRI study. Social Neuroscience, 3(2), 97–112.
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.
Simons, D. J., & Levin, D. T. (1997). Change blindness. Trends in Cognitive Sciences, 1(7), 261–267.
Smith, H., & Milne, E. (2009). Reduced change blindness suggests enhanced attention to detail in individuals with autism. The Journal of Child Psychology and Psychiatry, and Allied Disciplines, 50(3), 300–306.
South, M., Ozonoff, S., Suchy, Y., Kesner, R. P., McMahon, M. W., & Lainhart, J. E. (2008). Intact emotion facilitation for nonsocial stimuli in autism: Is amygdala impairment in autism specific for social information? Journal of the International Neuropsychological Society, 14(1), 42–54.
Taylor, S. E. (1991). Asymmetrical effects of positive and negative events: The mobilization-minimization hypothesis. Psychological Bulletin, 110, 67–85.
Tonge, B. J., Brereton, A. V., Gray, K. M., & Einfeld, S. L. (1999). Behavioural and emotional disturbance in high-functioning autism and Asperger’s disorder. Autism, 3, 117–130.
Tottenham, N., Hertzig, M. E., Gillespie-Lynch, K., Gilhooly, T., Millner, A. J., & Casey, B. J. (2013). Elevated amygdala response to faces and gaze aversion in autism spectrum disorder. Social Cognitive and Affective Neuroscience. doi:10.1093/scan/nst050.
Tracy, J. L., Robins, R. W., Schriber, R. A., & Solomon, M. (2011). Is emotion recognition impaired in individuals with autism spectrum disorders? Journal of Autism and Developmental Disorders, 41, 102–109.
Wainwright-Sharp, J. A., & Bryson, S. E. (1993). Visual orienting deficits in high functioning people with autism. Journal of Autism and Developmental Disorders, 23(1), 1–13.
Wallace, S., Coleman, M., & Bailey, A. (2008). An investigation of basic facial expression recognition in autism spectrum disorders. Cognition and Emotion, 22(7), 1353–1380.
Wechsler, D. (1991). Manual for the Wechsler Intelligence Scale for Children (3rd ed.). San Antonio, TX: Psychological Corporation.
Whalen, P. J. (2013). Neuroscience AND FACIAL EXPRESSIONS OF EMOTIon: The Role of Amygdala– Prefrontal Interactions. Emotion Review, 5(1), 78–83.
White, S. W., Keonig, K., & Scahill, L. (2007). Social Skills Development in Children with Autism Spectrum. Disorders: A Review of the Intervention Research. Journal of Autism and Developmental Disorders, 37(10), 1858–1868.
Wilbarger, J. L., McIntosh, D. N., & Winkielman, P. (2009). Startle modulation in autism: Positive affective stimuli enhance startle response. Neuropsychologia, 47, 1323–1331.
Williams, D., & Happé, F. (2010). Recognising ‘social’ and ‘non-social’ emotions in self and others: A study of autism. Autism, 14(4), 285–304.
Wolfe, J. M., Butcher, S. J., Lee, C., & Hyle, M. (2003). Changing your mind: On the contributions of top-down and bottomup guidance in visual search for feature singletons. Journal of Experimental Psychology: Human Perception and Performance, 29, 483–502.
Ziatas, K., Durkin, K., & Pratt, C. (1998). Belief term development in children with autism, Asperger syndrome, specific language impairment, and normal development: links to theory of mind development. Journal of Child Psychology and Psychiatry and Allied Disciplines, 39(5), 755–763.
Acknowledgments
We would like to thank all the children, parents, and teachers of primary schools “Istituto P.M. Corradini” and “Istituto Giuseppe Sinopoli”. We would also like to thank all the children with ASD and their parents; Flavia Caretto, MD and “Associazione Gruppo Asperger”, with particular regard to Miss Laura Imbimbo and Miss Adina Adami; the ward of Child Neuropsychiatry of the Institute of Rehabilitation “Villaggio Eugenio Litta” in Grottaferrata (Rome), with particular regard to Luisa Lopez, Nadia Volpe, and Chiara Terribili. This research was supported by the Grant PSI2011-23340 to L.J.F.
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Maccari, L., Pasini, A., Caroli, E. et al. Visual Search and Emotion: How Children with Autism Spectrum Disorders Scan Emotional Scenes. J Autism Dev Disord 44, 2871–2881 (2014). https://doi.org/10.1007/s10803-014-2148-0
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DOI: https://doi.org/10.1007/s10803-014-2148-0