Role of dopamine D2 receptors in human reinforcement learning

Neuropsychopharmacology

Volumn 39, Issue 10, 2014, Pages 2366-2375

  Eisenegger, Christoph ^a,b   Naef, Michael ^c   Linssen, Anke ^d   Clark, Luke ^a,e   Gandamaneni, Praveen K ^e   Müller, Ulrich ^a,f   Robbins, Trevor W ^a,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF LONDON   (United Kingdom)

^d MAASTRICHT UNIVERSITY   (Netherlands)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^f CAMBRIDGESHIRE AND PETERBOROUGH NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE 2 RECEPTOR; PROLACTIN; SULPIRIDE; DOPAMINE 3 RECEPTOR; DOPAMINE RECEPTOR BLOCKING AGENT; DRD2 PROTEIN, HUMAN;

ADULT; ARTICLE; AVOIDANCE BEHAVIOR; GENETIC ANALYSIS; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; MENTAL PERFORMANCE; NORMAL HUMAN; PRIORITY JOURNAL; PROLACTIN BLOOD LEVEL; PROTEIN BLOOD LEVEL; RECEPTOR DENSITY; REINFORCEMENT; VOLUNTEER; ANTAGONISTS AND INHIBITORS; BLOOD; CONTROLLED STUDY; DECISION MAKING; DOUBLE BLIND PROCEDURE; DRUG EFFECTS; GENETIC POLYMORPHISM; GENETICS; GENOTYPE; GENOTYPING TECHNIQUE; METABOLISM; NEUROPSYCHOLOGICAL TEST; PHYSIOLOGY; PSYCHOLOGICAL MODEL; RANDOMIZED CONTROLLED TRIAL; REACTION TIME; YOUNG ADULT;

ADULT; CHOICE BEHAVIOR; DOPAMINE ANTAGONISTS; DOUBLE-BLIND METHOD; GENOTYPE; GENOTYPING TECHNIQUES; HUMANS; MALE; MODELS, PSYCHOLOGICAL; NEUROPSYCHOLOGICAL TESTS; POLYMORPHISM, GENETIC; PROLACTIN; REACTION TIME; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; REINFORCEMENT (PSYCHOLOGY); SULPIRIDE; YOUNG ADULT;

EID: 84906324241     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2014.84     Document Type: Article

References (71)

1. Ahlenius S, Engel J, Zoller M (1977). Effects of apomorphine and haloperidol on exploratory-behavior and latent learning in mice. Phys Psychol 5: 290-294
2. Bai JS, Perron P (1998). Estimating and testing linear models with multiple structural changes. Econometrica 66: 47-78
3. Bardgett ME, Depenbrock M, Downs N, Points M, Green L (2009). Dopamine modulates effort-based decision making in rats. Behav Neurosci 123: 242-251
4. Bayer HM, Glimcher PW (2005). Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47: 129-141
5. Beninger RJ, Phillips AG (1981). The effects of pimozide during pairing on the transfer of classical conditioning to an operant discrimination. Pharmacol Biochem Behav 14: 101-105
6. Berridge KC, Robinson TE (1998). What is the role of dopamine in reward: Hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28: 309-369
7. Blackburn JR, Phillips AG, Fibiger HC (1987). Dopamine and preparatory behavior: I. effects of pimozide. Behav Neurosci 101: 352-360
8. Bond A, Lader M (1974). Use of analog scales in rating subjective feelings. Br J Med Psychol 47: 211-218
9. Bressan RA, Erlandsson K, Jones HM, Mulligan R, Flanagan RJ, Ell PJ et al (2003). Is regionally selective D2/D3 dopamine occupancy sufficient for atypical antipsychotic effect? An in vivo quantitative [123I]epidepride SPET study of amisulpride-Treated patients. Am J Psychiatry 160: 1413-1420
10. Brischoux F, Chakraborty S, Brierley DI, Ungless MA (2009). Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci USA 106: 4894-4899
11. Calabresi P, Centonze D, Gubellini P, Marfia GA, Pisani A, Sancesario G et al (2000). Synaptic transmission in the striatum: From plasticity to neurodegeneration. Prog Neurobiol 61: 231-265
12. Chowdhury R, Guitart-Masip M, Lambert C, Dayan P, Huys Q, Duzel E et al (2013). Dopamine restores reward prediction errors in old age. Nat Neurosci 16: 648-653
13. Cohen MX, Krohn-Grimberghe A, Elger CE, Weber B (2007). Dopamine gene predicts the brain's response to dopaminergic drug. Eur J Neurosci 26: 3652-3660
14. Daw ND, Kakade S, Dayan P (2002). Opponent interactions between serotonin and dopamine. Neural Netw 15: 603-616
15. Dodds CM, Clark L, Dove A, Regenthal R, Baumann F, Bullmore E et al (2009). The dopamine D2 receptor antagonist sulpiride modulates striatal BOLD signal during the manipulation of information in working memory. Psychopharmacology (Berl) 207: 35-45
16. Dreyer JK, Herrik KF, Berg RW, Hounsgaard JD (2010). Influence of phasic and tonic dopamine release on receptor activation. J Neurosci 30: 14273-14283
17. Eisenegger C, Knoch D, Ebstein RP, Gianotti LRR, Sandor PS, Fehr E (2010). Dopamine receptor D4 polymorphism predicts the effect of L-DOPA on gambling behavior. Biol Psychiatry 67: 702-706
18. Eisenegger C, Pedroni A, Rieskamp J, Zehnder C, Ebstein R, Fehr E et al (2013). DAT1 polymorphism determines L-DOPA effects on learning about others' prosociality. PLoS One 8: E67820
19. Frank MJ (2005). Dynamic dopamine modulation in the basal ganglia: A neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. J Cogn Neurosci 17: 51-72
20. Frank MJ, Fossella JA (2008). Neurogenetics and pharmacology of learning, motivation, and cognition. Neuropsychopharmacology 36: 133-152
21. Frank MJ, Seeberger LC, O'Reilly RC (2004). By carrot or by stick: Cognitive reinforcement learning in parkinsonism. Science 306: 1940-1943
22. Glimcher PW (2011). Understanding dopamine and reinforcement learning: The dopamine reward prediction error hypothesis. Proc Natl Acad Sci USA 108(Suppl 3): 15647-15654
23. Goto Y, Grace AA (2005). Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat Neurosci 8: 805-812
24. Ikemoto S, Panksepp J (1999). The role of nucleus accumbens dopamine in motivated behavior: A unifying interpretation with special reference to reward-seeking. Brain Res Brain Res Rev 31: 6-41
25. Jocham G, Klein TA, Neumann J, von Cramon DY, Reuter M, Ullsperger M (2009). Dopamine DRD2 polymorphism alters reversal learning and associated neural activity. J Neurosci 29: 3695-3704
26. Jocham G, Klein TA, Ullsperger M (2011). Dopamine-mediated reinforcement learning signals in the striatum and ventromedial prefrontal cortex underlie value-based choices. J Neurosci 31: 1606-1613
27. Jonsson EG, Nothen MM, Grunhage F, Farde L, Nakashima Y, Propping P et al (1999). Polymorphisms in the dopamine D2 receptor gene and their relationships to striatal dopamine receptor density of healthy volunteers. Mol Psychiatry 4: 290-296
28. Judd CM, McClelland GH (1989). Data Analysis, A Model-Comparison Approach Orlando, FL, USA
29. Kapur S (2003). Psychosis as a state of aberrant salience: A framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiat 160: 13-23
30. Kirsch P, Reuter M, Mier D, Vaitl D, Hennig J (2005). Imaging gene-substance interactions: The effect of the DRD2 Taq 1A polymorphism and the dopamine agonist bromocriptine on the brain activation during the anticipation of reward. J Psychophysiol 19: 126-126
31. Klein TA, Neumann J, Reuter M, Hennig J, von Cramon DY, Ullsperger M (2007). Genetically determined differences in learning from errors. Science 318: 1642-1645
32. Lammel S, Ion DI, Roeper J, Malenka RC (2011). Projectionspecific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70: 855-862
33. Lex B, Hauber W (2010). The role of nucleus accumbens dopamine in outcome encoding in instrumental and Pavlovian conditioning. Neurobiol Learn Mem 93: 283-290
34. Lovinger DM (2012). Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58: 951-961
35. Matsumoto M, Hikosaka O (2009). Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459: 837-U834
36. McCabe C, Huber A, Harmer CJ, Cowen PJ (2011). The D2 antagonist sulpiride modulates the neural processing of both rewarding and aversive stimuli in healthy volunteers. Psychopharmacology 217: 271-278
37. Mehta MA, Hinton EC, Montgomery AJ, Bantick RA, Grasby PM (2005). Sulpiride and mnemonic function: Effects of a dopamine D2 receptor antagonist on working memory, emotional memory and long-Term memory in healthy volunteers. J psychopharmacol 19: 29-38
38. Mehta MA, McGowan SW, Lawrence AD, Aitken MR, Montgomery AJ, Grasby PM (2003). Systemic sulpiride modulates striatal blood flow: Relationships to spatial working memory and planning. Neuroimage 20: 1982-1994
39. Mehta MA, Montgomery AJ, Kitamura Y, Grasby PM (2008). Dopamine D2 receptor occupancy levels of acute sulpiride challenges that produce working memory and learning impairments in healthy volunteers. Psychopharmacology 196: 157-165
40. Mirenowicz J, Schultz W (1996). Preferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli. Nature 379: 449-451
41. Montague PR, Dayan P, Sejnowski TJ (1996). A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J Neurosci 16: 1936-1947
42. Morris G, Nevet A, Arkadir D, Vaadia E, Bergman H (2006). Midbrain dopamine neurons encode decisions for future action. Nat Neurosci 9: 1057-1063
43. Niv Y (2007). Cost, benefit, tonic, phasic: What do response rates tell us about dopamine and motivation? Ann N Y Acad Sci 1104: 357-376
44. Palminteri S, Lebreton Ml, Worbe Y, Grabli D, Hartmann A, Pessiglione M (2009). Pharmacological modulation of subliminal learning in Parkinson's and Tourette's syndromes. Proc Natl Acad Sci USA 106: 19179-19184
45. Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD (2006). Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442: 1042-1045
46. Pizzagalli DA, Evins AE, Schetter EC, Frank MJ, Pajtas PE, Santesso DL et al (2008). Single dose of a dopamine agonist impairs reinforcement learning in humans: Behavioral evidence from a laboratory-based measure of reward responsiveness. Psychopharmacology (Berl) 196: 221-232
47. Pohjalainen T, Rinne JO, Nagren K, Lehikoinen P, Anttila K, Syvalahti EK et al (1998). The A1 allele of the human D2 dopamine receptor gene predicts low D2 receptor availability in healthy volunteers. Mol Psychiatry 3: 256-260
48. Riba J, Kramer UM, Heldmann M, Richter S, Munte TF (2008). Dopamine agonist increases risk taking but blunts rewardrelated brain activity. PLoS One 3: E2479
49. Rice ME, Cragg SJ (2008). Dopamine spillover after quantal release: Rethinking dopamine transmission in the nigrostriatal pathway. Brain Res Rev 58: 303-313
50. Ritchie T, Noble EP (1996). [3H]naloxone binding in the human brain: Alcoholism and the TaqI A D2 dopamine receptor polymorphism. Brain Res 718: 193-197
51. Ritchie T, Noble EP (2003). Association of seven polymorphisms of the D2 dopamine receptor gene with brain receptor-binding characteristics. Neurochem Res 28: 73-82
52. Robbins TW, Everitt BJ (1992). Functions of dopamine in the dorsal and ventral striatum. Semin Neurosci 4: 119-127
53. Rush CR, Stoops WW, Hays LR, Glaser PEA, Hays LS (2003). Risperidone attenuates the discriminative-stimulus effects of d-Amphetamine in humans. J Pharmacol Exp Ther 306: 195-204
54. Salamone JD (1994). The involvement of nucleus accumbens dopamine in appetitive and aversive motivation. Behav Brain Res 61: 117-133
55. Schultz W (1998). Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1-27
56. Schultz W (2002). Getting formal with dopamine and reward. Neuron 36: 241-263
57. Schultz W, Dayan P, Montague PR (1997). A neural substrate of prediction and reward. Science 275: 1593-1599
58. Seamans JK, Durstewitz D, Christie BR, Stevens CF, Sejnowski TJ (2001). Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. Proc Natl Acad Sci USA 98: 301-306
59. Shiner T, Seymour B, Wunderlich K, Hill C, Bhatia KP, Dayan P et al (2012). Dopamine and performance in a reinforcement learning task: Evidence from Parkinson's disease. Brain 135: 1871-1883
60. Smittenaar P, Chase HW, Aarts E, Nusselein B, Bloem BR, Cools R (2012). Decomposing effects of dopaminergic medication in Parkinson's disease on probabilistic action selection-learning or performance? Eur J Neurosci 35: 1144-1151
61. Sutton RS, Barto AG (1998). Reinforcement learning: An introduction. IEEE Trans Neural Netw 9: 1054-1054
62. Takano A, Suhara T, Yasuno F, Suzuki K, Takahashi H, Morimoto T et al (2006). The antipsychotic sultopride is overdosed-A PET study of drug-induced receptor occupancy in comparison with sulpiride. Int J Neuropsychopharmacol 9: 539-545
63. Thompson J, Thomas N, Singleton A, Piggott M, Lloyd S, Perry EK et al (1997). D2 dopamine receptor gene (DRD2) Taq1 A polymorphism: Reduced dopamine D2 receptor binding in the human striatum associated with the A1 allele. Pharmacogenetics 7: 479-484
64. Treadway MT, Zald DH (2013). Parsing anhedonia: Translational models of reward-processing deficits in psychopathology. Curr Dir Psychol Sci 22: 244-249
65. Van Der Schaaf ME, van Schouwenburg MR, Geurts DE, Schellekens AF, Buitelaar JK, Verkes RJ et al (2012). Establishing the dopamine dependency of human striatal signals during reward and punishment reversal learning. Cereb Cortex 24: 633-642
66. Voon V, Pessiglione M, Brezing C, Gallea C, Fernandez HH, Dolan RJ et al (2010). Mechanisms underlying dopaminemediated reward bias in compulsive behaviors. Neuron 65: 135-142
67. Wang J, O'Donnell P (2001). D(1) dopamine receptors potentiate nmda-mediated excitability increase in layer V prefrontal cortical pyramidal neurons. Cereb Cortex 11: 452-462
68. Wise RA (2004). Dopamine, learning and motivation. Nat Rev Neurosci 5: 483-494
69. Wise RA, Rompre PP (1989). Brain dopamine and reward. Annu Rev Psychol 40: 191-225
70. Xiberas X, Martinot JL, Mallet L, Artiges E, Canal M, Loc'h C et al (2001). In vivo extrastriatal and striatal D2 dopamine receptor blockade by amisulpride in schizophrenia. J Clin Psychopharmacol 21: 207-214
71. Zweifel LS, Parker JG, Lobb CJ, Rainwater A, Wall VZ, Fadok JP et al (2009). Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopaminedependent behavior. Proc Natl Acad Sci USA 106: 7281-7288