Differential effects of dopamine transporter inhibitors in the rodent Iowa gambling task: Relevance to mania

Psychopharmacology

Volumn 225, Issue 3, 2013, Pages 661-674

  Van Enkhuizen, Jordy ^a,b   Geyer, Mark A ^a,c   Young, Jared W ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UTRECHT UNIVERSITY   (Netherlands)

^c VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

Author keywords

Amphetamine; Bipolar disorder; Dopamine transporter; GBR12909; Impulsivity; Iowa gambling task; Mania; Mice; Modafinil; Risk taking

Indexed keywords

AMPHETAMINE; MODAFINIL; VANOXERINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; IMPULSIVENESS; IOWA GAMBLING TASK; MALE; MOTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT; TASK PERFORMANCE;

AMPHETAMINE; ANIMALS; BEHAVIOR, ANIMAL; BENZHYDRYL COMPOUNDS; BIPOLAR DISORDER; CHOICE BEHAVIOR; CONDITIONING, OPERANT; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; GAMBLING; HUMANS; IMPULSIVE BEHAVIOR; MICE; MICE, INBRED C57BL; PIPERAZINES; PUNISHMENT; REINFORCEMENT (PSYCHOLOGY);

EID: 84873724760     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-012-2854-2     Document Type: Article

References (75)

1. Adida M, Clark L, Pomietto P, Kaladjian A, Besnier N, Azorin JM, Jeanningros R, Goodwin GM (2008) Lack of insight may predict impaired decision making in manic patients. Bipolar Disord 10:829-837
2. Adida M, Jollant F, Clark L, Besnier N, Guillaume S, Kaladjian A, Mazzola-Pomietto P, Jeanningros R, Goodwin GM, Azorin JM, Courtet P (2011) Trait-related decision-making impairment in the three phases of bipolar disorder. Biol Psychiatry 70:357-365
3. Anand A, Barkay G, Dzemidzic M, Albrecht D, Karne H, Zheng QH, Hutchins GD, Normandin MD, Yoder KK (2011) Striatal dopamine transporter availability in unmedicated bipolar disorder. Bipolar Disord 13:406-413
4. Arban R, Maraia G, Brackenborough K, Winyard L, Wilson A, Gerrard P, Large C (2005) Evaluation of the effects of lamotrigine, valproate and carbamazepine in a rodent model of mania. Behav Brain Res 158:123-132
5. Bechara A, Damasio AR, Damasio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50:7-15
6. Bechara A, Damasio H, Tranel D, Damasio AR (1997) Deciding advantageously before knowing the advantageous strategy. Science 275:1293-1295
7. Bechara A, Damasio H, Damasio AR, Lee GP (1999) Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19:5473-5481
8. Bechara A, Damasio H, Tranel D, Damasio AR (2005) The Iowa Gambling Task and the somatic marker hypothesis: some questions and answers. Trends Cogn Sci 9:159-162, discussion 162-4
9. Berggren U, Tallstedt L, Ahlenius S, Engel J (1978) The effect of lithium on amphetamine-induced locomotor stimulation. Psychopharmacol (Berl) 59:41-45
10. Cardinal RN, Robbins TW, Everitt BJ (2000) The effects of d-amphetamine, chlordiazepoxide, alpha-flupenthixol and behavioural manipulations on choice of signalled and unsignalled delayed reinforcement in rats. Psychopharmacol (Berl) 152:362-375
11. Cassidy F, Ahearn EP, Carroll BJ (2002) Symptom profile consistency in recurrent manic episodes. Compr Psychiatry 43:179-181
12. Clark L, Iversen SD, Goodwin GM (2001) A neuropsychological investigation of prefrontal cortex involvement in acute mania. Am J Psychiatry 158:1605-1611
13. de Visser L, Homberg JR, Mitsogiannis M, Zeeb FD, Rivalan M, Fitoussi A, Galhardo V, van den Bos R, Winstanley CA, Dellu-Hagedorn F (2011) Rodent versions of the iowa gambling task: opportunities and challenges for the understanding of decision-making. Front Neurosci 5:109
14. Evenden JL (1999) Varieties of impulsivity. Psychopharmacol (Berl) 146:348-361
15. Flaisher-Grinberg S, Overgaard S, Einat H (2009) Attenuation of high sweet solution preference by mood stabilizers: a possible mouse model for the increased reward-seeking domain of mania. J Neurosci Methods 177:44-50
16. Floresco SB, St Onge JR, Ghods-Sharifi S, Winstanley CA (2008) Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making. Cogn Affect Behav Neurosci 8:375-389
17. Frey BN, Valvassori SS, Reus GZ, Martins MR, Petronilho FC, Bardini K, Dal-Pizzol F, Kapczinski F, Quevedo J (2006) Effects of lithium and valproate on amphetamine-induced oxidative stress generation in an animal model of mania. J Psychiatry Neurosci 31:326-332
18. Gould TD, Einat H (2007) Animal models of bipolar disorder and mood stabilizer efficacy: a critical need for improvement. Neurosci Biobehav Rev 31:825-831
19. Gould TJ, Keith RA, Bhat RV (2001) Differential sensitivity to lithium's reversal of amphetamine-induced open-field activity in two inbred strains of mice. Behav Brain Res 118:95-105
20. Granon S, Passetti F, Thomas KL, Dalley JW, Everitt BJ, Robbins TW (2000) Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex. J Neurosci 20:1208-1215
21. Greenwood TA, Alexander M, Keck PE, McElroy S, Sadovnick AD, Remick RA, Kelsoe JR (2001) Evidence for linkage disequilibrium between the dopamine transporter and bipolar disorder. Am J Med Genet 105:145-151
22. Greenwood TA, Schork NJ, Eskin E, Kelsoe JR (2006) Identification of additional variants within the human dopamine transporter gene provides further evidence for an association with bipolar disorder in two independent samples. Molecular Psychiatry 11:125-133
23. Grottick AJ, Higgins GA (2002) Assessing a vigilance decrement in aged rats: effects of pre-feeding, task manipulation, and psychostimulants. Psychopharmacology 164:33-41
24. Han DD, Gu HH (2006) Comparison of the monoamine transporters from human and mouse in their sensitivities to psychostimulant drugs. BMC Pharmacol 6:6
25. Harrison AA, Everitt BJ, Robbins TW (1997) Central 5-HT depletion enhances impulsive responding without affecting the accuracy of attentional performance: interactions with dopaminergic mechanisms. Psychopharmacol (Berl) 133:329-342
26. Heikkila RE, Manzino L (1984) Behavioral properties of GBR 12909, GBR 13069 and GBR 13098: specific inhibitors of dopamine uptake. Eur J Pharmacol 103:241-248
27. Helms CM, Reeves JM, Mitchell SH (2006) Impact of strain and d-amphetamine on impulsivity (delay discounting) in inbred mice. Psychopharmacol (Berl) 188:144-151
28. Homberg JR, van den Bos R, den Heijer E, Suer R, Cuppen E (2008) Serotonin transporter dosage modulates long-term decision-making in rat and human. Neuropharmacology 55:80-84
29. Horschitz S, Hummerich R, Lau T, Rietschel M, Schloss P (2005) A dopamine transporter mutation associated with bipolar affective disorder causes inhibition of transporter cell surface expression. Mol Psychiatry 10:1104-1109
30. Kelley AE, Lang CG (1989) Effects of GBR 12909, a selective dopamine uptake inhibitor, on motor activity and operant behavior in the rat. Eur J Pharmacol 167:385-395
31. Kim SW, Grant JE, Eckert ED, Faris PL, Hartman BK (2006) Pathological gambling and mood disorders: clinical associations and treatment implications. J Affect Disord 92:109-116
32. Lapin IP (1993) Anxiogenic effect of phenylethylamine and amphetamine in the elevated plus-maze in mice and its attenuation by ethanol. Pharmacol Biochem Behav 44:241-243
33. Loos M, Staal J, Schoffelmeer AN, Smit AB, Spijker S, Pattij T (2010) Inhibitory control and response latency differences between C57BL/6J and DBA/2J mice in a Go/No-Go and 5-choice serial reaction time task and strain-specific responsivity to amphetamine. Behav Brain Res 214:216-224
34. Madras BK, Xie Z, Lin Z, Jassen A, Panas H, Lynch L, Johnson R, Livni E, Spencer TJ, Bonab AA, Miller GM, Fischman AJ (2006) Modafinil occupies dopamine and norepinephrine transporters in vivo and modulates the transporters and trace amine activity in vitro. J Pharmacol Exp Ther 319:561-569
35. Manji HK, Quiroz JA, Payne JL, Singh J, Lopes BP, Viegas JS, Zarate CA (2003) The underlying neurobiology of bipolar disorder. World Psychiatry 2:136-146
36. Merikangas KR, Jin R, He JP, Kessler RC, Lee S, Sampson NA, Viana MC, Andrade LH, Hu C, Karam EG, Ladea M, Medina-Mora ME, Ono Y, Posada-Villa J, Sagar R, Wells JE, Zarkov Z (2011) Prevalence and correlates of bipolar spectrum disorder in the world mental health survey initiative. Arch Gen Psychiatry 68:241-251
37. Minassian A, Henry BL, Geyer MA, Paulus MP, Young JW, Perry W (2010) The quantitative assessment of motor activity in mania and schizophrenia. J Affect Disord 120:200-206
38. Navarra R, Graf R, Huang Y, Logue S, Comery T, Hughes Z, Day M (2008) Effects of atomoxetine and methylphenidate on attention and impulsivity in the 5-choice serial reaction time test. Prog Neuro-Psychopharmacol Biol Psychiatry 32:34-41
39. Onaivi ES, Martin BR (1989) Neuropharmacological and physiological validation of a computer-controlled two-compartment black and white box for the assessment of anxiety. Prog Neuro-Psychopharmacol Biol Psychiatry 13:963-976
40. Paine TA, Tomasiewicz HC, Zhang K, Carlezon WA Jr (2007) Sensitivity of the five-choice serial reaction time task to the effects of various psychotropic drugs in Sprague-Dawley rats. Biol Psychiatry 62:687-693
41. Pattij T, Janssen MC, Vanderschuren LJ, Schoffelmeer AN, van Gaalen MM (2007) Involvement of dopamine D1 and D2 receptors in the nucleus accumbens core and shell in inhibitory response control. Psychopharmacol (Berl) 191:587-598
42. Perry W, Minassian A, Paulus MP, Young JW, Kincaid MJ, Ferguson EJ, Henry BL, Zhuang X, Masten VL, Sharp RF, Geyer MA (2009) A reverse-translational study of dysfunctional exploration in psychiatric disorders: from mice to men. Arch Gen Psychiatry 66:1072-1080
43. Perry W, Minassian A, Henry B, Kincaid M, Young JW, Geyer MA (2010) Quantifying over-activity in bipolar and schizophrenia patients in a human open field paradigm. Psychiatry Res 178:84-91
44. Pinsonneault JK, Han DD, Burdick KE, Kataki M, Bertolino A, Malhotra AK, Gu HH, Sadee W (2011) Dopamine transporter gene variant affecting expression in human brain is associated with bipolar disorder. Neuropsychopharmacology 36(8):1644-1655
45. Qu WM, Huang ZL, Xu XH, Matsumoto N, Urade Y (2008) Dopaminergic D1 and D2 receptors are essential for the arousal effect of modafinil. J Neurosci 28:8462-8469
46. Rivalan M, Ahmed SH, Dellu-Hagedorn F (2009) Risk-prone individuals prefer the wrong options on a rat version of the Iowa Gambling Task. Biol Psychiatry 66(8):743-749
47. Rivalan M, Coutureau E, Fitoussi A, Dellu-Hagedorn F (2011) Inter-individual decision-making differences in the effects of cingulate, orbitofrontal, and prelimbic cortex lesions in a rat gambling task. Front Behav Neurosci 5:22
48. Robbins TW (2002) The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacol (Berl) 163:362-380
49. Robinson ES, Eagle DM, Mar AC, Bari A, Banerjee G, Jiang X, Dalley JW, Robbins TW (2008) Similar effects of the selective noradrenaline reuptake inhibitor atomoxetine on three distinct forms of impulsivity in the rat. Neuropsychopharmacology 33:1028-1037
50. Rothman RB, Baumann MH (2003) Monoamine transporters and psychostimulant drugs. Eur J Pharmacol 479:23-40
51. Sevy S, Burdick KE, Visweswaraiah H, Abdelmessih S, Lukin M, Yechiam E, Bechara A (2007) Iowa gambling task in schizophrenia: a review and new data in patients with schizophrenia and co-occurring cannabis use disorders. Schizophr Res 92:74-84
52. Silverstone PH, Pukhovsky A, Rotzinger S (1998) Lithium does not attenuate the effects of d-amphetamine in healthy volunteers. Psychiatry Res 79:219-226
53. Swann AC, Steinberg JL, Lijffijt M, Moeller FG (2008) Impulsivity: differential relationship to depression and mania in bipolar disorder. J Affect Disord 106:241-248
54. Swann AC, Lijffijt M, Lane SD, Steinberg JL, Moeller FG (2009) Increased trait-like impulsivity and course of illness in bipolar disorder. Bipolar Disord 11:280-288
55. van den Bos R, Lasthuis W, den Heijer E, van der Harst J, Spruijt B (2006) Toward a rodent model of the Iowa gambling task. Behav Res Methods 38:470-478
56. van den Buuse M, de Jong W (1989) Differential effects of dopaminergic drugs on open-field behavior of spontaneously hypertensive rats and normotensive Wistar-Kyoto rats. J Pharmacol Exp Ther 248:1189-1196
57. van der Plas EA, Crone EA, van den Wildenberg WP, Tranel D, Bechara A (2008) Executive control deficits in substance-dependent individuals: a comparison of alcohol, cocaine, and methamphetamine and of men and women. J Clin Exp Neuropsychol: 1-14
58. Vawter MP, Freed WJ, Kleinman JE (2000) Neuropathology of bipolar disorder. Biol Psychiatry 48:486-504
59. Volkow ND, Fowler JS, Logan J, Alexoff D, Zhu W, Telang F, Wang GJ, Jayne M, Hooker JM, Wong C, Hubbard B, Carter P, Warner D, King P, Shea C, Xu Y, Muench L, Apelskog-Torres K (2009) Effects of modafinil on dopamine and dopamine transporters in the male human brain: clinical implications. JAMA 301:1148-1154
60. Wade TR, de Wit H, Richards JB (2000) Effects of dopaminergic drugs on delayed reward as a measure of impulsive behavior in rats. Psychopharmacol (Berl) 150:90-101
61. Waters KA, Burnham KE, O'Connor D, Dawson GR, Dias R (2005) Assessment of modafinil on attentional processes in a five-choice serial reaction time test in the rat. J Psychopharmacol 19:149-158
62. Yan TC, Dudley JA, Weir RK, Grabowska EM, Pena-Oliver Y, Ripley TL, Hunt SP, Stephens DN, Stanford SC (2011) Performance deficits of NK1 receptor knockout mice in the 5-choice serial reaction-time task: effects of d-amphetamine, stress and time of day. PLoS One 6:e17586
63. Yechiam E, Hayden EP, Bodkins M, O'Donnell BF, Hetrick WP (2008) Decision making in bipolar disorder: a cognitive modeling approach. Psychiatry Res 161:142-152
64. Young JW, Geyer MA (2010) Action of modafinil - increased motivation via the dopamine transporter inhibition and D1 receptors? Biol Psychiatry 67:784-787
65. Young JW, Minassian A, Paulus MP, Geyer MA, Perry W (2007) A reverse-translational approach to bipolar disorder: rodent and human studies in the Behavioral Pattern Monitor. Neurosci Biobehav Rev 31:882-896
66. Young JW, Light GA, Marston HM, Sharp R, Geyer MA (2009) The 5-choice continuous performance test: evidence for a translational test of vigilance for mice. PLoS One 4:e4227
67. Young JW, Goey AK, Minassian A, Perry W, Paulus MP, Geyer MA (2010a) GBR 12909 administration as a mouse model of bipolar disorder mania: mimicking quantitative assessment of manic behavior. Psychopharmacol (Berl) 208:443-454
68. Young JW, Goey AK, Minassian A, Perry W, Paulus MP, Geyer MA (2010b) The mania-like exploratory profile in genetic dopamine transporter mouse models is diminished in a familiar environment and reinstated by subthreshold psychostimulant administration. Pharmacol Biochem Behav 96:7-15
69. Young JW, Henry BL, Geyer MA (2011a) Predictive animal models of mania, hits, misses, and future directions. Br J Pharmacol 164(4):1263-1284
70. Young JW, Kooistra K, Geyer MA (2011b) Dopamine receptor mediation of the exploratory/hyperactivity effects of modafinil. Neuropsychopharmacology 36:1385-1396
71. Young JW, van Enkhuizen J, Winstanley CA, Geyer MA (2011c) Increased risk-taking behavior in dopamine transporter knockdown mice: further support for a mouse model of mania. J Psychopharmacol 25:934-943
72. Zack M, Poulos CX (2009) Effects of the atypical stimulant modafinil on a brief gambling episode in pathological gamblers with high vs. low impulsivity. J Psychopharmacol 23:660-671
73. Zeeb FD, Winstanley CA (2011) Lesions of the basolateral amygdala and orbitofrontal cortex differentially affect acquisition and performance of a rodent gambling task. J Neurosci 31:2197-2204
74. Zeeb FD, Robbins TW, Winstanley CA (2009) Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 34:2329-2343
75. Zolkowska D, Jain R, Rothman RB, Partilla JS, Roth BL, Setola V, Prisinzano TE, Baumann MH (2009) Evidence for the involvement of dopamine transporters in behavioral stimulant effects of modafinil. J Pharmacol Exp Ther 329:738-746