Journal of Abnormal Child Psychology

, Volume 37, Issue 4, pp 551–564 | Cite as

Heterogeneity in ADHD: Neuropsychological Pathways, Comorbidity and Symptom Domains

  • Cecilia Wåhlstedt
  • Lisa B. Thorell
  • Gunilla Bohlin


The aim of the present study was to investigate different neuropsychological impairments and comorbid behavioral problems in relation to symptoms of Attention-Deficit/Hyperactivity Disorder (ADHD), studying the independent effects of different functions as well as specific relations to symptoms of hyperactivity/impulsivity and inattention. A community-based sample of school children (n = 182; the higher end of the ADHD symptom range was oversampled) completed neuropsychological tasks designed to measure executive function (EF), state regulation and delay aversion. Behavioral symptoms were measured through parental and teacher ratings of the DSM-IV criteria for ADHD and Oppositional Defiant Disorder (ODD). Both categorical and dimensional analyses were used to acquire a deeper understanding of ADHD. The results supported the notion that EF and state regulation constitute independent pathways to ADHD, primarily to symptoms of inattention. In addition, the present study points to the importance of viewing ADHD as a heterogeneous condition also with regard to the differential impact of neuropsychological functioning and comorbidity on different ADHD symptom groups and the two ADHD symptom domains.


ADHD Heterogeneity Hyperactivity Inattention Neuropsychological factors Comorbidity 


  1. Alderson, R. M., Rapport, M. D., & Kofler, M. J. (2007). Attention-deficit/hyperactivity disorder and behavioral inhibition: a meta-analytic review of the stop-signal paradigm. Journal of Abnormal Child Psychology, 35, 745–758.PubMedCrossRefGoogle Scholar
  2. American Psychiatric Association (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: Author.Google Scholar
  3. Barkley, R. A. (1997). ADHD and the nature of self-control. New York: Guilford.Google Scholar
  4. Barkley, R. A. (1998). Attention-Deficit Hyperactivity Disorder. A handbook for diagnosis and treatment (2ndnd ed.). New York: Guilford.Google Scholar
  5. Bauermeister, J. J., Shrout, P. E., Ramirez, R., Bravo, M., Alegria, M., Martinez-Taboas, A., et al. (2007). ADHD Correlates, comorbidity, and impairment in community and treated samples of children and adolescents. Journal of Abnormal Child Psychology, 35, 883–898. doi:10.1007/s10802-007-9141-4.PubMedCrossRefGoogle Scholar
  6. Berlin, L., & Bohlin, G. (2002). Response inhibition, hyperactivity and conduct problems among preschool children. Journal of Clinical Child and Adolescent Psychology, 31, 242–251.PubMedGoogle Scholar
  7. Berlin, L., Bohlin, G., Nyberg, L., & Janols, L.-O. (2004). How well do measures of inhibition and other executive functions discriminate between children with ADHD and controls? Child Neuropsychology, 1, 1–13.Google Scholar
  8. Berwid, O. G., Curko Kera, E. A., Marks, D. J., Santra, A., Bender, H. A., & Halperin, J. M. (2005). Sustained attention and response inhibition in young children at risk for attention deficit/hyperactivity disorder. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 46, 1219–1229. doi:10.1111/j.1469-7610.2005.00417.x.PubMedCrossRefGoogle Scholar
  9. Biederman, J. (2005). Attention-deficit/hyperactivity disorder: a selective overview. Biological Psychiatry, 57, 1215–1220. doi:10.1016/j.biopsych.2004.10.020.PubMedCrossRefGoogle Scholar
  10. Bitsakou, P., Psychogiou, L., Thompson, M., & Sonuga-Barke, E. J. S. (2008). Inhibitory deficits in attention-deficit/hyperactivity disorder are independent of basic processing efficiency and IQ. Journal of Neural Transmission, 115, 261–268. doi:10.1007/s00702-007-0828-z.PubMedCrossRefGoogle Scholar
  11. Brocki, K. C., & Bohlin, G. (2006). Developmental change in the relation between executive functions and symptoms of ADHD and co-occurring behaviour problems. Infant and Child Development, 15, 19–40. doi:10.1002/icd.413.CrossRefGoogle Scholar
  12. Brocki, K. C., Nyberg, L., Thorell, L. B., & Bohlin, G. (2007). Early concurrent and longitudinal symptoms of ADHD and ODD: relations to different types of inhibitory control and working memory. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 48, 1033–1041. doi:10.1111/j.1469-7610.2007.01811.x.PubMedCrossRefGoogle Scholar
  13. Castellanos, F. X., & Tannock, R. (2002). Neuroscience of attention-deficit/hyperactivity disorder: the search for endophenotypes. Nature Reviews. Neuroscience, 3, 617–628.PubMedGoogle Scholar
  14. Castellanos, F. X., Sonuga-Barke, E. J. S., Milham, M. P., & Tannock, R. (2006). Characterizing cognition in ADHD: beyond executive dysfunction. Trends in Cognitive Sciences, 10, 117–123. doi:10.1016/j.tics.2006.01.011.PubMedCrossRefGoogle Scholar
  15. Chen, L. A., Welsh, A. H., & Chan, W. (2001). Estimators for the linear regression model based on Winsorized observations. Statistica Sinica, 11, 147–172.Google Scholar
  16. Chhabildas, N. A., Pennington, B. F., & Willcutt, E. G. (2001). A comparison of the cognitive deficit in the DSM-IV subtypes of ADHD. Journal of Abnormal Child Psychology, 9, 28–32.Google Scholar
  17. Clarke, S. D., Kohn, M. R., Hermens, D. F., Rabbinge, M., Clark, C. R., Gordon, E., & Williams, L. M. (2007). Distinguishing symptom profiles in adolescent ADHD using an objective cognitive test battery. International Journal of Adolescent Medicine and Health, 19, 355–367.PubMedGoogle Scholar
  18. Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2ndnd ed.). Hillsdale, NJ: Erlbaum.Google Scholar
  19. Dalen, L., Sonuga-Barke, E. J. S., Hall, M., & Remington, B. (2004). Inhibitory deficits, delay aversion and preschool AD/HD: implications for the dual pathway model. Neural Plasticity, 11, 1–11. doi:10.1155/NP.2004.1.PubMedCrossRefGoogle Scholar
  20. DuPaul, G. J., Power, T. J., Anastopoulos, A. D., & Reid, R. (1998). ADHD rating Scale IV. Checklists, norms, and clinical interpretation. New York: Guilford.Google Scholar
  21. Epstein, J. N., Erkanli, A., Conners, C. K., Klaric, J., Costello, J. E., & Angold, A. (2003). Relations between continuous performance test performance measures and ADHD behaviors. Journal of Abnormal Child Psychology, 31, 543–554. doi:10.1023/A:1025405216339.PubMedCrossRefGoogle Scholar
  22. Faraone, S. V., Biederman, J., Weber, W., & Russell, R. L. (1998). Psychiatric, neuropsychological, and psychosocial features of DSM-IV subtypes of attention-deficit/hyperactivity disorder: results from a clinically reffered sample. Journal of the American Academy of Child and Adolescent Psychiatry, 37, 185–193.PubMedCrossRefGoogle Scholar
  23. Friedman, N. P., Haberstick, B. C., Willcutt, E. G., Miyake, A., Young, S. E., Corley, R. P., & Hewitt, J. K. (2007). Greater attention problems during childhood predict poorer executive functioning in late adolescence. Psychological Science, 18, 893–900. doi:10.1111/j.1467-9280.2007.01997.x.PubMedCrossRefGoogle Scholar
  24. Gaub, M., & Carlson, C. L. (1997). Behavioral characteristics of DSM-IV ADHD subtypes in a school-based population. Journal of Abnormal Child Psychology, 25, 103–111. doi:10.1023/A:1025775311259.PubMedCrossRefGoogle Scholar
  25. Gerstadt, C. L., Hong, Y. J., & Diamond, A. (1994). The relationship between cognition and action: performance of children 3 1/2–7 years old on a Stroop-like day-night test. Cognition, 53, 129–153. doi:10.1016/0010-0277(94)90068-X.PubMedCrossRefGoogle Scholar
  26. Geurts, H. M., Verté, S., Oosterlaan, J., Roeyers, H., & Sergeant, J. A. (2005). ADHD subtypes: do they differ in their executive functioning profile? Archives of Clinical Neuropsychology, 20, 457–477. doi:10.1016/j.acn.2004.11.001.PubMedCrossRefGoogle Scholar
  27. Groth-Marnat, G. (1997). Handbook of psychological assessment (3rdrd ed.). New York: Wiley and Sons.Google Scholar
  28. Henricsson, X., & Rydell, A.-M. (2006). Children with behavior problems: Development during the first 6 years of school. Infant and Child Development, 15, 347–366.CrossRefGoogle Scholar
  29. Huang-Pollock, C. L., Mikami, A. Y., Pfiffner, L., & McBurnett, K. (2007). ADHD subtype differences in motivational respnsivity but not inhibitory control: evidence from a reward-based variation of the stop signal paradigm. Journal of Clinical Child and Adolescent Psychology, 36, 127–136.PubMedGoogle Scholar
  30. Johnson, K. A., Kelly, S. P., Bellgrove, M. A., Barry, E., Cox, M., Gill, M., & Robertson, I. H. (2007). Response variability in attention deficit hyperactivity disorder: evidence for neuropsychological heterogeneity. Neuropsychologia, 45, 630–638. doi:10.1016/j.neuropsychologia.2006.03.034.PubMedCrossRefGoogle Scholar
  31. Kalff, A. C., De Sonneville, L. M. J., Hurks, P. P. M., Hendriksen, J. G. M., Kroes, M., Feron, F. J. M., Steyaert, J., et al. (2005). Speed, speed variability, and accuracy of information processing in 5 to 6 year-old children at risk of ADHD. Journal of the International Neuropsychological Society, 11, 173–183. doi:10.1017/S1355617705050216.PubMedCrossRefGoogle Scholar
  32. Klein, C., Wendling, K., Huettner, P., Ruder, H., & Peper, M. (2006). Intra-subject variability in attention-deficit hyperactivity disorder. Biological Psychiatry, 60, 1088–1097. doi:10.1016/j.biopsych.2006.04.003.PubMedCrossRefGoogle Scholar
  33. Kraemer, H. C., Noda, A., & O’Hara, R. (2004). Categorical versus dimensional approaches to diagnosis: methodological challenges. Journal of Psychiatric Research, 38, 17–25. doi:10.1016/S0022-3956(03)00097-9.PubMedCrossRefGoogle Scholar
  34. Kuntsi, J., Oosterlaan, J., & Stevenson, J. (2001). Psychological mechanisms in hyperactivity: I response inhibition deficit, working memory impairment, delay aversion, or something else? Journal of Child Psychology and Psychiatry, and Allied Disciplines, 42, 199–210. doi:10.1017/S0021963001006709.PubMedCrossRefGoogle Scholar
  35. Kuntsi, J., Andreou, P., Ma, J., Börger, N. A., & Van der Meere, J. J. (2005). Testing assumptions for endophenotype studies in ADHD: Reliability and validity of tasks in a general population sample. BMC Psychiatry, 5, 40. doi:10.1186/1471-244X-5-40.PubMedCrossRefGoogle Scholar
  36. Levy, F., Hay, D. A., McStephen, M., Wood, C., & Waldman, I. (1997). Attention-deficit hyperactivity disorder: a category or a continuum? Genetic analysis of a large-scale twin study. Journal of the American Academy of Child and Adolescent Psychiatry, 36, 737–744. doi:10.1097/00004583-199706000-00009.PubMedCrossRefGoogle Scholar
  37. Lijffijt, M., Kenemans, J. L., Verbaten, M. N., & van Engeland, H. (2005). A meta-analytic review of stopping performance in attention-deficit/hyperactivity disorder: deficient inhibitory motor control? Journal of Abnormal Psychology, 2, 216–222. doi:10.1037/0021-843X.114.2.216.CrossRefGoogle Scholar
  38. Malmberg, M., Rydell, A.-M., & Smedje, H. (2003). Validity of the Swedish version of the strengths and difficulties questionnaire (SDQ-Swe). Nordic Journal of Psychiatry, 57, 357–363. doi:10.1080/08039480310002697.PubMedCrossRefGoogle Scholar
  39. 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, 377–384. doi:10.1097/01.chi.0000153228.72591.73.PubMedCrossRefGoogle Scholar
  40. Martell, M., Nikolas, M., & Nigg, J. T. (2007). Executive function in adolescents with ADHD. Journal of the American Academy of Child and Adolescent Psychiatry, 46, 1437–1444. doi:10.1097/chi.0b013e31814cf953.CrossRefGoogle Scholar
  41. Massetti, G. M., Lahey, B. B., Pelham, W. E., Loney, J., Ehrhardt, A., Lee, S. S., & Kipp, H. (2008). Academic achievement over 8 years among children who met modified criteria for attention-deficit/hyperactivity disorder at 4-6 years of age. Journal of Abnormal Child Psychology, 36, 399–410. doi:10.1007/s10802-007-9186-4.PubMedCrossRefGoogle Scholar
  42. McInerney, R. J., Hrabok, M., & Kerns, K. A. (2005). The children’s size-ordering task: a new measure of nonverbal working memory. Journal of Clinical and Experimental Neuropsychology, 27, 735–745. doi:10.1081/13803390490918633.PubMedCrossRefGoogle Scholar
  43. Nassauer, K. W., & Halperin, J. M. (2003). Dissociation of perceptual and motor inhibition processes through the use of novel computerized conflict tasks. Journal of the International Neuropsychological Society, 9, 25–30. doi:10.1017/S1355617703910034.PubMedCrossRefGoogle Scholar
  44. Nigg, J. T. (2006). What Causes ADHD? Understanding What Goes Wrong and Why. New York: Guilford.Google Scholar
  45. Nigg, J. T., Willcut, 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, 224–1230. doi:10.1016/j.biopsych.2004.08.025.Google Scholar
  46. Nyberg, L., Bohlin, G., Berlin, L., & Janols, L.-O. (2003). Differentiating type a behaviour and hyperactivity using observed motivation during a reaction time task. Infant and Child Development, 12, 145–158. doi:10.1002/icd.270.CrossRefGoogle Scholar
  47. Nyberg, L., Bohlin, G., & Hagekull, B. (2004). Assessing type A behavior in children: a longitudinal exploration of the overlap between type A behavior and hyperactivity. Scandinavian Journal of Psychology, 45, 145–156. doi:10.1111/j.1467-9450.2004.00389.x.PubMedCrossRefGoogle Scholar
  48. Pasini, A., Paloscia, C., Alessandrelli, R., Porfirio, M. C., & Curatolo, P. (2007). Attention and executive functions profile in drug naive ADHD subtypes. Brain & Development, 29, 400–408. doi:10.1016/j.braindev.2006.11.010.CrossRefGoogle Scholar
  49. Power, T. J., Costigan, T. E., Eiraldi, R. B., & Stephen, S. L. (2004). Variations in anxiety and depression as a function of ADHD subtypes defined by DSM-IV: do subtype differences exist or not? Journal of Abnormal Child Psychology, 32, 27–37. doi:10.1023/B:JACP.0000007578.30863.93.PubMedCrossRefGoogle Scholar
  50. Rabiner, D., & Coie, J. D. (2000). Early attention problems and children’s reading achievement: a longitudinal investigation. Journal of the American Academy of Child and Adolescent Psychiatry, 39, 859–867. doi:10.1097/00004583-200007000-00014.PubMedCrossRefGoogle Scholar
  51. Schatz, D. B., & Rostain, A. L. (2006). ADHD with comorbid anxiety a review of the current litterature. Journal of Attention Disorders, 10, 141–149. doi:10.1177/1087054706286698.PubMedCrossRefGoogle Scholar
  52. Scheres, A., Dijkstra, M., Ainslie, E., Balkan, J., Reynolds, B., Sonuga-Barke, E., & Castellanos, F. X. (2006). Temporal and probabilistic discounting of rewards in children and adolescents: effects of age and ADHD symptoms. Neuropsychologia, 44, 2092–2103. doi:10.1016/j.neuropsychologia.2005.10.012.PubMedCrossRefGoogle Scholar
  53. Scheres, A., & Sumiya, L. M. (2008). Temporal reward discounting and ADHD: task and symptom specific effects. Journal of Neural Transmission, 115, 221–226. doi:10.1007/s00702-007-0813-6.PubMedCrossRefGoogle Scholar
  54. Sergeant, J. (2000). The cognitive-energetic model: an empirical approach to attention-deficit hyperactivity disorder. Neuroscience and Biobehavioral Reviews, 24, 7–12. doi:10.1016/S0149-7634(99)00060-3.PubMedCrossRefGoogle Scholar
  55. Sergeant, J. A. (2005). Modeling attention-deficit/hyperactivity disorder: a critical appraisal of the cognitive-energetic model. Biological Psychiatry, 57, 1248–1255. doi:10.1016/j.biopsych.2004.09.010.PubMedCrossRefGoogle Scholar
  56. Sergeant, J. A., Geurts, H., Huijbregts, S., Scheres, A., & Oosterlaan, J. (2003). The top and the bottom of ADHD: a neuropsychological perspective. Neuroscience and Biobehavioral Reviews, 27, 583–592. doi:10.1016/j.neubiorev.2003.08.004.PubMedCrossRefGoogle Scholar
  57. Simpson, A., & Riggs, K. J. (2005). Factors responsible for performance on the day-night task: response set or semantics? Developmental Science, 8(4), 360–371. doi:10.1111/j.1467-7687.2005.00424.x.PubMedCrossRefGoogle Scholar
  58. Solanto, M. V., Abikoff, H., Sonuga-Barke, E., Schachar, R., Logan, G. D., Wigal, T., et al. (2001). The ecological validity of delay aversion and response inhibition as measures of impulsivity in AD/HD: a supplement to the nimh multimodal treatment study of AD/HD. Journal of Abnormal Child Psychology, 29, 215–228. doi:10.1023/A:1010329714819.PubMedCrossRefGoogle Scholar
  59. Solanto, M. V., Gilbert, S. N., Raj, A., Zhu, J., Pope-Boyd, S., Stepak, B., Vail, L., & Newcorn, J. H. (2007). Neurocognitive functioning in AD/HD, Predominantly inattentive and combined subtypes. Journal of Abnormal Child Psychology, 35, 729–744. doi:10.1007/s10802-007-9123-6.PubMedCrossRefGoogle Scholar
  60. Sonuga-Barke, E. J. S. (2003). The dual pathway model of AD/HD: An elaboration of neuro-developmental characteristics. Neuroscience and Biobehavioral Reviews, 27, 593–604. doi:10.1016/j.neubiorev.2003.08.005.PubMedCrossRefGoogle Scholar
  61. Sonuga-Barke, E. J. S. (2005). Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biological Psychiatry, 57, 1231–1238. doi:10.1016/j.biopsych.2004.09.008.PubMedCrossRefGoogle Scholar
  62. Sonuga-Barke, E. J. S., Taylor, E., Sembi, S., & Smith, J. (1992). Hyperactivity and delay aversion I: The effect of delay on choice. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 33, 387–398. doi:10.1111/j.1469-7610.1992.tb00874.x.PubMedCrossRefGoogle Scholar
  63. Sonuga-Barke, E. J. S., Dalen, L., & Remington, B. (2003). Do executive deficits and delay aversion make independent contributions to preschool attention-deficit/hyperactivity disorder symptoms? Journal of the American Academy of Child and Adolescent Psychiatry, 42, 1335–1342. doi:10.1097/01.chi.0000087564.34977.21.PubMedCrossRefGoogle Scholar
  64. Sonuga-Barke, E. J. S., Sergeant, J. A., Nigg, J., & Willcutt, E. (2008). Executive dysfunction and delay aversion in attention deficit hyperactivity disorder: nosologic and diagnostic implications. Child and Adolescent Psychiatric Clinics of North America, 17, 367–384. doi:10.1016/j.chc.2007.11.008.PubMedCrossRefGoogle Scholar
  65. Stroop, J. R. (1935). Studies of interference in serial verbal reactions. Journal of Experimental Psychology, 18, 643–662. doi:10.1037/h0054651.CrossRefGoogle Scholar
  66. Tabachnick, B. G., & Fidell, L. S. (2007). Experimental designs using ANOVA. Belmont, CA: Thomson/Brooks/Cole, cop.Google Scholar
  67. Thorell, L. B. (2007). Do delay aversion and executive function deficits make distinct contributions to the functional impact of ADHD symptoms? A study of early academic skill deficits. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 48, 1061–1070. doi:10.1111/j.1469-7610.2007.01777.x.PubMedCrossRefGoogle Scholar
  68. Thorell, L. B., & Wåhlstedt, C. (2006). Executive functioning deficits in relation to symptoms of ADHD and/or ODD in preschool children. Infant and Child Development, 15, 503–518. doi:10.1002/icd.475.CrossRefGoogle Scholar
  69. Trommer, B. L., Hoeppner, J.-A. B., Lorber, R., & Armstrong, K. (1988). The go/no-go paradigm in attention deficit disorder. Annals of Neurology, 24, 610–614. doi:10.1002/ana.410240504.PubMedCrossRefGoogle Scholar
  70. Tucha, L., Tucha, O., Laufkötter, R., Walitza, S., Klein, H. E., & Lange, K. W. (2008). Neuropsychological assessment of attention in adults with different subtypes of attention-deficit/hyperactivity disorder. Journal of Neural Transmission, 115, 269–278. doi:10.1007/s00702-007-0836-z.PubMedCrossRefGoogle Scholar
  71. Van der Meere, J., Marzocchi, G. M., & De Meo, T. (2005). Response inhibition and attention deficit hyperactivity disorder with and without oppositional defiant disorder screened from a community sample. Developmental Neuropsychology, 28, 459–472. doi:10.1207/s15326942dn2801_1.PubMedCrossRefGoogle Scholar
  72. Wechsler, D. (1991). Wechsler Intelligence Scale for Children (3rd ed.) (Psykologiförlaget AB, Stockholm, Trans.) New York: Psychological Corporation.Google Scholar
  73. Welsh, M. C. (2002). Developmental and clinical variations in executive functions. In D. L. Molfese, & V. J. Molfese (Ed.), Developmental variations in learning: Applications to social, executive function, language, and reading skills (pp. 139–185). Mahawah, NJ: Lawrence Erlbaum Associates.Google Scholar
  74. Willcut, E. G., Doyle, A. E., Nigg, J. T., Faraone, S. V., & Pennington, B. F. (2005a). Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biological Psychiatry, 57, 1336–1346. doi:10.1016/j.biopsych.2005.02.006.CrossRefGoogle Scholar
  75. Willcutt, E. G., Brodsky, K., Chhabildas, N., Shanahan, M., Yerys, B., Scott, A., & Pennington, B. F. (2005b). The neuropsychology of ADHD: validity of the executive function hypothesis. In Attention Deficit Hyperactivity Disorder: From Genes to Patients (pp. 185–213). Totowa, NJ: Human.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Cecilia Wåhlstedt
    • 1
  • Lisa B. Thorell
    • 1
    • 2
  • Gunilla Bohlin
    • 1
  1. 1.Department of PsychologyUppsala UniversityUppsalaSweden
  2. 2.Stockholm Brain InstituteStockholmSweden

Personalised recommendations