Biological Psychiatry
Volume 65, Issue 1 , Pages 7-14 , 1 January 2009

Neural Hyporesponsiveness and Hyperresponsiveness During Immediate and Delayed Reward Processing in Adult Attention-Deficit/Hyperactivity Disorder

  • Michael M. Plichta

      Affiliations

    • Department of Psychiatry, Psychosomatics and Psychotherapy, Laboratory for Psychophysiology and Functional Imaging, University of Würzburg, Würzburg, Germany
    • Institute of Psychology, Biological Psychology, Clinical Psychology, and Psychotherapy, University of Würzburg, Würzburg, Germany
    • ,
  • Nenad Vasic

      Affiliations

    • Department of Psychiatry, University of Ulm, Ulm, Germany
    • ,
  • Robert Christian Wolf

      Affiliations

    • Department of Psychiatry, University of Ulm, Ulm, Germany
    • ,
  • Klaus-Peter Lesch

      Affiliations

    • Molecular and Clinical Psychobiology, Department of Psychiatry and Psychotherapy, University of Würzburg, Würzburg, Germany
    • ,
  • Dagmar Brummer

      Affiliations

    • Department of Psychiatry, University of Ulm, Ulm, Germany
    • ,
  • Christian Jacob

      Affiliations

    • Adult ADHD Outpatient Service, University of Würzburg, Würzburg, Germany
    • ,
  • Andreas J. Fallgatter

      Affiliations

    • Department of Psychiatry, Psychosomatics and Psychotherapy, Laboratory for Psychophysiology and Functional Imaging, University of Würzburg, Würzburg, Germany
    • ,
  • Georg Grön

      Affiliations

    • Department of Psychiatry, University of Ulm, Ulm, Germany
    • Corresponding Author InformationAddress reprint requests to Georg Grön, Ph.D., University of Ulm, Department of Psychiatry, Leimgrubenweg 12-14, 89075 Ulm, Germany

Received 14 November 2007 ,Revised 3 July 2008 ,Accepted 6 July 2008.

References 

  1. Tobin H, Logue AW. Self-control across species (Columba livia, Homo sapiens, and Rattus norvegicus). J Comp Psychol. 1994;108:126–133
  2. Ainslie G. Specious reward: A behavioral theory of impulsiveness and impulse control. Psychol Bull. 1975;82:463–496
  3. Ainslie G, Herrnstein RJ. Preference reversal and delayed reinforcement. Anim Learn Behav. 1981;9:476–482
  4. Smith A. The Theory of Moral Sentiments. Cambridge, England: Cambridge University Press; 2002;
  5. Perin CT. The effect of delayed reinforcement upon the differentiation of bar responses in white rats. J Exp Psychol. 1943;32:95–109
  6. McClure SM, Laibson DI, Loewenstein G, Cohen JD. Separate neural systems value immediate and delayed monetary rewards. Science. 2004;306:503–507
  7. McClure SM, Ericson KM, Laibson DI, Loewenstein G, Cohen JD. Time discounting for primary rewards. J Neurosci. 2007;27:5796–5804
  8. Miller GA, Galanter E, Pribram KH. Plans and the Structure of Behavior. New York: Henry Holt and Co; 1960;
  9. Metcalfe J, Mischel W. A hot/cool-system analysis of delay of gratification: Dynamics of willpower. Psychol Rev. 1999;106:3–19
  10. Barkley RA, Edwards G, Laneri M, Fletcher K, Metevia L. 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. 2001;29:541–556
  11. Luman M, Oosterlaan J, Sergeant JA. The impact of reinforcement contingencies on AD/HD: A review and theoretical appraisal. Clin Psychol Rev. 2005;25:183–213
  12. Tripp G, Alsop B. Sensitivity to reward delay in children with attention deficit hyperactivity disorder (ADHD). J Child Psychol Psychiatry. 2001;42:691–698
  13. Scheres A, Dijkstra M, Ainslie E, Balkan J, Sonuga Barke E, Reynolds B, et al. Temporal and probabilistic discounting of rewards in children and adolescents: Effects of age and ADHD symptoms. Neuropsychologia. 2006;44:2092–2103
  14. Tripp G, Wickens JR. Dopamine transfer deficit: A neurobiological theory of altered reinforcement mechanisms in ADHD. J Child Psychol Psychiatry. 2008;49:691–704
  15. Sagvolden T, Johansen EB, Aase H, Russell VA. A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav Brain Sci. 2005;28:397–419
  16. Sonuga Barke EJ. Psychological heterogeneity in AD/HD–a dual pathway model of behaviour and cognition. Behav Brain Res. 2002;130:29–36
  17. Sonuga Barke EJ. The dual pathway model of AD/HD: An elaboration of neuro-developmental characteristics. Neurosci Biobehav Rev. 2003;27:593–604
  18. Scheres A, Milham MP, Knutson B, Castellanos FX. Ventral striatal hyporesponsiveness during reward anticipation in attention-deficit/hyperactivity disorder. Biol Psychiatry. 2007;61:720–724
  19. Strohle A, Stoy M, Wrase J, Schwarzer S, Schlagenhauf F, Huss M, et al. Reward anticipation and outcomes in adult males with attention-deficit/hyperactivity disorder. Neuroimage. 2008;39:966–972
  20. Sonuga Barke EJ, Taylor E, Sembi S, Smith J. Hyperactivity and delay aversion–I (The effect of delay on choice). J Child Psychol Psychiatry. 1992;33:387–398
  21. Sonuga Barke EJ, Taylor E, Heptinstall E. Hyperactivity and delay aversion–II (The effect of self versus externally imposed stimulus presentation periods on memory). J Child Psychol Psychiatry. 1992;33:399–409
  22. Sonuga Barke EJ, Williams E, Hall M, Saxton T. Hyperactivity and delay aversion (III: The effect on cognitive style of imposing delay after errors). J Child Psychol Psychiatry. 1996;37:189–194
  23. Sonuga Barke EJ. Causal models of attention-deficit/hyperactivity disorder: From common simple deficits to multiple developmental pathways. Biol Psychiatry. 2005;57:1231–1238
  24. Breiter HC, Aharon I, Kahneman D, Dale A, Shizgal P. Functional imaging of neural responses to expectancy and experience of monetary gains and losses. Neuron. 2001;30:619–639
  25. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science. 1997;275:1593–1599
  26. Knutson B, Cooper JC. Functional magnetic resonance imaging of reward prediction. Curr Opin Neurol. 2005;18:411–417
  27. Koepp MJ, Gunn RN, Lawrence AD, Cunningham VJ, Dagher A, Jones T, et al. Evidence for striatal dopamine release during a video game. Nature. 1998;393:266–268
  28. Haruno M, Kawato M. Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J Neurophysiol. 2006;95:948–959
  29. Haber SN. The primate basal ganglia: Parallel and integrative networks. J Chem Neuroanat. 2003;26:317–330
  30. Tanaka SC, Doya K, Okada G, Ueda K, Okamoto Y, Yamawaki S. Prediction of immediate and future rewards differentially recruits cortico-basal ganglia loops. Nat Neurosci. 2004;7:887–893
  31. Ito R, Dalley JW, Robbins TW, Everitt BJ. Dopamine release in the dorsal striatum during cocaine-seeking behavior under the control of a drug-associated cue. J Neurosci. 2002;22:6247–6253
  32. Volkow ND, Wang GJ, Telang F, Fowler JS, Logan J, Childress AR, et al. Cocaine cues and dopamine in dorsal striatum: Mechanism of craving in cocaine addiction. J Neurosci. 2006;26:6583–6588
  33. Delgado MR, Locke HM, Stenger VA, Fiez JA. Dorsal striatum responses to reward and punishment: Effects of valence and magnitude manipulations. Cogn Affect Behav Neurosci. 2003;3:27–38
  34. Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA. Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol. 2000;84:3072–3077
  35. Zink CF, Pagnoni G, Martin ME, Dhamala M, Berns GS. Human striatal response to salient nonrewarding stimuli. J Neurosci. 2003;23:8092–8097
  36. Atallah HE, Lopez Paniagua D, Rudy JW, O'Reilly RC. Separate neural substrates for skill learning and performance in the ventral and dorsal striatum. Nat Neurosci. 2007;10:126–131
  37. O'Doherty J, Dayan P, Schultz J, Deichmann R, Friston K, Dolan RJ. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science. 2004;304:452–454
  38. Aron A, Fisher H, Mashek DJ, Strong G, Li H, Brown LL. Reward, motivation, and emotion systems associated with early-stage intense romantic love. J Neurophysiol. 2005;94:327–337
  39. Volkow ND, Wang GJ, Fowler JS, Logan J, Jayne M, Franceschi D, et al. “Nonhedonic” food motivation in humans involves dopamine in the dorsal striatum and methylphenidate amplifies this effect. Synapse. 2002;44:175–180
  40. Weiskrantz L. Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J Comp Physiolog Psychol. 1956;49:381–391
  41. Hamann S, Mao H. Positive and negative emotional verbal stimuli elicit activity in the left amygdala. Neuroreport. 2002;13:15–19
  42. Hommer DW, Knutson B, Fong GW, Bennett S, Adams CM, Varnera JL. Amygdalar recruitment during anticipation of monetary rewards: An event-related fMRI study. Ann N Y Acad Sci. 2003;985:476–478
  43. Small DM, Gregory MD, Mak YE, Gitelman D, Mesulam MM, Parrish T. Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron. 2003;39:701–711
  44. Anderson AK, Christoff K, Stappen I, Panitz D, Ghahremani DG, Glover G, et al. Dissociated neural representations of intensity and valence in human olfaction. Nat Neurosci. 2003;6:196–202
  45. O'Doherty J, Critchley H, Deichmann R, Dolan RJ. Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J Neurosci. 2003;23:7931–7939
  46. Iaria G, Committeri G, Pastorelli C, Pizzamiglio L, Watkins KE, Carota A. Neural activity of the anterior insula in emotional processing depends on the individuals' emotional susceptibility. Hum Brain Mapp. 2008;29:363–373
  47. Kaplan RF, Stevens M. A review of adult ADHD: A neuropsychological and neuroimaging perspective. CNS Spectr. 2002;7:355–362
  48. Bjork JM, Knutson B, Fong GW, Caggiano DM, Bennett SM, Hommer DW. Incentive-elicited brain activation in adolescents: Similarities and differences from young adults. J Neurosci. 2004;24:1793–1802
  49. Ward MF, Wender PH, Reimherr FW. The Wender Utah Rating Scale: An aid in the retrospective diagnosis of childhood attention deficit hyperactivity disorder. Am J Psychiatry. 1993;150:885–890
  50. Retz-Junginger P, Retz W, Schneider M, Schwitzgebel P, Steinbach E, Hengesch G, et al. Gender differences in self-descriptions of child psychopathology in attention deficit hyperactivity disorder. Nervenarzt. 2007;78:1046–1051
  51. Lehrl S. Mehrfachwahl-Wortschatz-Intelligenztest MWT-B. Balingen, Germany: Spitta Verlag; 2005;
  52. Swanson JM, Volkow ND. Pharmacokinetic and pharmacodynamic properties of stimulants: Implications for the design of new treatments for ADHD. Behav Brain Res. 2002;130:73–78
  53. Kessler RC, Adler L, Ames M, Demler O, Faraone S, Hiripi E, et al. The World Health Organization Adult ADHD Self-Report Scale (ASRS): A short screening scale for use in the general population. Psychol Med. 2005;35:245–256
  54. Reuter M, Kirsch P, Hennig J. Inferring candidate genes for attention deficit hyperactivity disorder (ADHD) assessed by the World Health Organization Adult ADHD Self-Report Scale (ASRS). J Neural Transm. 2006;113:929–938
  55. Maldjian JA, Laurienti PJ, Kraft RA, Burdette JH. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19:1233–1239
  56. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): Use of a cluster-size threshold. Magn Reson Med. 1995;33:636–647
  57. Wittmann M, Leland DS, Paulus MP. Time and decision making: Differential contribution of the posterior insular cortex and the striatum during a delay discounting task. Exp Brain Res. 2007;179:643–653
  58. Hare TA, Tottenham N, Davidson MC, Glover GH, Casey BJ. Contributions of amygdala and striatal activity in emotion regulation. Biol Psychiatry. 2005;57:624–632
  59. Volkow ND, Wang GJ, Newcorn J, Telang F, Solanto MV, Fowler JS, et al. Depressed dopamine activity in caudate and preliminary evidence of limbic involvement in adults with attention-deficit/hyperactivity disorder. Arch Gen Psychiatry. 2007;64:932–940
  60. Knutson B, Gibbs SE. Linking nucleus accumbens dopamine and blood oxygenation. Psychopharmacology (Berl). 2007;191:813–822
  61. Castellanos FX, Tannock R. Neuroscience of attention-deficit/hyperactivity disorder: The search for endophenotypes. Nat Rev Neurosci. 2002;3:617–628

PII: S0006-3223(08)00827-5

doi: 10.1016/j.biopsych.2008.07.008

Biological Psychiatry
Volume 65, Issue 1 , Pages 7-14 , 1 January 2009

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