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Attention allocation to facial expressions of emotion among persons with Williams and Down syndromes

Published online by Cambridge University Press:  27 December 2016

Karen J. Goldman*
Affiliation:
Hebrew University of Jerusalem David Yellin Academic College of Education
Cory Shulman
Affiliation:
Hebrew University of Jerusalem
Yair Bar-Haim
Affiliation:
Tel Aviv University
Rany Abend
Affiliation:
Tel Aviv University
Jacob A. Burack
Affiliation:
McGill University
*
Address correspondence and reprint requests to: Karen Goldman, David Yellin Academic College of Education, P.O. Box 3578, Jerusalem 91035, Israel; E-mail: [email protected].

Abstract

Individuals with Williams syndrome and those with Down syndrome are both characterized by heightened social interest, although the manifestation is not always similar. Using a dot-probe task, we examined one possible source of difference: allocation of attention to facial expressions of emotion. Thirteen individuals with Williams syndrome (mean age = 19.2 years, range = 10–28.6), 20 with Down syndrome (mean age = 18.8 years, range = 12.1–26.3), and 19 typically developing children participated. The groups were matched for mental age (mean = 5.8 years). None of the groups displayed a bias to angry faces. The participants with Williams syndrome showed a selective bias toward happy faces, whereas the participants with Down syndrome behaved similarly to the typically developing participants with no such bias. Homogeneity in the direction of bias was markedly highest in the Williams syndrome group whose bias appeared to result from enhanced attention capture. They appeared to rapidly and selectively allocate attention toward positive facial expressions. The complexity of social approach behavior and the need to explore other aspects of cognition that may be implicated in this behavior in both syndromes is discussed.

Type
Regular Articles
Copyright
Copyright © Cambridge University Press 2016 

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Footnotes

This research was funded by a grant from the Eisenberg Foundation (to K.J.G.). We thank all of the participants and their families and schools for their assistance in carrying out this research. We also thank Prof. Doron Gothelf and Dr. Ariel Tennenbaum for their help in recruiting participants with Williams syndrome and Down syndrome, respectively, and Dr. Asael Sklar for his help and advice. The authors have no potential or competing conflicts of interest.

References

Abend, R., Pine, D. S., & Bar-Haim, Y. (2014). The TAU-NIMH Attention Bias Measurement Toolbox. Retrieved from http://people.socsci.tau.ac.il/mu/anxietytrauma/research/ Google Scholar
Annaz, D., Karmiloff-Smith, A., Johnson, M. H., & Thomas, M. S. C. (2009). A cross-syndrome study of the development of holistic face recognition in children with autism, Down syndrome and Williams syndrome. Experimental Child Psychology, 102, 456486.Google Scholar
Bar-Haim, Y. (2010). Research review: Attention bias modification (ABM): A novel treatment for anxiety disorders. Journal of Child Psychology and Psychiatry, 51, 859870.Google Scholar
Bar-Haim, Y., Lamy, D., Pergamin, L., Bakermans-Kranenburg, M. J., & IJzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133, 124.Google Scholar
Broeren, S., Munis, P., Bouwmessler, S., Field, P., & Voerman, J. S. (2011). Processing biases for emotional faces in 4- to 12-year-old nonclinical children: An exploratory study of developmental patterns and relationships with social anxiety and behavioral inhibition. Journal of Experimental Psychopathology, 2, 454474.Google Scholar
Burack, J. A. (1990). Differentiating mental retardation: The two group approach and beyond. In Hodapp, R., Burack, J. A., & Zigler, E. (Eds.), Issues in the developmental approach to mental retardation (pp. 2748). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Burack, J. A., Iarocci, G., Flanagan, T. D., & Bowler, D. M. (2004). On mosaics and melting pots: Conceptual considerations of comparison and matching strategies. Journal of Autism and Developmental Disorders, 34, 6573.Google Scholar
Burack, J. A., Russo, N., Flores, H., Iarocci, G., & Zigler, E. (2012). The more we know, the less we know, but that's OK: Developmental implications for theory, methodology, and interpretation. In Burack, J. A., Hodapp, R. M., Iarocci, G., & Zigler, E. (Eds.), The Oxford handbook of intellectual disability and development (pp. 312). New York: Oxford University Press.Google Scholar
Burack, J. A., Russo, N., Gordon Green, C., Landry, O., & Iarocci, G. (2016). Developments in the developmental approach to intellectual disability. In Cicchetti, D. (Ed.), Developmental psychopathology: Vol. 3. Risk, disorder, and adaptation. Hoboken, NJ: Wiley.Google Scholar
Cebula, K. R., Moore, D. G., & Wishart, J. G. (2010). Social cognition in children with Down's syndrome: Challenges to research and theory building. Journal of Intellectual Disability Research, 54, 113134.Google Scholar
Chapman, R. S., & Hesketh, L. J. (2000). Behavioral phenotype of individuals with Down syndrome. Mental Retardation and Developmental Disabilities Research Reviews, 6, 8495.Google Scholar
Cicchetti, D., & Beeghly, M. (1990). Children with Down syndrome: A developmental perspective. Cambridge: Cambridge University Press.Google Scholar
Cicchetti, D., & Pogge-Hesse, P. (1982). Possible contributions of the study of organically retarded persons to developmental theory. In Zigler, E. & Balla, D. (Eds.), Mental retardation: The developmental-difference controversy. Hillsdale, NJ: Erlbaum.Google Scholar
Conrad, N. J., Schmidt, L. A., Niccols, A., Polak, C. P., Riniolo, P. C., & Burack, J. A. (2007). Frontal electroencephalogram asymmetry during affective processing in children with Down syndrome: A pilot study. Journal of Intellectual Disability Research, 51, 988995.Google Scholar
Cornish, K. M., & Wilding, J. (2010). Attention, genes, and developmental disorders. Oxford: Oxford University Press.Google Scholar
Costanzo, F., Varuzza, C., Menghini, D., Addona, F., Gianesini, T., & Vicari, S. (2013). Executive functions in intellectual disabilities: A comparison between Williams syndrome and Down syndrome. Research in Developmental Disabilities, 34, 17701780.Google Scholar
Dodd, H. F., & Porter, M. A. (2010). I see happy people: Attention bias towards happy but not angry facial expressions in Williams syndrome. Cognitive Neuropsychiatry, 15, 549567.Google Scholar
Donnai, D., & Karmiloff-Smith, A. (2000). Williams syndrome: From genotype through to the cognitive phenotype. American Journal of Medical Genetics, 97, 164171.Google Scholar
Down, J. L. H. (1866). Observations on an ethnic classification of idiots. London Hospital Clinical Lectures and Reports, 3, 259262.Google Scholar
Doyle, T. F., Bellugi, U., Korenberg, J. R., & Graham, J. (2004). “Everybody in the world is my friend”: Hypersociability in young children with Williams syndrome. American Journal of Medical Genetics, 124A, 263273.Google Scholar
Edgin, J. O., Pennington, B., & Mervis, C. B. (2010). Neuropsychological components of intellectual disability: The contributions of immediate, working and associative memory. Journal of Intellectual Disability Research, 54, 406417.Google Scholar
Elam, K. K., Carlson, J. M., DiLalla, L. F., & Reinke, K. S. (2010). Emotional faces capture spatial attention in 5-year-old children. Evolutionary Psychology, 8, 754767.Google Scholar
Elsabbagh, M., & Karmiloff-Smith, A. (2012). The contribution of developmental models toward understanding gene-to-behaviour mapping: The case of Williams syndrome. In Burack, J. A., Hodapp, R. M., Iarocci, G., & Zigler, E. (Eds.), The Oxford handbook of intellectual disability and development (pp. 3041). New York: Oxford University Press.Google Scholar
Fidler, D. J., Most, D. E., Booth-LaForce, C., & Kelly, J. F. (2008). Emerging social strengths in young children with Down syndrome. Infants and Young Children, 21, 207220.Google Scholar
Fisher, M. H. (2014). Evaluation of a stranger safety training programme for adults with Williams syndrome. Journal of Intellectual Disability Research, 58, 903914.Google Scholar
Gagliardi, C., Frigerio, E., Burt, D. M., Cazzaniga, I., Perett, D., & Borgatti, R. (2003). Facial expression recognition in Williams syndrome. Neuropsychologia, 41, 733738.Google Scholar
Gibbs, M. V., & Thorpe, J. G. (1983) Personality stereotype of non-institutionalized Down syndrome children. American Journal of Mental Deficiency, 87, 601605.Google Scholar
Goldman, K. J., Flanagan, T., Shulman, C., Enns, J. T., & Burack, J. A. (2005). Voluntary orienting among children and adolescents with Down syndrome and MA-matched typically developing children. American Journal on Mental Retardation, 110, 157163.Google Scholar
Gunn, P., Berry, P., & Andrews, R. J. (1982). Looking behavior of Down syndrome infants. American Journal of Mental Deficiency, 87, 344347.Google Scholar
Haas, B., Mills, D., Yam, A., Hoeft, F., Bellugi, U., & Reiss, A. (2009). Genetic influences on sociability: Heightened amygdala activity and event-related responses to positive social stimuli in Williams syndrome. Journal of Neuroscience, 29, 11321139.Google Scholar
Haas, B. W., & Reiss, A. L. (2012). Social brain development in Williams syndrome: The current status and directions for future research. Frontiers in Psychology, 3, 113.Google Scholar
Hodapp, R. M., & Burack, J. A. (2006). Developmental approaches to children with mental retardation: A second generation? In Cohen, D. J. & Cicchetti, D. (Eds.), Developmental psychopathology: Vol. 3. Risk, disorder, and adaptation (pp. 235267). Hoboken, NJ: Wiley.Google Scholar
Hodapp, R. M., Burack, J. A., & Zigler, E. (Ed.). (1990). Issues in the developmental approach to mental retardation. Cambridge: Cambridge University Press.Google Scholar
Järvinen, A., Korenberg, J. R., & Bellugi, U. (2013). The social phenotype of Williams syndrome. Current Opinion in Neurobiology, 23, 414422. doi:10.1016/j.conb.2012.12.006 Google Scholar
Jones, W., Bellugi, U., Lai, Z., Chiles, M., Reilly, J., Lincoln, A., & Adolphs, R. (2000). Hypersociability in Williams syndrome. Journal of Cognitive Neuroscience, 12(Suppl. 1), 3046.Google Scholar
Karmiloff-Smith, A., Klima, E., Bellugi, U., Grant, J., & Baron-Cohen, S. (1995). Is there a social module? Language, face processing and theory of mind in individuals with Williams syndrome. Journal of Cognitive Neuroscience, 7, 196208.Google Scholar
Kasari, C., Freeman, S. F. N., & Hughes, M. A. (2001). Emotional recognition by children with Down syndrome. American Journal on Mental Retardation, 106, 5972.Google Scholar
Koster, E. H. W., Crombez, G., Verschuere, B., & DeHouner, J. (2004). Selective attention to threat in the dot probe paradigm: Differentiating vigilance and difficulty to disengage. Behaviour Research and Therapy, 42, 11831192.Google Scholar
Landry, S. H., & Chapieski, M. L. (1990). Joint attention of six-month-old Down syndrome and preterm infants: I. Attention to toys and mother. American Journal on Mental Retardation, 94, 488498.Google Scholar
Lindstrom, K. M., Guyer, A. E., Mogg, K., Bradley, B. P., Fox, N. A., Ernst, M., … Bar-Haim, Y. (2009). Normative data on development of neural and behavioral mechanisms underlying attention orienting toward social-emotional stimuli: An exploratory study. Brain Research, 1292, 6170.Google Scholar
Little, K., Riby, D. M., Janes, E., Clark, F., Fleck, R., & Rodgers, J. (2013). Heterogeneity of social approach behaviour in Williams syndrome: The role of response inhibition. Research in Developmental Disabilities, 34, 959967.Google Scholar
Loane, M., Morris, J. K., Addor, M., Arriola, L., Budd, J., Doray, B., … Dolk, H. (2013). Twenty-year trends in the prevalence of Down syndrome and other trisomies in Europe: Impact of maternal age and prenatal screening. European Journal of Human Genetics, 21, 2733.Google Scholar
MacLeod, C., Mathews, A., & Tata, P. (1986). Attentional bias in emotional disorders. Journal of Abnormal Psychology, 95, 1520.Google Scholar
Mervis, C. B. (2012). Language development in Williams syndrome. In Burack, J. A., Hodapp, R. M., Iarocci, G., & Zigler, E. (Eds.), The Oxford handbook of intellectual disability and development (pp. 217235). New York: Oxford University Press.Google Scholar
Mervis, C. B., & Klein-Tasman, B. P. (2004). Methodological issues in group-matching designs: α levels for control variable comparisons and measurement characteristics of control and target variables. Journal of Autism and Developmental Disorders, 34, 717.Google Scholar
Mervis, C. B., Morris, C. A., Klein-Tasman, B. P., Bertrand, J., Kwitny, S., Appelbaum, L. G., & Rice, C. E. (2003). Attentional characteristics of infants and toddlers with Williams syndrome during triadic interactions. Developmental Neuropsychology, 23, 243268.Google Scholar
Meyer-Lindenberg, A., Hariri, A. R., Munoz, K. E., Mervis, C. B., Mattay, V. S., Morris, C. A., … Berman, K. F. (2005). Neural correlates of genetically abnormal social cognition in Williams syndrome. Nature Neuroscience, 8, 991993.Google Scholar
Mimura, M., Hoef, F., Kato, M., Kobayashi, N., Sheau, K., Piggot, J., … Reiss, A. L. (2010). A preliminary study of orbitofrontal activation and hypersociability in Williams syndrome. Journal of Neurodevelopmental Disorders, 2, 9398.Google Scholar
Morris, J. K., & Springett, A. (2014). The national Down syndrome cytogenic register for England Wales: 2013 annual report. Retrieved from http://www.binocar.org/content/annrep2013_FINAL_nologo.pdf Google Scholar
Ng, R., Järvinen, A., & Bellugi, U. (2014). Towards a deeper characterization of the social phenotype of Williams syndrome: The association between personality and social drive. Research in Developmental Disabilities, 35, 18381849.Google Scholar
Oates, A., Bebbington, A., Bourke, J., Girdler, S., & Leonard, H. (2011). Leisure participation for school-aged children with Down syndrome. Disability and Rehabilitation, 33, 18801889.Google Scholar
Phelps, E. A. (2005). The interaction of emotion and cognition: The relation between the human amygdala and cognitive awareness. In Hassin, R. R., Uleman, J. S., & Bargh, J. A. (Eds.), The new unconscious (pp. 6176). Oxford: Oxford University Press.Google Scholar
Plesa-Skwerer, D., Faja, S., Schofield, C., Verbalis, A., & Tager-Flusberg, H. (2006). Perceiving facial and vocal expressions of emotion in individuals with Williams syndrome. American Journal on Mental Retardation, 111, 1526.Google Scholar
Pober, B. R. (2010). Williams–Beuren syndrome. New England Journal of Medicine, 362, 239252.Google Scholar
Porter, M., Coltheart, M., & Langdon, R. (2007). The neuropsychological basis of hypersociability in Williams and Down syndrome. Neuropsychologia, 45, 28392849.Google Scholar
Randolph, B., & Burack, J. A. (2000). Visual filtering and covert orienting in persons with Down syndrome. International Journal of Behavioral Development, 24, 167172.Google Scholar
Reilly, J., Klima, E. S., & Bellugi, U. (1990). Once more with feeling: Affect and language in atypical populations. Development and Psychopathology, 2, 367392.Google Scholar
Riby, D. M., & Hancock, P. J. B. (2009). Looking at movies and cartoons: Eye-tracking evidence from Williams syndrome and autism. Journal of Intellectual Disability Research, 53, 169181.Google Scholar
Riby, D. M., Jones, N., Brown, P. H., Robinson, L. J. Langton, S., Bruce, V., & Riby, L. M. (2011). Attention to faces in Williams syndrome. Journal of Autism and Developmental Disorders, 41, 12281239.Google Scholar
Riby, D. M., Kirk, H., Hanley, M., & Riby, L. M. (2014). Stranger danger awareness in Williams syndrome. Journal of Intellectual Disability Research, 58, 572582.Google Scholar
Roid, G. M., & Miller, L. J. (1997). Leiter International Performance Scale—Revised. Woodale, IL: Stoelting.Google Scholar
Roy, A. K., Vasa, R. A., Bruck, M., Mogg, K., Bradley, B. P., Sweeney, M., … CAMS Team. (2008). Attention bias toward threat in pediatric anxiety disorders. Journal of the American Academy of Child & Adolescent Psychiatry, 47, 11891196.Google Scholar
Santos, A., Silva, C., Rosset, D., & Deruelle, C. (2010). Just another face in the crowd: Evidence for decreased attention in angry faces in children with Williams syndrome. Neuropsychologia, 48, 10711078.Google Scholar
Tager-Flusberg, H., & Plesa-Skewerer, D. (2013). Social engagement does not lead to social cognition: Evidence from Williams syndrome. In Banaji, M. R. & Gelman, S. A. (Eds.), Navigating the social world (pp. 117123). New York: Oxford University Press.Google Scholar
Tager-Flusberg, H., & Sullivan, K. (2000). A componential view of theory of mind: Evidence from Williams syndrome. Cognition, 76, 5989.Google Scholar
Todd, R. M., Evans, J. W., Morris, D., Lewis, M. D., & Taylor, M. J. (2011). The changing face of emotion: Age-related patterns of amygdala activation to salient faces. SCAN, 6, 1223.Google Scholar
Tottenham, N., Tanaka, J. W., Leon, A. C., McCarry, T., Nurse, M., Todd, A. H., … Nelson, C. (2009). The NimStim set of facial expressions: Judgments from untrained research participants. Psychiatry Research, 168, 242249.Google Scholar
Waters, A. M., Henry, J., Mogg, K., Bradley, B. P., & Pine, D. S. (2010). Attentional bias towards angry faces in childhood anxiety disorders. Journal of Behavior Therapy and Experimental Psychiatry, 41, 158164.Google Scholar
Williams, K. R., Wishart, J., Pitcairn, T., & Willis, D. (2005). Emotion recognition in children with Down syndrome: Investigation of specific impairments and error patterns. American Journal on Mental Retardation, 110, 378392.Google Scholar
Wishart, J. G., & Pitcairn, T. K. (2000). Recognition of identity and expression in faces by children with Down syndrome. American Journal on Mental Retardation, 105, 466479.Google Scholar
Wishart, J. G., Willis, D. S., Cebula, K. R., & Pitcairn, T. K. (2007). Collaborative learning: Comparison of outcomes for typically developing children and children with intellectual disabilities. American Journal on Mental Retardation, 112, 361374.Google Scholar
Ypsilanti, A., & Grouios, G. (2008). Linguistic profiles of individuals with Down syndrome: Comparing linguistic performance of three developmental disorders. Child Neuropsychology, 14, 148170.Google Scholar