Reduced Value-Driven Attentional Capture Among Children with ADHD Compared to Typically Developing Controls
The current study examined whether children with ADHD were more distracted by a stimulus previously associated with reward, but currently goal-irrelevant, than their typically-developing peers. In addition, we also probed the associated cognitive and motivational mechanisms by examining correlations with other behavioral tasks. Participants included 8–12 year-old children with ADHD (n = 30) and typically developing controls (n = 26). Children were instructed to visually search for color-defined targets and received monetary rewards for accurate responses. In a subsequent search task in which color was explicitly irrelevant, we manipulated whether a distractor item appeared in a previously reward-associated color. We examined whether children responded more slowly on trials with the previously-rewarded distractor present compared to trials without this distractor, a phenomenon referred to as value-driven attentional capture (VDAC), and whether children with and without ADHD differed in the extent to which they displayed VDAC. Correlations among working memory performance, immediate reward preference (delay discounting) and attentional capture were also examined. Children with ADHD were significantly less affected by the presence of the previously rewarded distractor than were control participants. Within the ADHD group, greater value-driven attentional capture was associated with poorer working memory. Although both ADHD and control participants were initially distracted by previously reward-associated stimuli, the magnitude of distraction was larger and persisted longer among control participants.
KeywordsADHD Attention Reward Distraction Reinforcement learning
Compliance with Ethical Standards
This work was supported in part by grants from the National Institute of Mental Health (RO1 MH078160; RO1 MH085328, K23 MH101322), the Johns Hopkins University School of Medicine Institute for Clinical and Translational Research National Institutes of Health/National Center for Research Resources Clinical and Translational Science Award program UL1 TR 000424–06, and the Kennedy Krieger Institute/Johns Hopkins University Intellectual and Developmental Disabilities Research Center (IDDRC; U54 HD079123).
Conflict of Interest
The authors declare that they have no conflict of interest.
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
- American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington: American Psychiatric Association.Google Scholar
- Anderson, B. A., Leal, S. L., Hall, M. G., Yassa, M. A., & Yantis, S. (2014b). The attribution of value-based attentional priority in individuals with depressive symptoms. Cognitive, Affective, & Behavioral Neuroscience, 14(4), 1221–1227. https://doi.org/10.3758/s13415-014-0301-z.CrossRefGoogle Scholar
- Anderson, B. A., Kuwabara, H., Wong, D. F., Roberts, J., Rahmim, A., Brasic, J. R., & Courtney, S. M. (2017). Linking dopaminergic reward signals to the development of attentional bias: a positron emission tomographic study. NeuroImage, 157, 27–33. https://doi.org/10.1016/j.neuroimage.2017.05.062.CrossRefPubMedGoogle Scholar
- Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289–300.Google Scholar
- Bubnik, M. G., Hawk, L. W., Pelham, W. E., Waxmonsky, J. G., & Rosch, K. S. (2015). Reinforcement enhances vigilance among children with ADHD: comparisons to typically developing children and to the effects of methylphenidate. Journal of Abnormal Child Psychology, 43(1), 149–161. https://doi.org/10.1007/s10802-014-9891-8.CrossRefPubMedPubMedCentralGoogle Scholar
- Conners, C. K. (1997). Conners' rating scales - revised. North Tonawanda: Mutli-Health Systems, Inc..Google Scholar
- Conners, C. K. (2008). Conners 3. North Tonawanda: Multi-Health Systems, Inc..Google Scholar
- DuPaul, G. J., Power, T. J., Anastopoulos, A. D., & Reid, R. (1998). ADHD rating scale—IV. New York: Guilford Press.Google Scholar
- Epstein, J. N., Brinkman, W. B., Froehlich, T., Langberg, J. M., Narad, M. E., Antonini, T. N., et al. (2011). Effects of stimulant medication, incentives, and event rate on reaction time variability in children with ADHD. Neuropsychopharmacology, 36(5), 1060–1072 https://doi.org/:10.1038/npp.2010.243.CrossRefPubMedPubMedCentralGoogle Scholar
- Fosco, W. D., Hawk Jr., L. W., Rosch, K. S., & Bubnik, M. G. (2015). Evaluating cognitive and motivational accounts of greater reinforcement effects among children with attention-deficit/hyperactivity disorder. Behavioral and Brain Functions, 11(1), 20. https://doi.org/10.1186/s12993-015-0065-9.CrossRefPubMedGoogle Scholar
- Hazell, P. L., Carr, V. J., Lewin, T. J., Dewis, S. A. M., Heathcote, D. M., & Brucki, B. M. (1999). Effortful and automatic information processing in boys with ADHD and specific learning disorders. Journal of Child Psychology and Psychiatry, 40(2), 275–286. https://doi.org/10.1111/1469-7610.00441.CrossRefPubMedGoogle Scholar
- Hollingshead, A. B. (1975). Four factor index of social status. New Haven, CT: Yale University, Department of Sociology.Google Scholar
- Kaufman, J., Birmaher, B., Axelson, D., Perepletchikova, F., Brent, D., & Ryan, N. (2013). Kiddie schedule for affective disorders and schizophrenia for school-aged children – Lifetime version (kiddie-SADS-PL 2013 working draft). Pittsburgh: Western Psychiatric Institute and Clinic and Yale University.Google Scholar
- Kristjansson, A., Sigurjonsdottir, O., & Driver, J. (2010). Fortune and reversals of fortune in visual search: reward contingencies for pop-out targets affect search efficiency and target repetition effects. Attention, Perception, & Psychophysics, 72(5), 1229–1236. https://doi.org/10.3758/APP.72.5.1229.CrossRefGoogle Scholar
- Le Pelley, M. E., Pearson, D., Griffiths, O., & Beesley, T. (2015). When goals conflict with values: counterproductive attentional and oculomotor capture by reward-related stimuli. Journal of Experimental Psychology. General, 144(1), 158–171. https://doi.org/10.1037/xge0000037.CrossRefPubMedGoogle Scholar
- Luciana, M. (2003). Practitioner review: computerized assessment of neuropsychological function in children: clinical and research applications of the Cambridge neuropsychological testing automated battery (CANTAB). Journal of Child Psychology and Psychiatry, 44(5), 649–663.CrossRefPubMedGoogle Scholar
- Martinussen, R., Hayden, J., Hogg-Johnson, S., & Tannock, R. (2005). A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 44(4), 377–384. https://doi.org/10.1097/01.chi.0000153228.72591.73.CrossRefPubMedGoogle Scholar
- Navalpakkam, V., Koch, C., & Perona, P. (2009). Homo economicus in visual search. Journal of Vision, 9(1), 31 31-16. https://doi.org/10.1167/9.1.31.
- Patros, C. H., Alderson, R. M., Kasper, L. J., Tarle, S. J., Lea, S. E., & Hudec, K. L. (2016). Choice-impulsivity in children and adolescents with attention-deficit/hyperactivity disorder (ADHD): a meta-analytic review. Clinical Psychology Review, 43, 162–174. https://doi.org/10.1016/j.cpr.2015.11.001.CrossRefPubMedGoogle Scholar
- Pessoa, L., & Engelmann, J. B. (2010). Embedding reward signals into perception and cognition. Frontiers in Neuroscience, 4. https://doi.org/10.3389/fnins.2010.00017.
- Plichta, M. M., & Scheres, A. (2014). Ventral-striatal responsiveness during reward anticipation in ADHD and its relation to trait impulsivity in the healthy population: a meta-analytic review of the fMRI literature. Neuroscience and Biobehavioral Reviews, 38, 125–134. https://doi.org/10.1016/j.neubiorev.2013.07.012.CrossRefPubMedGoogle Scholar
- Reich, W., Welner, Z., & Herjanic, B. (1997). Diagnostic interview for children and adolescents-IV (DICA-IV). North Tonawanda: Multi-Health Systems, Inc..Google Scholar
- Rosch, K. S., Fosco, W. D., Pelham Jr., W. E., Waxmonsky, J. G., Bubnik, M. G., & Hawk Jr., L. W. (2016). Reinforcement and stimulant medication ameliorate deficient response inhibition in children with attention-deficit/hyperactivity disorder. Journal of Abnormal Child Psychology, 44(2), 309–321. https://doi.org/10.1007/s10802-015-0031-x.CrossRefPubMedPubMedCentralGoogle Scholar
- Sagvolden, T., Johansen, E. B., Aase, H., & Russell, V. A. (2005). A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behavioral and Brain Sciences, 28(3), 397–419; discussion 419-368. https://doi.org/10.1017/S0140525X05000075.CrossRefPubMedGoogle Scholar
- Sali, A. W., Anderson, B. A., & Courtney, S. M. (2016). Information processing biases in the brain: Implications for decision-making and self-governance. Neuroethics. https://doi.org/10.1007/s12152-016-9251-1.
- Shiels, K., Hawk, L. W., Lysczek, C. L., Tannock, R., Pelham, W. E., Spencer, S. V., et al. (2008). The effects of incentives on visual-spatial working memory in children with attention-deficit/hyperactivity disorder. Journal of Abnormal Child Psychology, 36(6), 903–913. https://doi.org/10.1007/s10802-008-9221-0.CrossRefPubMedPubMedCentralGoogle Scholar
- Sonuga-Barke, E. J., Bitsakou, P., & Thompson, M. (2010). Beyond the dual pathway model: evidence for the dissociation of timing, inhibitory, and delay-related impairments in attention-deficit/hyperactivity disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 49(4), 345–355.PubMedGoogle Scholar
- Strand, M. T., Hawk Jr., L. W., Bubnik, M., Shiels, K., Pelham Jr., W. E., & Waxmonsky, J. G. (2012). Improving working memory in children with attention-deficit/hyperactivity disorder: the separate and combined effects of incentives and stimulant medication. Journal of Abnormal Child Psychology, 40(7), 1193–1207. https://doi.org/10.1007/s10802-012-9627-6.CrossRefPubMedPubMedCentralGoogle Scholar
- Visser, S. N., Danielson, M. L., Bitsko, R. H., Holbrook, J. R., Kogan, M. D., Ghandour, R. M., et al. (2014). Trends in the parent-report of health care provider-diagnosed and medicated attention-deficit/hyperactivity disorder: United States, 2003-2011. Journal of the American Academy of Child and Adolescent Psychiatry, 53(1), 34–46 e32.CrossRefPubMedGoogle Scholar
- Wechsler, D. L. (2002). Wechsler individual achievement test - second edition (WIAT-II). San Antonio: The Psychological Corporation.Google Scholar
- Wechsler, D. L. (2003). Wechsler intelligence scale for children - fourth edition (WISC-IV). San Antonio: The Psychological Corporation.Google Scholar
- Wechsler, D. L. (2014). Wechsler intelligence scale for children - fifth edition (WISC-V). The Psychological Corporation.Google Scholar
- Willcutt, E. G., Nigg, J. T., Pennington, B. F., Solanto, M. V., Rohde, L. A., Tannock, R., et al. (2012). Validity of DSM-IV attention deficit/hyperactivity disorder symptom dimensions and subtypes. Journal of Abnormal Psychology. https://doi.org/10.1037/a0027347.