Biological Psychiatry
Volume 66, Issue 10 , Pages 972-977 , 15 November 2009

Ventro-Striatal Reductions Underpin Symptoms of Hyperactivity and Impulsivity in Attention-Deficit/Hyperactivity Disorder

  • Susanna Carmona

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain
    • Corresponding Author InformationAddress correspondence to Susanna Carmona, Ph.D., Unitat de Recerca en Neurociència Cognitiva, Departments de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Campus Bellaterra, 08193 Bellaterra (Barcelona), Spain
    • ,
  • Erika Proal

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain
    • ,
  • Elseline A. Hoekzema

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain
    • ,
  • Juan-Domingo Gispert

      Affiliations

    • Institut d'Alta tecnologia-Parc de Recerca Biomédica de Barcelona and CRC Corporacio Sanitaria, Barcelona, Spain
    • ,
  • Marisol Picado

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain
    • ,
  • Irene Moreno

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain
    • ,
  • Juan Carlos Soliva

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain
    • ,
  • Anna Bielsa

      Affiliations

    • Servei de Psiquiatria, Hospital Vall d'Hebron, Barcelona, Spain
    • ,
  • Mariana Rovira

      Affiliations

    • CRC Corporacio Sanitaria, Barcelona, Spain
    • ,
  • Joseph Hilferty

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain
    • ,
  • Antonio Bulbena

      Affiliations

    • Institut d'Atenció Psiquiàtrica, Hospital del Mar, Barcelona, Spain
    • ,
  • Miquel Casas

      Affiliations

    • Servei de Psiquiatria, Hospital Vall d'Hebron, Barcelona, Spain
    • ,
  • Adolf Tobeña

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain
    • ,
  • Oscar Vilarroya

      Affiliations

    • Unitat de Recerca en Neurociència Cognitiva, Departament de Psiquiatria i Medicina Legal, Universitat Autònoma de Barcelona, Bellaterra, Spain

Received 5 November 2008 ,Revised 5 May 2009 ,Accepted 12 May 2009.

References 

  1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 4th ed., Text Revised. Washington, DC: American Psychiatric Association; 2000;
  2. Solanto MV. Neuropharmacological basis of stimulant drug action in attention deficit disorder with hyperactivity: A review and synthesis. Psychol Bull. 1984;95:387–409
  3. Barkley RA. Behavioral inhibition, sustained attention, and executive functions: Constructing a unifying theory of ADHD. Psychol Bull. 1997;121:65–94
  4. Giedd JN, Blumenthal J, Molloy E, Castellanos FX. Brain imaging of attention deficit/hyperactivity disorder. Ann N Y Acad Sci. 2001;931:33–49
  5. Valera EM, Faraone SV, Murray KE, Seidman LJ. Meta-analysis of structural imaging findings in attention-deficit/hyperactivity disorder. Biol Psychiatry. 2007;61:1361–1369
  6. Castellanos FX, Sonuga-Barke EJ, Milham MP, Tannock R. Characterizing cognition in ADHD: Beyond executive dysfunction. Trends Cogn Sci. 2006;10:117–123
  7. 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;28:397–419discussion: 419–368
  8. Sonuga-Barke EJ. Psychological heterogeneity in AD/HD—A dual pathway model of behaviour and cognition. Behav Brain Res. 2002;130:29–36
  9. Sonuga-Barke EJ. The dual pathway model of AD/HD: An elaboration of neuro-developmental characteristics. Neurosci Biobehav Rev. 2003;27:593–604
  10. 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
  11. Tripp G, Alsop B. Sensitivity to reward frequency in boys with attention deficit hyperactivity disorder. J Clin Child Psychol. 1999;28:366–375
  12. Solanto MV, Abikoff H, Sonuga-Barke E, Schachar R, Logan GD, Wigal T, 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. 2001;29:215–228
  13. Kuntsi J, Oosterlaan J, Stevenson J. Psychological mechanisms in hyperactivity (I. Response inhibition deficit, working memory impairment, delay aversion, or something else?). J Child Psychol Psychiatry. 2001;42:199–210
  14. 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
  15. 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
  16. Antrop I, Stock P, Verte S, Wiersema JR, Baeyens D, Roeyers H. ADHD and delay aversion: The influence of non-temporal stimulation on choice for delayed rewards. J Child Psychol Psychiatry. 2006;47:1152–1158
  17. Schweitzer JB, Sulzer-Azaroff B. Self-control in boys with attention deficit hyperactivity disorder: Effects of added stimulation and time. J Child Psychol Psychiatry. 1995;36:671–686
  18. Russell VA. Dopamine hypofunction possibly results from a defect in glutamate-stimulated release of dopamine in the nucleus accumbens shell of a rat model for attention deficit hyperactivity disorder—the spontaneously hypertensive rat. Neurosci Biobehav Rev. 2003;27:671–682
  19. Johansen EB, Aase H, Meyer A, Sagvolden T. Attention-deficit/hyperactivity disorder (ADHD) behaviour explained by dysfunctioning reinforcement and extinction processes. Behav Brain Res. 2002;130:37–45
  20. Carboni E, Silvagni A, Valentini V, Di Chiara G. Effect of amphetamine, cocaine and depolarization by high potassium on extracellular dopamine in the nucleus accumbens shell of SHR rats (An in vivo microdyalisis study). Neurosci Biobehav Rev. 2003;27:653–659
  21. Viggiano D, Vallone D, Sadile A. Dysfunctions in dopamine systems and ADHD: Evidence from animals and modeling. Neural Plast. 2004;11:97–114
  22. Sonuga-Barke EJ, Taylor E. The effect of delay on hyperactive and non-hyperactive children's response times: A research note. J Child Psychol Psychiatry. 1992;33:1091–1096
  23. Antrop I, Roeyers H, Van Oost P, Buysse A. Stimulation seeking and hyperactivity in children with ADHD (Attention Deficit hyperactivity Disorder). J Child Psychol Psychiatry. 2000;41:225–231
  24. Antrop I, Buysse A, Roeyers H, Van Oost P. Stimulation seeking and hyperactive behavior in children with ADHD: A re-analysis. Percept Mot Skills. 2002;95:71–90
  25. Cardinal RN, Pennicott DR, Sugathapala CL, Robbins TW, Everitt BJ. Impulsive choice induced in rats by lesions of the nucleus accumbens core. Science. 2001;292:2499–2501
  26. Cardinal RN, Howes NJ. Effects of lesions of the nucleus accumbens core on choice between small certain rewards and large uncertain rewards in rats. BMC Neurosci. 2005;6:37
  27. Christakou A, Robbins TW, Everitt BJ. Prefrontal cortical-ventral striatal interactions involved in affective modulation of attentional performance: Implications for corticostriatal circuit function. J Neurosci. 2004;24:773–780
  28. 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
  29. Scheres A, Lee A, Sumiya M. Temporal reward discounting and ADHD: Task and symptom specific effects. J Neural Transm. 2008;115:221–226
  30. 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. 2007;39:966–972
  31. Plichta MM, Vasic N, Wolf C, Lesch KP, Brummer D, Jacob C, et al. Neural hyporesponsiveness and hyperresponsiveness during immediate and delayed reward processing in adult attention-deficit/hyperactivity disorder. Biol Psychiatry. 2008;65:7–14
  32. Andersen SL, Napierata L, Brenhouse HC, Sonntag KC. Juvenile methylphenidate modulates reward-related behaviors and cerebral blood flow by decreasing cortical D3 receptors. Eur J Neurosci. 2008;27:2962–2972
  33. Knutson B, Bjork JM, Fong GW, Hommer D, Mattay VS, Weinberger DR. Amphetamine modulates human incentive processing. Neuron. 2004;43:261–269
  34. Kim Y, Teylan MA, Baron M, Sands A, Nairn AC, Greengard P. Methylphenidate-induced dendritic spine formation and DeltaFosB expression in nucleus accumbens. Proc Natl Acad Sci U S A. 2009;106:2915–2920
  35. Leo D, Adriani W, Cavaliere C, Cirillo G, Marco EM, Romano E, et al. Methylphenidate to adolescent rats drives enduring changes of accumbal Htr7 expression: Implications for impulsive behavior and neuronal morphology. Genes Brain Behav. 2009;8:356–368
  36. Gunduz H, Wu H, Ashtari M, Bogerts B, Crandall D, Robinson DG, et al. Basal ganglia volumes in first-episode schizophrenia and healthy comparison subjects. Biol Psychiatry. 2002;51:801–808
  37. Nacewicz BM, Dalton KM, Johnstone T, Long MT, McAuliff EM, Oakes TR, et al. Amygdala volume and nonverbal social impairment in adolescent and adult males with autism. Arch Gen Psychiatry. 2006;63:1417–1428
  38. Heal DJ, Smith SL, Kulkarni RS, Rowley HL. New perspectives from microdialysis studies in freely-moving, spontaneously hypertensive rats on the pharmacology of drugs for the treatment of ADHD. Pharmacol Biochem Behav. 2008;90:184–197
  39. Qiu A, Crocetti D, Adler M, Mahone EM, Denckla MB, Miller MI, et al. Basal ganglia volume and shape in children with attention deficit hyperactivity disorder. Am J Psychiatry. 2009;166:74–82
  40. Seidman LJ, Valera EM, Makris N, Monuteaux MC, Boriel DL, Kelkar K, et al. Dorsolateral prefrontal and anterior cingulate cortex volumetric abnormalities in adults with attention-deficit/hyperactivity disorder identified by magnetic resonance imaging. Biol Psychiatry. 2006;60:1071–1080
  41. Shaw P, Eckstrand K, Sharp W, Blumenthal J, Lerch JP, Greenstein D, et al. Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation. Proc Natl Acad Sci U S A. 2007;104:19649–19654
  42. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science. 1997;275:1593–1599
  43. Schultz W. Reward signaling by dopamine neurons. Neuroscientist. 2001;7:293–302
  44. Schultz W. Predictive reward signal of dopamine neurons. J Neurophysiol. 1998;80:1–27
  45. Johansen EB, Killeen PR, Russell VA, Tripp G, Wickens JR, Tannock R, et al. Origins of altered reinforcement effects in ADHD. Behav Brain Funct. 2009;5:7
  46. Williams J, Dayan P. Dopamine, learning, and impulsivity: A biological account of attention-deficit/hyperactivity disorder. J Child Adolesc Psychopharmacol. 2005;15:160–179discussion: 157–169
  47. Tripp G, Wickens JR. Research review: Dopamine transfer deficit: A neurobiological theory of altered reinforcement mechanisms in ADHD. J Child Psych Psychiatry. 2008;49:691–704

PII: S0006-3223(09)00633-7

doi: 10.1016/j.biopsych.2009.05.013

Biological Psychiatry
Volume 66, Issue 10 , Pages 972-977 , 15 November 2009

Article Tools

* Image Usage & Resolution