Overlapping and Distinct Cognitive Impairments in Attention-Deficit/Hyperactivity and Autism Spectrum Disorder without Intellectual Disability

  • Sarah L. Karalunas
  • Elizabeth Hawkey
  • Hanna Gustafsson
  • Meghan Miller
  • Marybeth Langhorst
  • Michaela Cordova
  • Damien Fair
  • Joel T. Nigg
Article

Abstract

Attention-deficit/hyperactivity disorder (ADHD) and autism spectrum disorder (ASD) are commonly comorbid, share genetic liability, and often exhibit overlapping cognitive impairments. Clarification of shared and distinct cognitive effects while considering comorbid symptoms across disorders has been lacking. In the current study, children ages 7–15 years assigned to three diagnostic groups:ADHD (n = 509), ASD (n = 97), and controls (n = 301) completed measures spanning the cognitive domains of attention/arousal, working memory, set-shifting, inhibition, and response variability. Specific processes contributing to response variability were examined using a drift diffusion model, which separately quantified drift rate (i.e., efficiency of information processing), boundary separation (i.e., speed-accuracy trade-offs), and non-decision time. Children with ADHD and ASD were impaired on attention/arousal, processing speed, working memory, and response inhibition, but did not differ from controls on measures of delayed reward discounting, set-shifting, or interference control. Overall, impairments in the ASD group were not attributable to ADHD symptoms using either continuous symptom measures or latent categorical grouping approaches. Similarly, impairments in the ADHD group were not attributable to ASD symptoms. When specific RT parameters were considered, children with ADHD and ASD shared impairments in drift rate. However, children with ASD were uniquely characterized by a wider boundary separation. Findings suggest a combination of overlapping and unique patterns of cognitive impairment for children with ASD as compared to those with ADHD, particularly when the processes underlying reaction time measures are considered separately.

Keywords

Attention-deficit/hyperactivity disorder (ADHD) Autism spectrum disorders (ASD) Executive function Neuropsychology Reaction time variability Diffusion model 

Notes

Acknowledgements

This project was supported by Simons Foundation #177894 and by National Institutes of Health R01 MH096773 (Fair), R00MH091238 (Fair), R01 MH086654 (Nigg), R37 MH059105 13 (Nigg), and K23 MH108656 (Karalunas). We thank Corinne Stevens, Libby Nousen, and Andrew Bontemps for assistance with data collection and preparation. We gratefully acknowledge the participants and their caregivers, as well as the graduate students, staff, and research assistants whose remarkable dedication has made this research possible.

Compliance with Ethical Standards

Conflict of Interest

The authors have no conflicts of interest or financial disclosures to report.

Ethical Approval

All procedures were approved by the Oregon Health & Science University’s Institutional Review Board.

Informed Consent

Parents provided written informed consent and children provided written assent.

Supplementary material

10802_2017_394_MOESM1_ESM.docx (41 kb)
ESM 1 (DOCX 40 kb)

References

  1. Baddeley, A. (1996). The fractionation of working memory. Proceedings of the National Academy of Sciences U S A, 93(24), 13468–13472.CrossRefGoogle Scholar
  2. 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), 289–300.Google Scholar
  3. Best, J. R., & Miller, P. H. (2010). A developmental perspective on executive function. Child Development, 81(6), 1641–1660.  https://doi.org/10.1111/j.1467-8624.2010.01499.x.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bishop, D. V. M. (2003). The Children’s Communication Checklist, Second Edition (CCC-2). London: The Psychological Corporation.Google Scholar
  5. Conners, C. K. (2008). The Conners 3rd Edition (Conners 3). North Tonawanda: Multi-Health System.Google Scholar
  6. Constantino, J. N., & Gruber, C. P. (2012). The social responsiveness scale, Second Edition (SRS-2). Los Angeles: Western Psychological Services.Google Scholar
  7. Corbett, B. A., Constantine, L. J., Hendren, R., Rocke, D., & Ozonoff, S. (2009). Examining executive functioning in children with autism spectrum disorder, attention deficit hyperactivity disorder and typical development. Psychiatry Research, 166(2), 210–222.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Davis, N. O., & Kollins, S. H. (2012). Treatment for co-occurring attention deficit/hyperactivity disorder and autism spectrum disorder. Neurotherapeutics, 9(3), 518–530.CrossRefPubMedPubMedCentralGoogle Scholar
  9. De Luca, C. R., Wood, S. J., Anderson, V., Buchanan, J. A., Proffitt, T. M., Mahony, K., & Pantelis, C. (2003). Normative data from the CANTAB. I: development of executive function over the lifespan. Journal of Clinical Experimental Neuropsychology, 25(2), 242–254.  https://doi.org/10.1076/jcen.25.2.242.13639.CrossRefPubMedGoogle Scholar
  10. Delis, D. C., Kaplan, E., & Kramer, J. H. (2001). Delis-Kaplan Executive Function System (D-KEFS). San Antonio: The Pscyhological Corporation.Google Scholar
  11. Demurie, E., Roeyers, H., Baeyens, D., & Sonuga-Barke, E. (2012). Temporal discounting of monetary rewards in children and adolescents with ADHD and autism spectrum disorders. Developmental Science, 15(6), 791–800.  https://doi.org/10.1111/j.1467-7687.2012.01178.x.CrossRefPubMedGoogle Scholar
  12. Dennis, M., Francis, D. J., Cirino, P. T., Schachar, R., Barnes, M. A., & Fletcher, J. M. (2009). Why IQ is not a covariate in cognitive studies of neurodevelopmental disorders. Journal of the International Neuropsychological Society, 15(3), 331–343.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Di Martino, A., Zuo, X.-N., Kelly, C., Grzadzinski, R., Mennes, M., Schvarcz, A., & Milham, M. P. (2013). Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder. Biological Psychiatry, 74(8), 623–632.CrossRefPubMedPubMedCentralGoogle Scholar
  14. DuPaul, G., Power, T., Anastopoulos, A., & Reid, R. (1998). ADHD Rating Scale—IV: Checklists, Norms, and Clinical Interpretation. NY: Guilford Press.Google Scholar
  15. Engle, R. W. (2002). Working memory capacity as executive attention. Current Directions in Psychological Science, 11(1), 19–23.CrossRefGoogle Scholar
  16. Fair, D. A., Bathula, D., Nikolas, M. A., & Nigg, J. T. (2012). Distinct neuropsychological subgroups in typically developing youth inform heterogeneity in children with ADHD. Proceedings of the National Academy of Sciences of the USA, 109(17), 6769–6774.  https://doi.org/10.1073/pnas.1115365109.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gargaro, B. A., Rinehart, N. J., Bradshaw, J. L., Tonge, B. J., & Sheppard, D. M. (2011). Autism and ADHD: how far have we come in the comorbidity debate? Neuroscience & Biobehavioral Reviews, 35(5), 1081–1088.CrossRefGoogle Scholar
  18. Geurts, H. M., Verte, S., Oosterlaan, J., Roeyers, H., & Sergeant, J. A. (2004). How specific are executive functioning deficits in attention deficit hyperactivity disorder and autism? Journal of Child Psychology and Psychiatry, 45(4), 836–854.CrossRefPubMedGoogle Scholar
  19. Goodman, R. (2001). Psychometric properties of the strengths and difficulties questionnaire. Journal of the American Academy of Child and Adolescent Psychiatry, 40(11), 1337–1345.  https://doi.org/10.1097/00004583-200111000-00015.CrossRefPubMedGoogle Scholar
  20. Happe, F., Booth, R., Charlton, R., & Hughes, C. (2006). Executive function deficits in autism spectrum disorders and attention-deficit/hyperactivity disorder: examining profiles across domains and ages. Brain and Cognition, 61(1), 25–39.  https://doi.org/10.1016/j.bandc.2006.03.004.CrossRefPubMedGoogle Scholar
  21. Harris, P. A., Taylor, R., Thielke, R., Payne, J., Gonzalez, N., & Conde, J. G. (2009). Research electronic data capture (REDCap)--a metadata-driven methodology and workflow process for providing translational research informatics support. Journal of Biomedical Informatics, 42(2), 377–381.  https://doi.org/10.1016/j.jbi.2008.08.010.CrossRefPubMedGoogle Scholar
  22. Hill, E. L. (2004). Executive dysfunction in autism. Trends in Cognitive Sciences, 8(1), 26–32.  https://doi.org/10.1016/j.tics.2003.11.003.CrossRefPubMedGoogle Scholar
  23. Huang-Pollock, C. L., Karalunas, S. L., Tam, H., & Moore, A. N. (2012). Evaluating vigilance deficits in ADHD: a meta-analysis of CPT performance. Journal of Abnormal Psychology, 121(2), 360–371.  https://doi.org/10.1037/a0027205.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Hulst, B. M., Zeeuw, P., Bos, D. J., Rijks, Y., Neggers, S. F., & Durston, S. (2017). Children with ADHD symptoms show decreased activity in ventral striatum during the anticipation of reward, irrespective of ADHD diagnosis. Journal of Child Psychology and Psychiatry, 58(2), 206–214.CrossRefPubMedGoogle Scholar
  25. Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., & Wang, P. (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. The American Journal of Psychiatry, 167(7), 748–751.  https://doi.org/10.1176/appi.ajp.2010.09091379.CrossRefPubMedGoogle Scholar
  26. Kane, M.J., Conway, A., Hambrick, D.Z., & Engle, R.W. (2007). Variation in working memory capacity as variation in executive attention and control Variation in Working Memory (pp. 21–48).Google Scholar
  27. Karalunas, S. L., Geurts, H. M., Konrad, K., Bender, S., & Nigg, J. T. (2014). Annual research review: Reaction time variability in ADHD and autism spectrum disorders: measurement and mechanisms of a proposed trans-diagnostic phenotype. Journal of Child Psychology and Psychiatry, 55(6), 685–710.  https://doi.org/10.1111/jcpp.12217.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Karalunas, S. L., Gustafsson, H. C., Dieckmann, N., Tipsord, J., Mitchell, S. H., & Nigg, J. T. (2017). Heterogeneity in development of aspects of working memory predicts longitudinal ADHD symptom change. Journal of Abnormal Psychology, 126(6), 774.Google Scholar
  29. Karalunas, S. L., & Huang-Pollock, C. L. (2013). Integrating impairments in reaction time and executive function using a diffusion model framework. Journal of Abnormal Child Psychology, 41(5), 837–850.  https://doi.org/10.1007/s10802-013-9715-2.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kofler, M. J., Rapport, M. D., Sarver, D. E., Raiker, J. S., Orban, S. A., Friedman, L. M., & Kolomeyer, E. G. (2013). Reaction time variability in ADHD: A meta-analytic review of 319 studies. Clinical Psychology Review, 33(6), 795–811.CrossRefPubMedGoogle Scholar
  31. Logan, G. (1994). On the ability to inhibit thought and action: A users' guide to the stop signal paradigm. In D. Dagenbach & T. H. Carr (Eds.), Inhibitory processes in attention, memory, and language (pp. 189–239). San Diego: Academic Press.Google Scholar
  32. Lord, C., Rutter, M., DiLavore, P. C., & Risi, S. (2001). Autism Diagnostic Observation Schedule (ADOS). Los Angeles: Western Psychological Services.Google Scholar
  33. McDonald, J. H. (2014). Handbook of Biological Statistics (3rd ed.). Baltimore: Sparky House Publishing.Google Scholar
  34. Miller, M., Loya, F., & Hinshaw, S. P. (2013). Executive functions in girls with and without childhood ADHD: developmental trajectories and associations with symptom change. Journal of Child Psychology and Psychiatry, 54(9), 1005–1015.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Miodovnik, A., Harstad, E., Sideridis, G., & Huntington, N. (2015). Timing of the diagnosis of attention-deficit/hyperactivity disorder and autism spectrum disorder. Pediatrics, 136(4), e830–e837.CrossRefPubMedGoogle Scholar
  36. Mitchell, S. H. (1999). Measures of impulsivity in cigarette smokers and non-smokers. Psychopharmacology, 146(4), 455–464.CrossRefPubMedGoogle Scholar
  37. Mitchell, S. H., Wilson, V. B., & Karalunas, S. L. (2015). Comparing hyperbolic, delay-amount sensitivity and present-bias models of delay discounting. Behavioural Processes, 114, 52–62.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Musser, E. D., Hawkey, E., Kachan-Liu, S. S., Lees, P., Roullet, J. B., Goddard, K., & Nigg, J. T. (2014). Shared familial transmission of autism spectrum and attention-deficit/hyperactivity disorders. Journal of Child Psychology and Psychiatry, 55(7), 819–827.  https://doi.org/10.1111/jcpp.12201.CrossRefPubMedPubMedCentralGoogle Scholar
  39. Nigg, J., Willcutt, E. G., Doyle, A. E., & Sonuga-Barke, E. J. S. (2005). Causal Heterogeneity in Attention-Deficit/ Hyperactivity Disorder: Do We Need Neuropsychologically Impaired Subtypes? Biological Psychiatry, 57(11), 1224–1230.CrossRefPubMedGoogle Scholar
  40. Nigg, J. T. (1999). The ADHD response-inhibition deficit as measured by the stop task: Replication with DSM-IV combined type, extension, and qualification. Journal of Abnormal Child Psychology, 27(5), 393–402.CrossRefPubMedGoogle Scholar
  41. Nigg, J. T. (2000). On inhibition/disinhibition in developmental psychopathology: views from cognitive and personality psychology and a working inhibition taxonomy. Psychological Bulletin, 126(2), 220–246.CrossRefPubMedGoogle Scholar
  42. Nigg, J. T., Hinshaw, S. P., & Halperin, J. M. (1996). Continuous performance test in boys with attention deficit hyperactivity disorder: Methylphenidate dose response and relations with observed behaviors. Journal of Clinical Child Psychology, 25(3), 330–340.CrossRefGoogle Scholar
  43. Nyden, A., Niklasson, L., Stahlberg, O., Anckarsater, H., Wentz, E., Rastam, M., & Gillberg, C. (2010). Adults with autism spectrum disorders and ADHD neuropsychological aspects. Research in Developmental Disabilities, 31(6), 1659–1668.  https://doi.org/10.1016/j.ridd.2010.04.010.CrossRefPubMedGoogle Scholar
  44. Ozonoff, S., & Jensen, J. (1999). Brief report: specific executive function profiles in three neurodevelopmental disorders. Journal of Autism and Developmental Disorders, 29(2), 171–177.CrossRefPubMedGoogle Scholar
  45. Pennington, B. F., & Ozonoff, S. (1996). Executive functions and developmental psychopathology. Journal of Child Psychology and Psychiatry. Special Issue: Annual research review, 37(1), 51–87.CrossRefPubMedGoogle Scholar
  46. Pirrone, A., Dickinson, A., Gomez, R., Stafford, T., & Milne, E. (2017). Understanding perceptual judgment in autism spectrum disorder using the drift diffusion model. Neuropsychology, 31(2), 173.CrossRefPubMedGoogle Scholar
  47. Puig-Antich, J., & Ryan, N. (1986). Kiddie schedule for affective disorders and schizophrenia. Pittsburgh: Western Psychiatric Institute.Google Scholar
  48. Ratcliff, R. (2002). A diffusion model account of response time and accuracy in a brightness discrimination task: fitting real data and failing to fit fake but plausible data. Psychonomic Bulletin & Review, 9(2), 278–291.  https://doi.org/10.3758/BF03196283.CrossRefGoogle Scholar
  49. Ratcliff, R. (2006). Modeling response signal and response time data. Cognitive Psychology, 53(3), 195–237.  https://doi.org/10.1016/j.cogpsych.2005.10.002.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ratcliff, R., & Rouder, J. N. (2016). Modeling response times for two-choice decisions. Psychological Science, 9(5), 347–356.  https://doi.org/10.1111/1467-9280.00067.CrossRefGoogle Scholar
  51. Raymaekers, R., Antrop, I., van der Meere, J. J., Wiersema, J. R., & Roeyers, H. (2007). HFA and ADHD: a direct comparison on state regulation and response inhibition. Journal of Clinical and Experimental Neuropsychology, 29(4), 418–427.  https://doi.org/10.1080/13803390600737990.CrossRefPubMedGoogle Scholar
  52. Rommelse, N., Geurts, H., Franke, B., Buitelaar, J., & Hartman, C. (2011). A review on cognitive and brain endophenotypes that may be common in autism spectrum disorder and attention-deficit/hyperactivity disorder and facilitate the search for pleiotropic genes. Neuroscience & Biobehavioral Reviews, 35, 1363–1396.CrossRefGoogle Scholar
  53. Rommelse, N. N., Franke, B., Geurts, H. M., Hartman, C. A., & Buitelaar, J. K. (2010). Shared heritability of attention-deficit/hyperactivity disorder and autism spectrum disorder. European Child & Adolescent Psychiatry, 19(3), 281–295.  https://doi.org/10.1007/s00787-010-0092-x.CrossRefGoogle Scholar
  54. Ronald, A., Larsson, H., Anckarsäter, H., & Lichtenstein, P. (2014). Symptoms of autism and ADHD: A Swedish twin study examining their overlap. Journal of Abnormal Psychology, 123(2), 440.CrossRefPubMedGoogle Scholar
  55. Ronald, A., Simonoff, E., Kuntsi, J., Asherson, P., & Plomin, R. (2008). Evidence for overlapping genetic influences on autistic and ADHD behaviours in a community twin sample. Journal of Child Psychology and Psychiatry, 49(5), 535–542.  https://doi.org/10.1111/j.1469-7610.2007.01857.x.CrossRefPubMedGoogle Scholar
  56. Rutter, M., Le Couteur, A., & Lord, C. (2003). Autism Diagnostic Interview–Revised (ADI-R). Los Angeles: Western Psychological Services.Google Scholar
  57. Sagvolden, T., Aase, H., Zeiner, P., & Berger, D. (1998). Altered reinforcement mechanisms in attention-deficit/hyperactivity disorder. Behavioural and brain research, 94(1), 61–71.  https://doi.org/10.1016/S0166-4328(97)00170-8.CrossRefGoogle Scholar
  58. Sanders, J., Johnson, K. A., Garavan, H., Gill, M., & Gallagher, L. (2008). A review of neuropsychological and neuroimaging research in autistic spectrum disorders: Attention, inhibition and cognitive flexibility. Research in Autism Spectrum Disorders, 2(1), 1–16.CrossRefGoogle Scholar
  59. Sanislow, C. A., Pine, D. S., Quinn, K. J., Kozak, M. J., Garvey, M. A., Heinssen, R. K., & Cuthbert, B. N. (2010). Developing constructs for psychopathology research: research domain criteria. Journal of Abnormal Psychology, 119(4), 631–639.  https://doi.org/10.1037/a0020909.CrossRefPubMedGoogle Scholar
  60. Semrud-Clikeman, M., Walkowiak, J., Wilkinson, A., & Butcher, B. (2010). Executive functioning in children with Asperger syndrome, ADHD-combined type, ADHD-predominately inattentive type, and controls. Journal of Autism and Developmental Disorders, 40(8), 1017–1027.  https://doi.org/10.1007/s10803-010-0951-9.CrossRefPubMedGoogle Scholar
  61. Sinzig, J., Bruning, N., Morsch, D., & Lehmkuhl, G. (2008). Attention profiles in autistic children with and without comorbid hyperactivity and attention problems. Acta Neuropsychiatrica, 20(4), 207–215.CrossRefPubMedGoogle Scholar
  62. Unsworth, N., & Engle, R. W. (2007). The nature of individual differences in working memory capacity: active maintenance in primary memory and controlled search from secondary memory. Psychological Review, 114(1), 104–132.  https://doi.org/10.1037/0033-295X.114.1.104.CrossRefPubMedGoogle Scholar
  63. van der Meer, J. M., Oerlemans, A. M., van Steijn, D. J., Lappenschaar, M. G., de Sonneville, L. M., Buitelaar, J. K., & Rommelse, N. N. (2012). Are autism spectrum disorder and attention-deficit/hyperactivity disorder different manifestations of one overarching disorder? Cognitive and symptom evidence from a clinical and population-based sample. Journal of the American Academy of Child and Adolescent Psychiatry, 51(11), 1160–1172 e1163.  https://doi.org/10.1016/j.jaac.2012.08.024.CrossRefPubMedGoogle Scholar
  64. van Mourik, R., Oosterlaan, J., & Sergeant, J. A. (2005). The Stroop revisited: a meta-analysis of interference control in AD/HD. Journal of Child Psychology and Psychiatry, 46(2), 150–165.  https://doi.org/10.1111/j.1469-7610.2004.00345.x.CrossRefPubMedGoogle Scholar
  65. Voss, A., & Voss, J. (2007). Fast-dm: a free program for efficient diffusion model analysis. Behavior Research Methods, 39(4), 767–775.  https://doi.org/10.3758/BF03192967.CrossRefPubMedGoogle Scholar
  66. Willcutt, E. G., Doyle, A., Nigg, J. T., Faraone, S. V., & Pennington, B. F. (2005). Validity of the executive function theory of attention-deficit/hyperactivity disorder: A meta-analytic review. Biological Psychiatry, 57(11), 1336–1346.  https://doi.org/10.1016/j.biopsych.2005.02.006.CrossRefPubMedGoogle Scholar
  67. Wilson, V. B., Mitchell, S. H., Musser, E. D., Schmitt, C. F., & Nigg, J. T. (2011). Delay discounting of reward in ADHD: application in young children. Journal of Child Psychology and Psychiatry, 52(3), 256–264.  https://doi.org/10.1111/j.1469-7610.2010.02347.x.CrossRefPubMedGoogle Scholar
  68. Yerys, B. E., Kenworthy, L., Jankowski, K. F., Strang, J., & Wallace, G. L. (2013). Separate components of emotional go/no-go performance relate to autism versus attention symptoms in children with autism. Neuropsychology, 27(5), 537.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Sarah L. Karalunas
    • 1
    • 2
  • Elizabeth Hawkey
    • 2
  • Hanna Gustafsson
    • 1
  • Meghan Miller
    • 3
  • Marybeth Langhorst
    • 2
  • Michaela Cordova
    • 2
  • Damien Fair
    • 1
    • 2
    • 4
  • Joel T. Nigg
    • 1
    • 2
  1. 1.Department of PsychiatryOregon Health & Science UniversityPortlandUSA
  2. 2.Department of Behavioral NeuroscienceOregon Health & Science UniversityPortlandUSA
  3. 3.Department of Psychiatry & Behavioral Sciences and MIND InstituteUniversity of California, DavisSacramentoUSA
  4. 4.Advanced Imaging Research CenterOregon Health & Science UniversityPortlandUSA

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