Activation of dopamine D4 receptors within the anterior cingulate cortex enhances the erroneous expectation of reward on a rat slot machine task

Neuropharmacology

Volumn 105, Issue , 2016, Pages 186-195

  Cocker, P J ^a,b   Hosking, J G ^a   Murch, W S ^a   Clark, L ^a   Winstanley, C A ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Anterior cingulate cortex; D4; Dopamine; Gambling; Near miss

Indexed keywords

DOPAMINE 4 RECEPTOR; N [4 (2 CYANOPHENYL) 1 PIPERAZINYLMETHYL] 3 METHYLBENZAMIDE; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; BACLOFEN; BENZAMIDE DERIVATIVE; MUSCIMOL; N-((4-(2-CYANOPHENYL)-1-PIPERAZINYL)METHYL)-3-METHYLBENZAMIDE; PIPERAZINE DERIVATIVE;

ANIMAL EXPERIMENT; ANTERIOR CINGULATE; ARTICLE; CONTROLLED STUDY; FRONTAL CORTEX; LIMBIC CORTEX; MALE; NONHUMAN; PATHOLOGICAL GAMBLING; PRIORITY JOURNAL; RAT; REWARD; SIGNAL TRANSDUCTION; SLOT MACHINE TASK; TASK PERFORMANCE; AGONISTS; ANIMAL; CINGULATE GYRUS; DECISION MAKING; DRUG EFFECTS; GAMBLING; GAME; LONG EVANS RAT; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BACLOFEN; BENZAMIDES; CHOICE BEHAVIOR; GABA-A RECEPTOR AGONISTS; GABA-B RECEPTOR AGONISTS; GAMBLING; GAMES, EXPERIMENTAL; GYRUS CINGULI; MALE; MUSCIMOL; PIPERAZINES; RATS; RATS, LONG-EVANS; RECEPTORS, DOPAMINE D4; REWARD;

EID: 84955311260     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.01.019     Document Type: Article

References (70)

1. V. Asghari, S. Sanyal, S. Buchwaldt, A. Paterson, V. Jovanovic, and H.H. Van Tol Modulation of intracellular cyclic AMP levels by different human dopamine D4 receptor variants J. Neurochem. 65 1995 1157 1165
2. V. Asghari, O. Schoots, S. van Kats, K. Ohara, V. Jovanovic, H.C. Guan, J.R. Bunzow, A. Petronis, and H.H. Van Tol Dopamine D4 receptor repeat: analysis of different native and mutant forms of the human and rat genes Mol. Pharmacol. 46 1994 364 373
3. I.M. Balodis, H. Kober, P.D. Worhunsky, M.C. Stevens, G.D. Pearlson, and M.N. Potenza Diminished frontostriatal activity during processing of monetary rewards and losses in pathological gambling Biol. Psychiatry 71 2012 749 757
4. H. Barbas, and D.N. Pandya Architecture and intrinsic connections of the prefrontal cortex in the Rhesus-Monkey J. Comp. Neurol. 286 1989 353 375
5. S.J. Boyson, P. McGonigle, and P.B. Molinoff Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain J. Neurosci. 6 1986 3177 3188
6. M. Brand, E. Kalbe, K. Labudda, E. Fujiwara, J. Kessler, and H.J. Markowitsch Decision-making impairments in patients with pathological gambling Psychiatry Res. 133 2005 91 99
7. R.B. Breen, and M. Zimmerman Rapid onset of pathological gambling in machine gamblers J. Gambl. Stud. 18 2002 31 43
8. J.W. Brown, and T.S. Braver Learned predictions of error likelihood in the anterior cingulate cortex Science 307 2005 1118 1121
9. G. Bush, B.A. Vogt, J. Holmes, A.M. Dale, D. Greve, M.A. Jenike, and B.R. Rosen Dorsal anterior cingulate cortex: a role in reward-based decision making Proc. Natl. Acad. Sci. U. S. A. 99 2002 523 528
10. R.N. Cardinal, D.R. Pennicott, C.L. Sugathapala, T.W. Robbins, and B.J. Everitt Impulsive choice induced in rats by lesions of the nucleus accumbens core Science 292 2001 2499 2501
11. P. Cavedini, G. Riboldi, R. Keller, A. D'Annucci, and L. Bellodi Frontal lobe dysfunction in pathological gambling patients Biol. Psychiatry 51 2002 334 341
12. Y. Chudasama, F. Passetti, S.E.V. Rhodes, D. Lopian, A. Desai, and T.W. Robbins Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity (vol. 146, pg 105, 2003) Behav. Brain Res. 152 2004 453-453
13. L. Clark Decision-making during gambling: an integration of cognitive and psychobiological approaches Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci. 365 2010 319 330
14. L. Clark, A.J. Lawrence, F. Astley-Jones, and N. Gray Gambling near-misses enhance motivation to gamble and recruit win-related brain circuitry Neuron 61 2009 481 490
15. P.J. Cocker, K. Dinelle, R. Kornelson, V. Sossi, and C.A. Winstanley Irrational choice under uncertainty correlates with lower striatal D(2/3) receptor binding in rats J. Neurosci. Off. J. Soc. Neurosci. 32 2012 15450 15457
16. P.J. Cocker, B. Le Foll, R.D. Rogers, and C.A. Winstanley A selective role for dopamine D(4) receptors in modulating reward expectancy in a rodent slot machine task Biol. Psychiatry 75 2014 817-24
17. P.J. Cocker, and C.A. Winstanley Irrational beliefs, biases and gambling: exploring the role of animal models in elucidating vulnerabilities for the development of pathological gambling Behav. Brain Res. 279 2015 259 273
18. D.E. Comings, N. Gonzalez, S. Wu, R. Gade, D. Muhleman, G. Saucier, P. Johnson, R. Verde, R.J. Rosenthal, H.R. Lesieur, L.J. Rugle, W.B. Miller, and J.P. MacMurray Studies of the 48 bp repeat polymorphism of the DRD4 gene in impulsive, compulsive, addictive behaviors: tourette syndrome, ADHD, pathological gambling, and substance abuse Am. J. Med. Genet. 88 1999 358 368
19. D. Cote, A. Caron, J. Aubert, V. Desrochers, and R. Ladouceur Near wins prolong gambling on a video lottery terminal J. Gambl. Stud. Co-sponsored Natl. Counc. Problem Gambl. Inst. Study Gambl. Commer. Gaming 19 2003 433 438
20. P. Di Ciano, A. Pushparaj, A. Kim, J. Hatch, T. Masood, A. Ramzi, M.A. Khaled, I. Boileau, C.A. Winstanley, and B. Le Foll The Impact of selective Dopamine D2, D3 and D4 ligands on the rat gambling task 2015 PloS One 10: e0136267
21. N. Eshel, E.E. Nelson, R.J. Blair, D.S. Pine, and M. Ernst Neural substrates of choice selection in adults and adolescents: development of the ventrolateral prefrontal and anterior cingulate cortices Neuropsychologia 45 2007 1270 1279
22. J.L. Evenden Varieties of impulsivity Psychopharmacology 146 1999 348 361
23. C.D. Fiorillo, P.N. Tobler, and W. Schultz Discrete coding of reward probability and uncertainty by dopamine neurons Science 299 2003 1898 1902
24. S.B. Floresco, S. Ghods-Sharifi, C. Vexelman, and O. Magyar Dissociable roles for the nucleus accumbens core and shell in regulating set shifting J. Neurosci. Off. J. Soc. Neurosci. 26 2006 2449 2457
25. S.B. Floresco, O. Magyar, S. Ghods-Sharifi, C. Vexelman, and M.T. Tse Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 31 2006 297 309
26. S.B. Floresco, J.R. St Onge, S. Ghods-Sharifi, and C.A. Winstanley Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making Cognitive Affect. Behav. Neurosci. 8 2008 375 389
27. P. Gaspar, B. Berger, A. Febvret, A. Vigny, and J.P. Henry Catecholamine innervation of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine-beta-hydroxylase J. Comp. Neurol. 279 1989 249 271
28. F. Grabenhorst, and E.T. Rolls Value, pleasure and choice in the ventral prefrontal cortex Trends Cogn. Sci. 15 2011 56 67
29. J.E. Grant, and S.W. Kim Medication management of pathological gambling Minn. Med. 89 2006 44 48
30. R. Habib, and M.R. Dixon Neurobehavioral evidence for the 'near-miss' effect in pathological gamblers J. Exp. Anal. Behav. 93 2010 313 328
31. C.B. Holroyd, and S.M. McClure Hierarchical control over effortful behavior by rodent medial frontal cortex: a computational model Psychol. Rev. 122 2015 54 83
32. J.G. Hosking, P.J. Cocker, and C.A. Winstanley Dissociable contributions of anterior cingulate cortex and basolateral amygdala on a rodent cost/benefit decision-making task of cognitive effort. Neuropsychopharmcol. Off. Publ. Am. Coll Neuropsychopharmacol 39 2014 1558 1567
33. J.M. Hyman, J. Whitman, E. Emberly, T.S. Woodward, and J.K. Seamans Action and outcome activity state patterns in the anterior cingulate cortex Cereb. Cortex 23 2013 1257 1268
34. J.I. Kassinove, and M.L. Schare Effects of the "near miss" and the "big win" on persistence at slot machine gambling Psychol. Addict. Behav. 15 2001 155 158
35. S.W. Kennerley, and J.D. Wallis Evaluating choices by single neurons in the frontal lobe: outcome value encoded across multiple decision variables Eur. J. Neurosci. 29 2009 2061 2073
36. S.W. Kennerley, M.E. Walton, T.E. Behrens, M.J. Buckley, and M.F. Rushworth Optimal decision making and the anterior cingulate cortex Nat. Neurosci. 9 2006 940 947
37. Z.U. Khan, A. Gutierrez, R. Martin, A. Penafiel, A. Rivera, and A. De La Calle Differential regional and cellular distribution of dopamine D2-like receptors: an immunocytochemical study of subtype-specific antibodies in rat and human brain J. Comp. Neurol. 402 1998 353 371
38. R. Ladouceur, C. Sylvain, C. Boutin, S. Lachance, C. Doucet, J. Leblond, and C. Jacques Cognitive treatment of pathological gambling J. Nerv. Ment. Dis. 189 2001 774 780
39. N.M. Lauzon, T. Ahmad, and S.R. Laviolette Dopamine D4 receptor transmission in the prefrontal cortex controls the salience of emotional memory via modulation of calcium calmodulin-dependent kinase II Cereb. Cortex 22 2012 2486 2494
40. N.M. Lauzon, S.F. Bishop, and S.R. Laviolette Dopamine D1 versus D4 receptors differentially modulate the encoding of salient versus nonsalient emotional information in the medial prefrontal cortex J. Neurosci. Off. J. Soc. Neurosci. 29 2009 4836 4845
41. A.J. Lawrence, J. Luty, N.A. Bogdan, B.J. Sahakian, and L. Clark Problem gamblers share deficits in impulsive decision-making with alcohol-dependent individuals Addiction 104 2009 1006 1015
42. D.A. Lewis The catecholaminergic innervation of primate prefrontal cortex J. Neural Transm. Suppl. 36 1992 179 200
43. X. Liu, J. Hairston, M. Schrier, and J. Fan Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies Neurosci. Biobehav. Rev. 35 2011 1219 1236
44. E. Magno, J.J. Foxe, S. Molholm, I.H. Robertson, and H. Garavan The anterior cingulate and error avoidance J. Neurosci. Off. J. Soc. Neurosci. 26 2006 4769 4773
45. J.P. Marquis, S. Killcross, and J.E. Haddon Inactivation of the prelimbic, but not infralimbic, prefrontal cortex impairs the contextual control of response conflict in rats Eur. J. Neurosci. 25 2007 559 566
46. M. Matsumoto, K. Hidaka, S. Tada, Y. Tasaki, and T. Yamaguchi Low levels of mRNA for dopamine D4 receptor in human cerebral cortex and striatum J. Neurochem. 66 1996 915 919
47. S.F. Miedl, C. Buchel, and J. Peters Cue-Induced Craving increases impulsivity via changes in striatal value signals in problem gamblers J. Neurosci. 34 2014 4750 4755
48. C. Moodie, and F. Finnigan A comparison of the autonomic arousal of frequent, infrequent and non-gamblers while playing fruit machines Addiction 100 2005 51 59
49. L. Mrzljak, C. Bergson, M. Pappy, R. Huff, R. Levenson, and P.S. Goldman-Rakic Localization of dopamine D4 receptors in GABAergic neurons of the primate brain Nature 381 1996 245 248
50. J.L. Muir, B.J. Everitt, and T.W. Robbins The cerebral cortex of the rat and visual attentional function: dissociable effects of mediofrontal, cingulate, anterior dorsolateral, and parietal cortex lesions on a five-choice serial reaction time task Cereb. Cortex 6 1996 470 481
51. W.S. Murch, and L. Clark Games in the brain: neural substrates of gambling addiction Neuroscientist 2015 Jun 26. pii: 1073858415591474. [Epub ahead of print]
52. D. Ongur, and J.L. Price The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans Cereb. Cortex 10 2000 206 219
53. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates 4th ed 1998 Academic Press San Diego xxvi [237] p of platespp
54. M.N. Potenza Should addictive disorders include non-substance-related conditions? Addiction 101 Suppl. 1 2006 142 151
55. M.N. Potenza Impulsivity and compulsivity in pathological gambling and obsessive-compulsive disorder Rev. Bras. Psiquiatr. 29 2007 105 106
56. M.N. Potenza Review. The neurobiology of pathological gambling and drug addiction: an overview and new findings Philos. Trans. R. Soc. Lond. Ser. B, Biol. Sci. 363 2008 3181 3189
57. R.L. Reid The psychology of the near miss J. Gambl. Behav. 2 1986 32 39
58. J. Reuter, T. Raedler, M. Rose, I. Hand, J. Glascher, and C. Buchel Pathological gambling is linked to reduced activation of the mesolimbic reward system Nat. Neurosci. 8 2005 147 148
59. J.V. Richardson, and A. Baron Avoidance of timeout from response-independent food: effects of delivery rate and quality J. Exp. Anal. Behav. 89 2008 169 181
60. M.F. Rushworth, M.J. Buckley, T.E. Behrens, M.E. Walton, and D.M. Bannerman Functional organization of the medial frontal cortex Curr. Opin. Neurobiol. 17 2007 220 227
61. R. Shao, J. Read, T.E.J. Behrens, and R.D. Rogers Shifts in reinforcement signalling while playing slot-machines as a function of prior experience and impulsivity (vol. 3, e235, 2013) Transl. Psychiatry 3 2013
62. A. Shenhav, M.A. Straccia, J.D. Cohen, and M.M. Botvinick Anterior cingulate engagement in a foraging context reflects choice difficulty, not foraging value Nat. Neurosci. 17 2014 1249 1254
63. J.R. St Onge, and S.B. Floresco Dopaminergic modulation of risk-based decision making Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 34 2009 681 697
64. C. Sylvain, R. Ladouceur, and J.M. Boisvert Cognitive and behavioral treatment of pathological gambling: a controlled study J. Consult. Clin. Psychol. 65 1997 727 732
65. S.L. Vincent, Y. Khan, and F.M. Benes Cellular distribution of dopamine D1 and D2 receptors in rat medial prefrontal cortex J. Neurosci. 13 1993 2551 2564
66. B.A. Vogt, P.R. Hof, K. Zilles, L.J. Vogt, C. Herold, and N. Palomero-Gallagher Cingulate area 32 homologies in mouse, rat, macaque and human: cytoarchitecture and receptor architecture J. Comp. Neurol. 521 2013 4189 4204
67. K.N. Westlund, S.M. Carlton, D. Zhang, and W.D. Willis Direct catecholaminergic innervation of primate spinothalamic tract neurons J. Comp. Neurol. 299 1990 178 186
68. C.A. Winstanley, P.J. Cocker, and R.D. Rogers Dopamine modulates reward expectancy during performance of a slot machine task in rats: evidence for a 'near-miss' effect Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 36 2011 913 925
69. E.Y. Yuen, P. Zhong, and Z. Yan Homeostatic regulation of glutamatergic transmission by dopamine D4 receptors Proc. Natl. Acad. Sci. U. S. A. 107 2010 22308 22313
70. F.D. Zeeb, T.W. Robbins, and C.A. Winstanley Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task Neuropsychopharmacol. Off. Publ. Am. Coll. Neuropsychopharmacol. 34 2009 2329 2343