Abstract
Attention-deficit/hyperactivity disorder (ADHD) often persists into adulthood, albeit with changes in clinical symptoms throughout the life span. Although effect sizes of neuropsychological deficits in ADHD are well established, developmental approaches have rarely been explored and little is yet known about age-dependent changes in cognitive dysfunction from childhood to adulthood. In this cross-sectional study, 20 male children (8–12 years), 20 adolescents (13–16 years), and 20 adults (18–40 years) with ADHD and a matched control group were investigated using six experimental paradigms tapping into different domains of cognitive dysfunction. Subjects with ADHD were more delay-aversive and showed deficits in time discrimination and time reproduction, but they were not impaired in working memory, interference control or time production. Independent of age, the most robust group differences were observed with respect to delay aversion and time reproduction, pointing to persistent dysfunction in the mesolimbic reward circuitry and in the frontal-striatal-cerebellar timing system in subjects with ADHD. Across all tasks, effect sizes were lowest for adolescents with ADHD compared to age-matched controls. Developmental dissociations were found only for simple stimuli comparison, which was particularly impaired in ADHD children. Thus, in line with current multiple-pathway approaches to ADHD, our data suggest that deficits in different cognitive domains are persistent across the lifespan, albeit less pronounced in adolescents with ADHD.
Similar content being viewed by others
References
Albrecht B, Rothenberger A, Sergeant J, Tannock R, Uebel H, Banaschewski T (2008) Interference control in attention-deficit/hyperactivity disorder: differential Stroop effects for colour-naming versus counting. J Neural Transm 115:241–247
Barkley RA (1997) Behavioral inhibition, sustained attention, and executive functions: constructing a unifying theory of ADHD. Psychol Bull 121:65–94
Barkley RA (1998) Attention-deficit hyperactivity disorder: a handbook for diagnosis and treatment, 2nd edn. Guilford Press, New York
Barkley RA, Edwards G, Laneri M, Fletcher K, Metevia L (2001a) Executive functioning, temporal discounting, and sense of time in adolescents with attention deficit hyperactivity disorder (ADHD) and oppositional defiant disorder (ODD). J Abnorm Child Psychol 29:541–556
Barkley RA, Murphy KR, Bush T (2001b) Time perception and reproduction in young adults with attention deficit hyperactivity disorder. Neuropsychology 15:351–360
Bauermeister JJ, Barkley RA, Martinez JV, Cumba E, Ramirez RR, Reina G et al (2005) Time estimation and performance on reproduction tasks in subtypes of children with attention deficit hyperactivity disorder. J Clin Child Adolesc Psychol 34:151–162
Biederman J, Faraone SV, Spencer T, Wilens T, Norman D, Lapey KA, Mick E et al (1993) Patterns of psychiatric comorbidity, cognition, and psychosocial functioning in adults with attention deficit hyperactivity disorder. Am J Psychiatry 150:1792–1798
Biederman J, Mick E, Faraone SV (2000) Age-dependent decline of symptoms of attention deficit hyperactivity disorder: impact of remission definition and symptom type. Am J Psychiatry 157:816–818
Biederman J, Petty CR, Fried R, Doyle AE, Spencer T, Seidman LJ et al (2007) Stability of executive function deficits into young adult years: a prospective longitudinal follow-up study of grown up males with ADHD. Acta Psychiatr Scand 116:129–136
Blasi G, Goldberg TE, Weickert T, Das S, Kohn P, Zoltick B et al (2006) Brain regions underlying response inhibition and interference monitoring and suppression. Eur J Neurosci 23:658–1664
Boonstra AM, Oosterlaan J, Sergeant JA, Buitelaar JK (2005) Executive functioning in adult ADHD: a meta-analytic review. Psychol Med 35:1097–1108
Bunge SA, Ochsner KN, Desmond JE, Glover GH, Gabrieli JD (2001) Prefrontal regions involved in keeping information in and out of mind. Brain 124:2074–2086
Bush G, Frazier JA, Rauch SL, Seidman LJ, Whalen PJ, Jenike MA et al (1999) Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and the Counting Stroop. Biol Psychiatry 45:1542–1552
Carlson CL, Tamm L (2000) Responsiveness of children with attention deficit-hyperactivity disorder to reward and response cost: differential impact on performance and motivation. J Consult Clin Psychol 69:73–83
Castellanos FX, Lee PP, Sharp W, Jeffries NO, Greenstein DK, Clasen LS et al (2002) Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA 288:1740–1748
Conners C, Erhardt D, Sparrow E (1998) The Conners Adult ADHD Rating Scale-Long Version (CAARS-S-L). Multi-Health Systems, Toronto
Conners CK, Epstein JN, Angold A, Klaric J (2003) Continuous performance test performance in a normative epidemiological sample. J Abnorm Child Psychol 31:555–562
Crone EA, Wendelken C, Donohue S, van Leijenhorst L, Bunge SA (2006) Neurocognitive development of the ability to manipulate information in working memory. Proc Natl Acad Sci USA 103:9315–9320
Dige N, Wik G (2005) Adult attention deficit hyperactivity disorder identified by neuropsychological testing. Int J Neurosci 115: 169–183
Doepfner M, Lehmkuhl G (1998) Diagnostic system for mental disorders in child and adolescence according to ICD-10 and DSM-IV (DISYPS-KJ). Huber, Bern
Dowson JH, McLean A, Bazanis E, Toone B, Young S, Robbins TW et al (2004) Impaired spatial working memory in adults with attention-deficit/hyperactivity disorder: comparisons with performance in adults with borderline personality disorder and in control subjects. Acta Psychiatr Scand 110:45–54
Drechsler R, Brandeis D, Foldenyi M, Imhof K, Steinhausen HC (2005) The course of neuropsychological functions in children with attention deficit hyperactivity disorder from late childhood to early adolescence. J Child Psychol Psychiatry 46:824–836
Drechsler R, Rizzo P, Steinhausen HC (2009) Decision making with uncertain reinforcement in children with attention deficit/hyperactivity disorder (ADHD). Child Neuropsychol (in press)
Ernst M, Zametkin AJ, Matochik JA, Jons PH, Cohen RM (1998) DOPA decarboxylase activity in attention deficit hyperactivity disorder adults. A [fluorine-18]fluorodopa positron emission tomographic study. J Neurosci 18:5901–5907
Faraone SV, Biederman J, Mick E (2006) The age-dependent decline of attention deficit hyperactivity disorder: a meta-analysis of follow-up studies. Psychol Med 36:159–165
Fayyad J, De Graaf R, Kessler R, Alonso J, Angermeyer M, Demyttenaere K et al (2007) Cross-national prevalence and correlates of adult attention-deficit hyperactivity disorder. Br J Psychiatry 190:402–409
Garrett A, Penniman L, Epstein JN, Casey BJ, Hinshaw SP, Glover G et al (2008) Neuroanatomical abnormalities in adolescents with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 47:1321–1328
Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A et al (1999) Brain development during childhood and adolescence: a longitudinal MRI study. Nat Neurosci 2:861–863
Gillberg C, Gillberg IC, Rasmussen P, Kadesjö B, Söderström H, Rastam M et al (2004) Co-existing disorders in ADHD–implications for diagnosis and intervention. Eur Child Adolesc Psychiatry 13 Suppl 1:180–192
Halperin JM, Schulz KP (2006) Revisiting the role of the prefrontal cortex in the pathophysiology of attention-deficit/hyperactivity disorder. Psychol Bull 132:560–581
Halperin JM, Trampush JW, Miller CJ, Marks DJ, Newcorn JH (2008) Neuropsychological outcome in adolescents/young adults with childhood ADHD: profiles of persisters, remitters and controls. J Child Psychol Psychiatry 49:958–966
Hervey AS, Epstein JN, Curry JF (2004) Neuropsychology of adults with attention-deficit/hyperactivity disorder: a meta-analytic review. Neuropsychologia 18:485–503
Himpel S, Banaschewski T, Grüttner A, Becker A, Heise A, Üebel A et al (2009) Duration discrimination in the range of milliseconds and seconds in children with ADHD and their unaffected siblings. Psychol Med 39:1745–1751
Homack S, Riccio CA (2004) A meta-analysis of the sensitivity and specificity of the Stroop Color and Word Test with children. Arch Clin Neuropsychol 19:725–743
Ivry R (1996) The representation of temporal information in perception and motor control. Curr Opin Neurobiol 6:851–857
Kaufman J, Birmaher B, Brent D, Rao U, Flynn C, Moreci P et al (1997) Schedule for Affective Disorders and Schizophrenia for School-Age Children-Present and Lifetime Version (K-SADS-PL): initial reliability and validity data. J Am Acad Child Adolesc Psychiatry 36:980–988
Kittler JE, Menard W, Phillips KA (2007) Weight concerns in individuals with body dysmorphic disorder. Eat Behav 8:115–120
Konrad K, Neufang S, Fink GR, Herpertz-Dahlmann B (2007) Long-term effects of methylphenidate on neural networks of attention in children with ADHD: results from a longitudinal functional MRI study. J Am Acad Child Adolesc Psychiatry 46:1633–1641
Levitt H (1971) Transformed up-down methods in psychoacoustics. J Acoust Soc Am 49:467–477
Lijffijt M, Kenemans JL, Verbaten MN, van Engeland H (2005) A meta-analytic review of stopping performance in attention-deficit/hyperactivity disorder: deficient inhibitory motor control? J Abnorm Psychol 114:216–222
Mackie S, Shaw P, Lenroot R, Pierson R, Greenstein DK, Nugent TF et al (2007) Cerebellar development and clinical outcome in attention deficit hyperactivity disorder. Am J Psychiatry 164:647–655
Martel M, Nikolas M, Nigg JT (2007) Executive function in adolescents with ADHD. J Am Acad Child Adolesc Pschiatry 46:1437–1444
Martinussen R, Hayden J, Hogg-Johnson SH, Tannock R (2005) A meta-analysis of working memory impairments in children with attention-deficit/hyperactivity disorder. J Am Acad Child Adolesc Psychiatry 44:377–384
McClure SM, Laibson DI, Loewenstein G, Cohen JD (2004) Separate neural systems value immediate and delayed monetary rewards. Science 306:503–507
McInerney RJ, Kerns KA (2003) Time reproduction in children with ADHD: motivation matters. Child Neuropsychol 9:91–108
McLoughlin G, Albrecht B, Banaschewski T, Rothenberger A, Brandeis D, Asherson P et al (2009) Performance monitoring is altered in adult ADHD: a familial event-related potential investigation. Neuropsychologia 47:3134–3142
Meaux JB, Chelonis JJ (2003) Time perception differences in children with and without ADHD. J Pediatr Health Care 17:64–71
Mullins C, Bellgrove MA, Gill M, Robertson IH (2005) Variability in time reproduction: difference in ADHD combined and inattentive subtypes. J Am Acad Child Adolesc Psychiatry 44:169–176
Neufang S, Fink GR, Herpertz-Dahlmann B, Willmes K, Konrad K (2008) Developmental changes in neural activation and psychophysiological interaction patterns of brain regions associated with interference control and time perception. Neuroimage 43:399–409
Nigg JT (2006) Temperament and developmental psychopathology. J Child Psychol Psychiatry 47:395–422
Nigg JT, Casey BJ (2005) An integrative theory of attention-deficit/hyperactivity disorder based on the cognitive and affective neurosciences. Dev Psychopathol 17:785–806
Nigg JT, Stavro G, Ettenhofer M, Hambrick DZ, Miller T, Henderson JM (2005) Executive functions and ADHD in adults: evidence for selective effects on ADHD symptom domains. J Abnorm Psychol 114:706–717
Pennington BF, Ozonoff S (1996) Executive functions and developmental psychopathology. J Child Psychol Psychiatry 37:51–87
Peterson BS, Kane MJ, Alexander GM, Lacadie C, Skudlarski P, Leung HC et al (2002) An event-related functional MRI study comparing interference effects in the Simon and Stroop tasks. Cogn Brain Res 13:427–440
Plichta MM, Vasic N, Wolf C, Lesch KP, Brummer D, Jacob C et al (2009) Neural hyporesponsiveness and hyperresponsiveness during immediate and delayed reward processing in adult attention-deficit/hyperactivity disorder. Biol Psychiatry 65:7–14
Pliszka SR (1998) Comorbidity of attention-deficit/hyperactivity disorder with psychiatric disorder: an overview. J Clin Psychiatry 59:50–58
Polanczyk G, de Lima MS, Horta BL, Biederman J, Rohde LA (2007) The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am J Psychiatry 164:942–948
Ragland JD, Turetsky BI, Gur RC, Gunning-Dixon F, Turner T, Schroeder L et al (2002) Working memory for complex figures: an fMRI comparison of letter and fractal n-back tasks. Neuropsychology 16:370–379
Retz-Junginger P, Retz W, Blocher D, Weijers HG, Trott GE, Wender PH et al (2002) Wender Utah rating scale. The short-version for the assessment of the attention-deficit hyperactivity disorder in adults. Nervenarzt 73:830–838
Retz-Junginger P, Retz W, Blocher D, Stieglitz RD, Supprian T, Wender PH et al (2003) Reliabilität und Validität der Wender Utah Rating Scale Kurzform. Nervenarzt 74:987–993
Rosler M, Retz W, Retz-Junginger P, Thome J, Supprian T, Nissen T et al (2004) Instrumente zur Diagnostik der Aufmerksamkeitsdefizit-/Hyperaktivitätsstörung (ADHS) im Erwachsenenalter: Selbstbeurteilungsskala (ADHS-SB) und Diagnosecheckliste (ADHS-DC). Nervenarzt 75:888–895
Rubia K, Smith AB, Woolley J, Nosarti C, Heyman I, Taylor E et al (2006) Progressive increase of frontostriatal bran activation from childhood to adulthood during event-related tasks of cognitive control. Hum Brain Mapp 27:973–993
Scahill L, Schwab-Stone M (2000) Epidemiology of ADHD in school-age children. Child Adolesc Psychiatr Clin N Am 9:541–555
Scheres A, Dijkstra M, Ainslie E, Balkan J, Reynolds B, Sonuga-Barke E et al (2006) Temporal and probabilistic discounting of rewards in children and adolescents: effects of age and ADHD symptoms. Neuropsychologia 44:2092–2103
Scheres A, Milham MP, Knutson B, Castellanos FX (2007) Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder. Biol Psychiatry 61:720–724
Schwartz K, Verhaeghen P (2008) ADHD and Stroop interference from age 9 to age 41 years: a meta-analysis of developmental effects. Psychol Med 38:1607–1616
Sergeant JA, Oosterlaan J, van der Merre J (1999) Information processing and energetic factors in attention-deficit/hyperactivity disorder. In: Quay HC, Hogan AE (eds) Handbook of disruptive behaviour disorders. Kluwer Academic/Plenum Publishers, New York, pp 75–104
Smith A, Taylor E, Rogers JW, Newman S, Rubia K (2002) Evidence for a pure time perception deficit in children with ADHD. J Child Psychol Psychiatry 43:529–542
Smith A, Taylor E, Lidzba K, Rubia K (2003) A right hemispheric frontocerebellar network for time discrimination of several hundreds of milliseconds. Neuroimage 20:344–350
Smith AB, Taylor E, Brammer M, Halari R, Rubia K (2008) Reduced activation in right lateral prefrontal cortex and anterior cingulate gyrus in medication-naive adolescents with attention deficit hyperactivity disorder during time discrimination. J Child Psychol Psychiatry 49:977–985
Solanto MV, Abikoff H, Sonuga-Barke E, Schachar R, Logan GD, 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 multi-modal treatment study of AD/HD. J Abnorm Child Psychol 29:215–228
Sonuga-Barke EJS (2002) Psychological heterogeneity in AD/HD: a dual pathway model of behaviour and cognition. Behav Brain Res 130:29–36
Sonuga-Barke EJS, Taylor E, Sembi S, Smith J (1992) Hyperactivity and delay aversion–I. The effect of delay on choice. J Child Psychol Psychiatry 33:387–398
Sonuga-Barke EJS, Dalen L, Remington B (2003) Do executive deficits and delay aversion make independent contributions to preschool attention-deficit/hyperactivity disorder symptoms? J Am Acad Child Adolesc Psychiatry 42:1335–1342
Sowell ER, Peterson BS, Thompson PM, Welcome SE, Henkenius AL, Toga AW (2003) Mapping cortical change across the human life span. Nat Neurosci 6:309–315
Spencer T, Biederman J, Wilens T (1999) Attention-deficit/hyperactivity disorder and comorbidity. Pediatr Clin N Am 46:915–927
Steinhausen HC, Metzke CW, Meier M, Kannenberg R (1998) Prevalence of child and adolescent psychiatric disorders: the Zurich epidemiological study. Acta Psychiatr Scand 98:262–271
Strohle A, Stoy M, Wrase J, Schwarzer S, Schlagenhauf F, Huss M et al (2008) Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder. Neuroimage 39:966–972
Tabachnick BG, Fidell LS (1996) Using multivariate statistics, 3rd edn. HarperCollins College Publishers, New York
Tewes U (1994) Hamburg-Wechsler-Intelligenztest für Erwachsene–Revision 1991 (HAWIE-R). Huber, Bern
Thompson PM, Giedd JN, Woods RP, MacDonald D, Evans AC, Toga AW (2000) Growth patterns in the developing brain detected by using continuum mechanical tensor maps. Nature 404:190–193
Toplak ME, Tannock R (2005) Time perception: modality and duration effects in attention-deficit/hyperactivity disorder (ADHD). J Abnorm Child Psychol 33:639–654
Tripp G, Alsop B (2001) Sensitivity to reward delay in children with attention deficit hyperactivity disorder (ADHD). J Child Psychol Psychiatry 42:691–698
Tucha L, Tucha O, Walitza S, Sontag TA, Laufkötter R, Linder M et al (2009) Vigilance and sustained attention in children and adults with ADHD. J Atten Disord 12:410–421
Valera EM, Faraone SV, Biederman J, Poldrack RA, Seidman LJ (2005) Functional neuroanatomy of working memory in adults with attention-deficit/hyperactivity disorder. Biol Psychiatry 57: 439–447
Van Mourik R, Oosterlaan J, Sergeant JA (2005) The Stroop revisited: a meta-analysis of interference control in AD/HD. J Child Psychol Psychiatry 46:150–165
Wager TD, Smith EE (2003) Neuroimaging studies of working memory: a meta-analysis. Cogn Affect Behav Neurosci 3:255–274
Weiss RH (1998) Grundintelligenztest Skala 2 (CFT 20). Hogrefe, Göttingen
Weiss RH, Osterland J (1997) Grundintelligenztest Skala 1 (CFT1). Hogrefe, Göttingen
Wilcox RR, Keselman HJ, Kowalchuk RK (1998) Can tests for treatment group equality be improved? The bootstrap and trimmed means conjecture. Br J Math Stat Psychol 51:123–134
Willcutt EG, Doyle AE, Nigg JT, Faraone SV, Pennington BF (2005) Validity of the executive function theory of attention-deficit/hyperactivity disorder: a meta-analytic review. Biol Psychiatry 57:1336–1346
Wittchen H, Zaudig M, Fydrich T (1997) Strukturiertes Klinisches Interview für DSM IV (SKID). Hogrefe, Göttingen
Acknowledgments
This study was supported by a grant to K.K., S.C.H. and B.H–D. by the Interdisciplinary Center of Clinical Research Aachen (IZKF N65) in Germany. K.K., B.H.-D. gratefully acknowledge further support by the Deutsche Forschungsgemeinschaft (DFG-KFO112-II, TP 5).
Conflict of interest statement
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Marx, I., Hübner, T., Herpertz, S.C. et al. Cross-sectional evaluation of cognitive functioning in children, adolescents and young adults with ADHD. J Neural Transm 117, 403–419 (2010). https://doi.org/10.1007/s00702-009-0345-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00702-009-0345-3