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

Volumn 49, Issue 4, 2010, Pages 345-355

  Sonuga Barke, Edmund ^a,b   Bitsakou, Paraskevi ^a   Thompson, Margaret ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

ADHD; delay aversion; heterogeneity; inhibitory control; timing

Indexed keywords

ADOLESCENT; ARTICLE; ATTENTION DEFICIT DISORDER; CHILD; CONTROLLED STUDY; CORRELATION ANALYSIS; DISSOCIATION; FEMALE; GENETIC HETEROGENEITY; HUMAN; INTELLIGENCE QUOTIENT; MAJOR CLINICAL STUDY; MALE; MENTAL FUNCTION; NEUROPSYCHOLOGICAL TEST; NEUROPSYCHOLOGY; PRIORITY JOURNAL; PSYCHOLOGIC ASSESSMENT; PSYCHOLOGIC TEST; SIBLING; TASK PERFORMANCE; WORKING MEMORY;

ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; CHILD; COGNITION; HUMANS; INHIBITION (PSYCHOLOGY); INTELLIGENCE TESTS; MEMORY, SHORT-TERM; MODELS, NEUROLOGICAL; MODELS, PSYCHOLOGICAL; MOTIVATION; NEUROPSYCHOLOGICAL TESTS; NEUROPSYCHOLOGY; SIBLINGS; TIME PERCEPTION;

EID: 77949658571     PISSN: 08908567     EISSN: 15275418     Source Type: Journal    
DOI: 10.1097/00004583-201004000-00009     Document Type: Article

References (71)

1. Nigg J.T. Neuropsychologic theory and findings in attention-deficit/hyperactivity disorder: the state of the field and salient challenges for the coming decade. Biol Psychiatry 57 (2005) 1424-1435
2. Willcutt E.G., Doyle A.E., Nigg J.T., Faraone S.V., and Pennington B.F. Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry 57 (2005) 1336-1346
3. Bitsakou P., Psychogiou L., Thompson M., and Sonuga-Barke E. Inhibitory Deficits in Attention Deficit Hyperactivity Disorder are Independent of Basic Processing Efficiency and IQ. J Neur Trans. 115 (2008) 261-268
4. Rapport M.D., Bolden J., Kofler M.J., Sarver D.E., Raiker J.S., and Alderson R.M. Hyperactivity in boys with attention-deficit/hyperactivity disorder (ADHD): a ubiquitous core symptom or manifestation of working memory deficits?. J Abnorm Child Psychol. 37 (2009) 521-534
5. Banaschewski T., Ruppert S., Tannock R., et al. Colour perception in ADHD. J Child Psychol Psychiatry 47 (2006) 568-572
6. Coghill D.R., Rhodes S.M., and Matthews K. The neuropsychological effects of chronic methylphenidate on drug-naïve boys with attention-deficit/hyperactivity disorder. Biol Psychiatry 62 (2007) 954-962
7. Toplak M.E., and Dockstader C Tannock R. Temporal information processing in ADHD: findings to date and new methods. J Neurosci Methods 151 (2006) 15-29
8. Luman M., Oosterlaan J., and Sergeant J.A. The impact of reinforcement contingencies on AD/HD: a review and theoretical appraisal. Clin Psychol Rev. 25 (2005) 183-213
9. Sergeant J.A., Willcutt E., and Nigg J. How clinically functional are executive function measures of ADHD?. In: Shaffer D., Leibenluft E., Rohde L.A., Sirovatka P., and Regier D.A. (Eds). Externalizing Disorders of Childhood: Refining the Research Agenda for DSM-V (2007), American Psychiatric Association, Arlington, VA
10. Nigg J.T., Willcutt E.G., Doyle A.E., and Sonuga-Barke E.J.S. Causal heterogeneity in attention-deficit/hyperactivity disorder: do we need neuropsychologically impaired subtypes?. Biol Psychiatry 57 (2005) 1224-1230
11. Sonuga-Barke E.J., Sergeant J., Nigg J., and Willcutt E. Executive dysfunction and delay aversion in ADHD: nosological and diagnostic implications. Child Adolesc Psychiatr Clin North Am. 17 (2008) 367-384
12. Sonuga-Barke E.J. Psychological heterogeneity in AD/HD-a dual pathway model of behaviour and cognition. Behav Brain Res. 130 (2002) 29-36
13. Sonuga-Barke E.J. The dual pathway model of AD/HD: an elaboration of neuro-developmental characteristics. Neurosci Biobehav Rev. 27 (2003) 593-604
14. Sonuga-Barke E.J. Causal models of attention-deficit/hyperactiviy disorder: from common simple deficits to multiple developmental pathways. Biol Psychiatry 57 (2005) 1231-1238
15. Marco R., Miranda A., Schlotz W., et al. Delay and choice in ADHD: a test of the delay aversion hypothesis. Neuropsychology 23 (2009) 367-380
16. Solanto M.V., Abikoff H., Sonuga-Barke E., et al. 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. J Abnorm Child Psychol. 29 (2001) 215-228
17. Sonuga-Barke E.J., De Houwer J., De Ruiter K., Ajzenstzen M., and Holland S. AD/HD and the capture of attention by briefly exposed delay-related cues: evidence from a conditioning paradigm. J Chid Psychol Psychiatry 44 (2003) 1-11
18. Thorell L.B. Do delay aversion and executive function deficits make distinct contributions to the functional impact of ADHD symptoms?. A study of early academic skill deficits. J Child Psychol Psychiatry 14 (2007) 1061-1070
19. Campbell S.B., and von Stauffenberg C. Delay and inhibition as early predictors of ADHD symptoms in third grade. J Abnorm Child Psychol. 37 (2009) 1-15
20. Van den Bergh F.S., Bloemarts E., Groenink L., Olivier B., and Oosting R.S. Delay aversion: effects of 7-OH-DPAT, 5-HT1A/B-receptor stimulation and D-cycloserine. Pharmacol Biochem Behav. 85 (2006) 736-743
21. Wåhlstedt C., Thorell L.B., and Bohlin G. Heterogeneity in ADHD: neuropsycholgical pathways, comorbidity and symptom domain. J Abnorm Child Psychol. 37 (2009) 551-564
22. Koch G., Brusal L., Carrillo F., et al. Cerebellar magnetic stimulation decreases-inducd dyskinesias in Parkinson disease. Neurology 73 (2009) 113-119
23. Shih L.Y., Kuo W.J., Yeh T.C., Tzeng O.J., and Hsieh J.C. Common neural mechanisms for explicit timing in the sub-second range. Neuroreport 20 (2009) 897-901
24. Neufang S., Fink G.R., Herpetz-Dahlmann B., Willmes K., and Konrad K. Developmental changes in neural activation and psychphysiological interaction patterns of brain regions associated with interference control and time perception. Neuroimage 43 (2008) 399-409
25. Toplak M.E., Rucklidge J.J., Hetherington R., John S.C.F., and Tannock R. Time perception deficits in attention-deficit/hyperactivity disorder and comorbid reading difficulties in child and adolescent samples. J Child Psychol Psychiatry 44 (2003) 888-903
26. Barkley R.A., Koplowitz S., Anderson T., and McMurray M.B. Sense of time in children with ADHD: effects of duration, distraction, and stimulant medication. J Internat Neuropsychol Soc. 3 (1997) 359-369
27. Barkley R.A., Murphy K.R., and Bush T. Time perception and reproduction in young adults with attention deficit hyperactivity disorder. Neuropsychology 15 (2001) 351-360
28. Rommelse N.N.J., Oosterlaan J., Buitelaar J., Faraone S.V., and Sergeant J.A. Time reproduction in children with ADHD and their nonaffected siblings. J Am Child Adolesc Psychiatry 46 (2007) 582-590
29. Rubia K., Noorloos J., Smith A., Gunning B., and Sergeant J. Motor timing deficits in community and clinical boys with hyperactivity behavior: the effect of methylphenidate on motor timing. J Abn Child Psychol. 31 (2003) 301-313
30. Smith A., Taylor E., Rogers J.W., Newman S., and Rubia K. Evidence for a pure time perception deficit in children with ADHD. J Child Psychol Psychiatry 43 (2002) 529-542
31. Yang B., Chan R.C.K., Zou X., et al. Time perception deficit in children with ADHD. Brain Res. 1170 (2009) 90-96
32. Ben-Pazi H., Gross-Tsur V., Bergman H., and Shalev R.S. Abnormal rhythmic motor response in children with attention-deficit-hyperactivity disorder. Dev Med Child Neurol. 45 (2003) 743-745
33. Rommelse N.N.J., Altink M.E., Oosterlaan J., et al. Speed, variability, and timing on motor output in ADHD: which measures are useful for endophenotypic research?. Behav Gen. 38 (2008) 121-132
34. Rubia K., Taylor A., Taylor E., and Sergeant J. Synchronization, anticipation, and consistency in motor timing of children with dimensionally defined attention deficit hyperactivity behavior. Percept Mot Skills 89 (1999) 1237-1258
35. Rubia K., Halari R., Christakou A., and Taylor E. Impulsiveness as a timing disturbance: neurocognitive abnormalities in attention-deficit hyperactivity disorder during temporal processes and normaliztion iwht methylphenidate. Phil Trans R Soc Lond B Biol Sci. 364 (2009) 1919-1931
36. Coghill D., Nigg J., Rothenberger A., Sonuga-Barke E.J., and Tannock R. Whither causal models in the neuroscience of ADHD?. Dev Sci. 8 (2005) 105-114
37. Swanson J.M., Kinsbourne M., Nigg J., et al. Etiologic subtypes of attention-deficit/hyperactivity disorder: brain imaging, molecular genetic and environmental factors and the dopamine hypothesis. Neuropsychol Rev. 17 (2007) 39-59
38. Gottesman I.I., and Gould T.D. The endophenotype concept in psychiatry: etymology and strategic intentions. Am J Psychiatry 160 (2003) 636-645
39. Waldman I.D. Statistical approaches to complex phenotypes: evaluating neuropsychological endophenotypes for attention-deficit/hyperactivity disorder. Biol Psychiatry 57 (2005) 1347-1356
40. Schachar R.J., Crosbie J., Barr C.L., et al. Inhibition of motor responses in siblings concordant and discordant for attention deficit hyperactivity disorder. Am J Psychiatry 162 (2005) 1076-1082
41. Rommelse N.N.J., Altink M.E., Oosterlaan J., Buschgens C.J.M., Buitelaar J., and Sergeant J.A. Support for an independent familial segregation of executive and intelligence endophenotypes in ADHD families. Psychol Med. 38 (2008) 1595-1606
42. Himpel S., Banaschewski T., Gruttner A., et al. Duration discrimination in the range of milliseconds and seconds in children with ADHD and their unaffected siblings. Psychol Med. 6 (2009) 1-7
43. Slaats-Willemse D., de Sonneville L., Swaab-Barneveld H., and Buitelaar J. Motor flexibility problems as a marker for genetic susceptibility to ADHD. Biol Psychiatry 58 (2005) 233-238
44. Bitsakou P., Psychogiou L., Thompson M., and Sonuga-Barke E. Delay aversion in attention deficit/hyperactivity disorder (ADHD): an empirical investigation of the broader phenotype. Neuropsychologia 47 (2009) 446-456
45. Toplak M.E., and Tannock R. Tapping and anticipation performance in attention deficit hyperactivity disorder. Percept Mot Skills 100 (2005) 659-675
46. Carelli M.G., Forman H., and Mantyla T. Sense of time and executive functioning in children and adults. Child Neuropsychol. 14 (2008) 372-386
47. Barkley R.A. Behavioural inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull. 121 (1997) 65-94
48. Engelhardt P.E., Nigg J.T., Carr L.A., and Ferreira F. Cognitive inhibition and working memory in attention-deficit hyperactivity disorder. J Abnorm Psychol. 117 (2008) 591-605
49. Kasselimis D.S., Margarity M., and Vlachos F. Cerebellar function, dyslexia and articulation speed. Child Neuropsychol. 14 (2008) 303-313
50. Ramus F., Pidgeon E., and Frith U. The relationship between motor control and phonology in dyslexic children. J Child Psychol Psychiatry 44 (2003) 712-722
51. Brookes K., Xu X., Chen W., et al. The analysis of 51 genes in DSM-IV combined type attention deficit hyperactivity disorder: association signals in DRD4, DAT1 and 16 other genes. Mol Psychiatry 11 (2006) 934-953
52. Taylor E., Sandberg G., Thorley G., and Giles S. The epidemiology of childhood hyperactivity. Maudsley Monograph No. 33 (1991), Oxford University Press, Oxford
53. Goodman R. The Strengths and Difficulties Questionnaire: a research note. J Child Psychol Psychiatry 38 (1997) 581-586
54. Logan G.D., Schachar R.J., and Tannock R. Impulsivity and inhibitory control. Psychol Sci. 8 (1997) 60-64
55. Hogan A.M., Vergha-Khadem F., Kirkham F.J., and Baldeweg T. Maturation of action monitoring from adolescents to adulthood: an ERP study. Dev Sci. 8 (2005) 525-534
56. Kuntsi J., Oosterlaan J., and Stevenson J. Psychological mechanisms in hyperactivity: I. Response inhibition deficit, working memory impairment, delay aversion, or something else?. J Child Psychol Psychiatry 42 (2001) 199-210
57. Bitsakou P., Antrop I., Wiersema J.R., and Sonuga-Barke E.J.S. Probing the limits of delay intolerance: preliminary young adult data from the Delay Frustration Task (DeFT). J Neurosci Methods 151 (2006) 38-44
58. Sonuga-Barke E.J., and Taylor E. The effect of delay on hyperactive and non-hyperactive children's response times: a research note. J Child Psychol Psychiatry 33 (1992) 1091-1096
59. Wetherill G.B., and Levitt H. Sequential estimation of points on a psychological function. Br J Math Stat Psychol. 18 (1965) 1-10
60. rd ed.) (1991), Psychological Corporation, San Antonio, TX
61. Torgesen J.K., Wagner R.K., and Rashotte C.A. Test of word reading efficacy (TOWRE) (1999), Pro-ed, Austin, TX
62. Sattler J.M. Assessment of children: WISC-III and WPPSI-R Supplement (1992), J. M. Sattler, San Diego, CA
63. Bidwell L.C., Willcutt E.G., DeFries J.C., and Pennington B.F. Testing for neuropsychological endophenotypes in siblings discordant for attention-deficit/hyperactivity disorder. Biol Psychiatry 62 (2007) 991-998
64. Nigg J.T., Blaskey L., Stawicki J., and Sachek J. Evaluating the endophenotype model of ADHD neuropsychological deficit: results for parents and siblings of children with DSM-IV ADHD combined and inattentive subtypes. J Abnorm Psychol. 113 (2004) 614-625
65. Slaats-Willemse D., Swaab-Barneveld H., de Sonneville L., van der Meulen E., and Buitelaar J. Deficient response inhibition as a cognitive endophenotype of ADHD. J Am Acad Child Adolesc Psychiatry 42 (2003) 1242-1248
66. Waldman I.D., Nigg J.T., Gizer I.R., Park L., Rappley M.D., and Friderici K. The adrenergic receptor α-2A gene (ADRA2A) and neuropsychological executive functions as putative endophenotypes for childhood ADHD. Cogn Aff Behav Neurosci. 6 (2006) 18-30
67. Doyle A.E., Biederman J., Seidman L.J., Reske-Nielsen J.J., and Faraone S. Neuropsychological functioning in relatives of girls with and without ADHD. Psychol Med. 35 (2005) 1121-1132
68. Andreou P., Neale B.M., Chen W., Christiansen H., Gabriels I., Heise A., et al. Reaction time performance in ADHD: improvement under fast-incentive condition and familial effects. Psychol Med. 31 (2007) 1-13
69. Kuntsi J., Rogers H., Swinard G., Rörger N., van der Meere J., Rijsdijk F., and Asherson P. Reaction time, inhibition, working memory and 'delay aversion' performance: genetic influences and their interpretation. Psychol Med 36 (2006) 613-1624
70. Sonuga-Barke E.J.S., Wiersema J.R., van der Meere J.J., and Roeyers H. Context dependent dynamic models of attention deficit/hyperactivity disorder: differentiating common and unique elements of the state regulation deficit and delay aversion models. Neuropsychol Rev (2009) In press
71. Markomichali P., Donnelly N., and Sonuga-Barke E. Cognitive training for attention, inhibition and working memory deficits: a potential treatment for ADHD?. Advanc ADHD 3 (2009) 89-96