Testing computational models of dopamine and noradrenaline dysfunction in attention deficit/hyperactivity disorder

Neuropsychopharmacology

Volumn 32, Issue 7, 2007, Pages 1583-1599

  Frank, Michael J ^a   Santamaria, Amy ^b,c   O'Reilly, Randall C ^b   Willcutt, Erik ^b  

^a University of Arizona   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c ALION SCIENCE AND TECHNOLOGY   (United States)

Author keywords

Attention deficit hyperactivity disorder; Dopamine; Noradrenaline computational models; Reinforcement learning; Working memory

Indexed keywords

AMPHETAMINE; DEXAMPHETAMINE; DOPAMINE; DOPAMINE 2 RECEPTOR; METHYLPHENIDATE; NORADRENALIN; PEMOLINE;

ADULT; ARTICLE; ATTENTION DEFICIT DISORDER; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; DOPAMINE BRAIN LEVEL; FEMALE; HUMAN; MALE; PREFRONTAL CORTEX; PRIORITY JOURNAL; REACTION TIME; REINFORCEMENT; STRIATE CORTEX; TASK PERFORMANCE; WORKING ANIMAL;

ADOLESCENT; ADULT; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; BRAIN; BRAIN CHEMISTRY; CENTRAL NERVOUS SYSTEM STIMULANTS; COMPUTER SIMULATION; DOPAMINE; FEMALE; HUMANS; LEARNING; MALE; MEMORY, SHORT-TERM; NEURAL PATHWAYS; NOREPINEPHRINE; PREFRONTAL CORTEX; REINFORCEMENT (PSYCHOLOGY);

EID: 34249032875     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301278     Document Type: Article

References (93)

1. Aase H, Meyer A, Sagvolden T (2006). Moment-to-moment dynamics of ADHD behaviour in South African children. Behav Brain Funct 2: 11.
2. Alexander GE, DeLong MR, Strick PL (1986). Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9: 357-381.
3. APA (ed) (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Press: Washington, DC.
4. Arnsten AF, Steere JC, Hunt RD (1996). The contribution of alpha 2-noradrenergic mechanisms of prefrontal cortical cognitive function. Potential significance for attention-deficit hyperactivity disorder. Arch Gen Psychiatry 53: 448-455.
5. Aron AR, Poldrack RA (2005). The cognitive neuroscience of response inhibition: relevance for genetic research in attentiondeficit/hyperactivity disorder. Biol Psychiatry 57: 1285-1292.
6. Aston-Jones G, Cohen JD (2005). An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annu Rev Neurosci 28: 403-450.
7. Barch DM, Braver TS, Nystom LE, Forman SD, Noll DC, Cohen JD (1997). Dissociating working memory from task difficulty in human prefrontal cortex. Neuropsychologia 35: 1373-1380.
8. Barch DM, Carter CS, Braver TS, Ans Sabb FW, MacDonald AR, Noll DC et al (2001). Selective deficits in prefrontal cortex function in medication-naive patients with schizophrenia. Arch Gen Psychiatry 58: 280-288.
9. Barkley RA (1997). Behavioral inhibition, sustained attention, and executive functions: Constructing a unifying theory of ADHD. Psycholo Bull 121: 65-94.
10. Barkley RA, Murphy K (1998). Attention-Deficit Hyperactivity Disorder: A Clinical Workbook. Guilford Press: New York.
11. Berridge CW, Devilbiss DM, Andrzejewski ME, Arnsten AFT, Kelley AE, Schmeichel B et al (2006). Methylphenidate preferentially increases catecholamine neurotransmission within the prefrontal cortex at low doses that enhance cognitive function. Biol Psychiatry 60: 1111-1120.
12. Bertrand E, Lechowicz W, Szpak GM, Dymecki J (1997). Qualitative and quantitative analysis of locus coeruleus neurons in Parkinson's disease. Folia Neuropathol 35: 80-86.
13. Biederman J, Faraone SV (2002). Current concepts on the neurobiology of attention-deficit/hyperactivity disorder. J Attention Disorders 6(Suppl 1): S7-S16.
14. Braver TS, Barch DM, Keys BA, Carter CS, Cohen JD, Kaye JA et al (2001). Context processing in older adults: Evidence for a theory relating cognitive control to neurobiology in healthy aging. J Exp Psychol Gene 130: 746-763.
15. Brown RG, Marsden CD (1990). Cognitive function in parkinson's disease: From description to theory. Trends Neurosci 13: 21-29.
16. Bymaster FP, Katner JS, Nelson DL, Hemrick-Luecke SK, Threlkeld PG, Heiligenstein JH et al (2002). Atomoxetine increases extracellular levels of norepinephrine and dopamine in prefrontal cortex of rat: a potential mechanism for efficacy in attention deficit/hyperactivity disorder. Neuropsychopharmacology 27: 699-711.
17. Castellanos FX, Sonuga-Barke EJS, Milham MP, Tannock R (2006). Characterizing cognition in ADHD: beyond executive dysfunction. Trends Cogn Sci 10: 117-123.
18. Castellanos FX, Sonuga-Barke EJS, Scheres A, Di Martino A, Hyde C, Walters JR (2005). Varieties of attention-deficit/hyperactivity disorder-related intra-individual variability. Biol Psychiatry 57: 1416-1423.
19. Chamberlain SR, Muller U, Blackwell AD, Clark L, Robbins TW, Sahakian BJ (2006). Neurochemical Modulation of Response Inhibition and Probabilistic Learning in Humans. Science 311: 861-863.
20. Chee P, Logan G, Schachar R, Lindsay P, Wachsmuth R (1989). Effects of event rate and display time on sustained attention in hyperactive, normal, and control children. J Abnorm Child Psychol 17: 371-391.
21. Cools R (2006). Dopaminergic modulation of cognitive function- implications for L-DOPA treatment in Parkinson's disease. Neurosci Biobehav Rev 30: 1-23.
22. Cools R, Barker RA, Sahakian BJ, Robbins TW (2001). Enhanced or impaired cognitive function in Parkinson's disease as a function of dopaminergic medication and task demands. Cerebral Cortex 11: 1136-1143.
23. Cragg SJ, Hille CJ, Greenfield SA (2002). Functional domains in dorsal striatum of the nonhuman primate are defined by the dynamic behavior of dopamine. J Neurosci 22: 5705-5712.
24. Diamond A (2005). Attention-deficit disorder (attention-deficit/ hyperactivity disorder without hyperactivity): a neurobiologically and behaviorally distinct disorder from attention-deficit/hyperactivity disorder (with hyperactivity). Dev Psychopathol 17: 807-825.
25. Dougherty DD, Bonab AA, Spencer TJ, Rauch SL, Madras BK, Fischman AJ (1999). Dopamine transporter density in patients with attention deficit hyperactivity disorder. Lancet 354: 2132-2133.
26. Durston S, Fossella JA, Casey BJ, Pol HEH, Galvan A, Schnack HG et al (2005). Differential effects of DRD4 and DAT1 genotype on fronto-striatal gray matter volumes in a sample of subjects with attention deficit hyperactivity disorder, their unaffected siblings, and controls. Mol Psychiatry 10: 678-685.
27. Durston S, Tottenham NT, Thomas KM, Davidson MC, Eigsti I-M, Yang Y et al (2003). Differential patterns of striatal activation in young children with and without ADHD. Biol Psychiatry 53: 871-878.
28. Faraone SV, Perlis RH, Doyle AE, Smoller JW, Goralnick JJ, Holmgren MA et al (2005). Molecular genetics of attention-deficit/hyperactivity disorder. Biol Psychiatry 57: 1313-1323.
29. Frank MJ (2005). Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and non-medicated Parkinsonism. J Cogn Neurosci 17: 51-72.
30. Frank MJ (2006). Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Networks 19: 1120-1136.
31. Frank MJ, Claus ED (2006). Anatomy of a decision: striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychol Rev 113: 300-326.
32. Frank MJ, O'Reilly RC (2006). A mechanistic account of striatal dopamine function in human cognition: Psychopharmacological studies with cabergoline and haloperidol. Behav Neurosci 120: 497-517.
33. Frank MJ, Loughry B, O'Reilly RC (2001). Interactions between the frontal cortex and basal ganglia in working memory: A computational model. Cognitive, Affective, and Behavioral Neuroscience 1: 137-160.
34. Frank MJ, Scheres A, Sherman SJ (in press). Understanding decision making deficits in neurological conditions: Insights from models of natural action selection. Philos Trans Roy Soc-B.
35. Frank MJ, Seeberger LC, O'Reilly RC (2004). By carrot or by stick: cognitive reinforcement learning in Parkinsonism. Science 306: 1940-1943.
36. Frank MJ, Woroch BS, Curran T (2005). Error-related negativity predicts reinforcement learning and conflict biases. Neuron 47: 495-501.
37. Grace AA (2001). Psychostimulant actions on dopamine and limbic system function: relevance to the pathophysiology and treatment of ADHD. In: Solanto MV and Arnsten AF (eds). Stimulant Drugs and ADHD: Basic and Clinical Neuroscience. Oxford University Press: New York. pp 134-155.
38. Hornykiewicz O, Kish SJ (1987). Biochemical pathophysiology of Parkinson's disease. Adv Neurol 45: 19-34.
39. Joel D, Weiner I (2000). The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96: 451.
40. Jucaite A, Fernell E, Halldin C, Forssberg H, Farde L (2005). Reduced midbrain dopamine transporter binding in male adolescents with attention-deficit/hyperactivity disorder: association between striatal dopamine markers and motor hyperactivity. Biol Psychiatry 57: 229-238.
41. Krain AL, Castellanos FX (2006). Brain development and ADHD. Clin Psychol Rev 26: 433-444.
42. Krause K, Dresel SH, Krause J, Kung HF, Tatsch K (2000). Increased striatal dopamine transporter in adult patients with attention deficit hyperactivity disroder: effects of methylphenidate as measured by single photon emission computed tomography. Neurosci Lett 285: 107-110.
43. Leth-Steensen C, Elbaz ZK, Douglas VI (2000). Mean response times, variability, and skew in the responding of adhd children: a response time distributional approach. Acta Psychol 104: 167-190.
44. Lewis SJ, Dove A, Robbins TW, Barker RA, Owen AM (2004). Striatal contributions to working memory: a functional magnetic resonance imaging study in humans. Eur J Neurosci 19: 755.
45. 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 Abnormal Psychol 114: 216-222.
46. Llorente AM, Voigt RG, Jensen CL, Berretta MC, Fraley JK, Heird WC (2006). Performance on a visual sustained attention and discrimination task is associated with urinary excretion of norepineprhine metabolite in children with attention-deficit/hyperactivity disorder (AD/HD). Clin Neuropsychol 20: 133-144.
47. Luman M, Oosterlaan J, Sergeant JA (2005). The impact of reinforcement contingencies on AD/HD: a review and theoretical appraisal. Clin Psychol Rev 25: 183-213.
48. Madras BK, Miller GM, Fischman AJ (2005). The dopamine transporter and attention-deficit/hyperactivity disorder. Biol Psychiatry 57: 1397-1409.
49. Martinussen R, Hayden J, Hogg-Johnson S, 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.
50. Mazei MS, Pluto CP, Kirkbride B, Pehek EA (2002). Effects of catecholamine uptake blockers in the caudate-putamen and subregions of the medial prefrontal cortex of the rat. Brain Res 936: 58-67 (DAT blockade preferentially increases BG rel to PFC DA).
51. McClure SM, Laibson DI, Loewenstein G, Cohen JD (2004). Separate neural systems value immediate and delayed rewards. Science 306: 503-507.
52. McClure S, Gilzenrat M, Cohen J (2006). An exploration-exploitation model based on norepinepherine and dopamine activity. Adv Neural Inform Process Systems 18: 867-874.
53. Michelson D, Faries D, Wernicke J, Kelsey D, Kendrick K, Sallee FR et al (2001). Atomoxetine in the treatment of children and adolescents with attention-deficit/hyperactivity disorder: a randomized, placebo-controlled, dose-response study. Pediatrics 108: E83.
54. Mobini S, Body S, Ho MY, Bradshaw CM, Szabadi E, Deakin JF et al (2002). Effects of lesions of the orbitofrontal cortex on sensitivity to delayed and probabilistic reinforcement. Psychopharmacology 160: 290-298.
55. 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.
56. O'Reilly RC, Frank MJ (2006). Making working memory work: A computational model of learning in the prefrontal cortex and basal ganglia. Neural Comput 18: 283-328.
57. Overtoom CC, Verbaten MN, Kenemans JL, van Engeland H, Buitelaar JK, van der Molen MW et al (2003). Effects of methylphenidate, desipramine, and L-dopa on attention and inhibition in children with attention deficit hyperactivity disorder. Behav Brain Res 145: 7-15.
58. Owen AM, Doyon J, Dagher A, Sadikot A, Evans AC (1998). Abnormal basal ganglia outflow in Parkinson's disease identified with PET implications for higher cortical functions. Brain 121: 949-965.
59. Redgrave P, Prescott TJ, Gurney K (1999). Is the short-latency dopamine response too short to signal reward error? Trends Neurosci 22: 146-151.
60. Rhodes SM, Coghill DR, Matthews K (2005). Neuropsychological functioning in stimulant-naive boys with hyperkinetic disorder. Psychol Med 35: 1109-1120.
61. Rinne UK, Laihinen A, Rinne JO, Nagren K, Bergman J, Ruotsalainen U (1990). Positron emission tomography demonstrates dopamine D2 receptor supersensitivity in the striatum of patients with early Parkinson's disease. Mov Disord 5: 55-59.
62. Robbins TW, Everitt BJ (1999). Drug addiction: bad habits add up. Nature 398: 567-570.
63. Ruskin DN, Bergstrom DA, Shenker A, Freeman LE, Baek D, Walters JR (2001). Drugs used in the treatment of attention-deficit/hyperactivity disorder affect postsynaptic firing rate and oscillation without preferential dopamine autoreceptor action. Biol Psychiatry 49: 340-350.
64. Ruskin DN, Bergstrom DA, Tierney PL, Walters JR (2003). Correlated multisecond oscillations in firing rate in the basal ganglia: modulation by dopamine and the subthalamic nucleus. Neuroscience 117: 427-438.
65. Russell V, Allie S, Wiggins T (2000). Increased noradrenergic activity in prefrontal cortex slices of an animal model for attention-deficit hyperactivity disorder - the spontaneously hypertensive rat. Behav Brain Res 117: 69-74.
66. Russell VA, Wiggins TM (2000). Increased glutamate-stimulated norepinephrine release from prefrontal cortex slices of spontaneously hypertensive rats. Metab Brain Dis 15: 297-304.
67. Sagvolden T, Aase H, Zeiner P, Berger D (1998). Altered reinforcement mechanisms in attention-deficit/hyperactivity disorder. Behav Brain Res 94: 61-71.
68. Sagvolden T, Johansen EB, Aase H, Russell VA (2005). A dynamic developmental theory of attention-deficit/hyperactivity disorder (ADHD) predominantly hyperactive/impulsive and combined subtypes. Behav Brain Sci 28: 397-419; discussion 419-68.
69. Santamaria A, O'Reilly R, Willcutt E (in preparation). Working memory deficits explain timing impairments in ADHD.
70. Scheres A, Dijkstra M, Ainslie E, Balkan J, Reynolds B, Sonuga-Barke E, Castellanos FX (2006a). Temporal probabilistic discounting of rewards in children adolescents: effects of age ADHD symptoms. Neuropsychologia 44: 2092-2103.
71. Scheres A, Milham MP, Knutson B, Castellanos FX (2006b). Ventral striatal hyporesponsiveness during reward anticipation in attention deficit/ hyperactivity disorder. Biol Psychiatry [Epub ahead of print].
72. Schiffer WK, Volkow ND, Fowler JS, Alexoff DL, Logan J, Dewey SL (2006). Therapeutic doses of amphetamine or methylphenidate differentially increase synaptic and extracellular dopamine. Synapse 59: 243-251 (ritalin and amphetamine both increase synaptic (phasic) DA to same degree (both amp increases extracellular DA much more)).
73. Schultz W (2002). Getting formal with dopamine and reward. Neuron 36: 241-263.
74. Seeman P, Madras B (2002). Methylphenidate elevates resting dopamine which lowers the impulse-triggered release of dopamine: a hypothesis. Behav Brain Res 130: 79-83.
75. Servan-Schreiber D, Cohen JD, Steingard S (1997). Schizophrenic deficits in the processing of context: A test of a theoretical model. Arch Gen Psychiatry 53: 1105-1113.
76. Sesack SR, Hawrylak VA, Matus C, Guido MA, Levey AI (1998). Dopamine axon varicosities in the prelimbic division of the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J Neurosci 18: 2697-2708.
77. Solanto MV (2002). Dopamine dysfunction in AD/HD: integrating clinical and basic neuroscience research. Behav Brain Res 130: 65-71.
78. 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 multimodal treatment study of AD/HD. J Abnorm Child Psychol 29: 215-228.
79. Sonuga-Barke EJS (2003). The dual pathway model of AD/HD: an elaboration of neuro-developmental characteristics. Neurosci Biobehav Rev 27: 593-604.
80. Sonuga-Barke EJS (2005). Causal models of attention-deficit/hyperactivity disorder: from common simple deficits to multiple developmental pathways. Biol Psychiatry 57: 1231-1238.
81. Stryjer R, Klein C, Treves TA, Rabey JM (2005). The effects of acute loading with levodopa and levodopa with selegiline on blood pressure and plasma norepinephrine levels in chronic Parkinson's disease patients. Acta Neurol Scand 111: 89-94.
82. Swanson CJ, Perry KW, Koch-Krueger S, Katner J, Svensson KA, Bymaster FP (2006). Effect of the attention deficit/hyperactivity disorder drug atomoxetine on extracellular concentrations of norepinephrine and dopamine in several brain regions of the rat. Neuropharmacology 50: 755-760.
83. Todd RD, Huang H, Smalley SL, Nelson SF, Willcutt EG, Pennington BF et al (2005). Collaborative analysis of DRD4 and DAT genotypes in population-defined ADHD subtypes. J Child Psychol Psychiatry 46: 1067-1073.
84. Toplak ME, Jain U, Tannock R (2005). Executive and motivational processes in adolescents with Attention-Deficit-Hyperactivity Disorder (ADHD). Behav Brain Funct 1: 8.
85. Usher M, Cohen JD, Servan-Schreiber D, Rajkowski J, Aston-Jones G (1999). The role of locus coeruleus in the regulation of cognitive performance. Science 283: 549-554.
86. Volkow ND, Wang GJ, Fowler JS, Logan J, Gerasimov M, Maynard L et al (2001). Therapeutic doses of methylphenidate significantly increase extracellular dopamine in the human brain. J Neurosci 21: RC121.
87. Weiner I, Joel D (2002). Dopamine in schizophrenia: Dysfunctional processing in basal ganglia -thalamocortical split circuits. In: Di Chiara G (ed). Handbook of Experimental Pharmacology, Vol. 154/ii. Dopa1e in the CNS II. Springer-Verlag: Berlin.
88. Wichmann T, Kliem MA, Soares J (2002). Slow oscillatory discharge in the primate basal ganglia. J Neurophysiol 87: 1145-1148.
89. 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.
90. Wu Q, Reith ME, Walker QD, Kuhn CM, Caroll FI, Garris PA (2002). Concurrent autoreceptor-mediated control of dopamine release and uptake during neurotransmission: an in vivo voltammetric study. J Neurosci 22: 6272-6281.
91. Yano M, Steiner H (2005). Methylphenidate (Ritalin) induces Homer 1a and zif 268 expression in specific corticostriatal circuits. Neuroscience 132: 855-865.
92. Yano M, Beverley JA, Steiner H (2006). Inhibition of methylphenidate- induced gene expression in the striatum by local blockade of D1 dopamine receptors: interhemispheric effects. Neuroscience 140: 699-709.
93. Zametkin AJ, Rapoport JL (1987). Neurobiology of attention deficit disorder with hyperactivity: where have we come in 50 years? J Am Acad Child Adolesc Psychiatry 26: 676-686.