Establishing the dopamine dependency of human striatal signals during reward and punishment reversal learning

Cerebral Cortex

Volumn 24, Issue 3, 2014, Pages 633-642

  Van Der Schaaf, Marieke E ^a,b   Van Schouwenburg, Martine R ^a,b   Geurts, Dirk E M ^a,b   Schellekens, Arnt F A ^b   Buitelaar, Jan K ^c   Verkes, Robbert Jan ^b   Cools, Roshan ^a,b  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b Department of Psychiatry ^*  (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

bromocriptine; dopamine; pharmacological functional magnetic resonance imaging; striatum; sulpiride

Indexed keywords

BROMOCRIPTINE; DOPAMINE; PHARMACOLOGICAL FUNCTIONAL MAGNETIC RESONANCE IMAGING; STRIATUM; SULPIRIDE;

ADULT; BLOOD PRESSURE; BROMOCRIPTINE; CORPUS STRIATUM; DOPAMINE AGENTS; DOUBLE-BLIND METHOD; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MALE; MEMORY, SHORT-TERM; NEUROPSYCHOLOGICAL TESTS; OXYGEN; PHOTIC STIMULATION; PUNISHMENT; REVERSAL LEARNING; REWARD; SULPIRIDE; YOUNG ADULT;

EID: 84894270748     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs344     Document Type: Article

References (62)

1. Barch D, Ceaser A. 2011. Cognition in schizophrenia: core psychological and neural mechanisms. Trends Cogn Sci. 16:27-34.
2. Bodi N, Keri S, Nagy H, Moustafa A, Myers CE, Daw N, Dibo G, Takats A, Bereczki D, Gluck MA. 2009. Reward-learning and the novelty-seeking personality: a between-and within-subjects study of the effects of dopamine agonists on young Parkinson's patients. Brain. 132:2385-2395.
3. Bond AL, Lader M. 1974. The use of analogue scales in rating subjective feelings. Br J Med Psychol. 47:211-218.
4. Bray S, Shimojo S, O'Doherty J. 2010. Human medial orbitofrontal cortex is recruited during experience of imagined and real rewards. J Neurophysiol. 103:2506-2518.
5. Brett M, Anton JL, Valabregue R, Poline JB. 2002. Region of interest analysis using an SPM toolbox. International Conference on Functional Mapping of the Human Brain. Sendai, Japan.
6. Cools R. 2011. Dopaminergic control of the striatum for high-level cognition. Curr Opin Neurobiol. 21:402-407.
7. Cools R, Altamirano L, D'Esposito M. 2006. Reversal learning in Parkinson's disease depends on medication status and outcome valence. Neuropsychologia. 44:1663-1673.
8. Cools R, D'Esposito M. 2011. Inverted-u-shaped dopamine actions on human working memory and cognitive control. Biol Psychiatry. 69:e113-125.
9. Cools R, Frank MJ, Gibbs SE, Miyakawa A, Jagust W, D'Esposito M. 2009. Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. J Neurosci. 29:1538-1543.
10. Cools R, Gibbs SE, Miyakawa A, Jagust W, D'Esposito M. 2008. Working memory capacity predicts dopamine synthesis capacity in the human striatum. J Neurosci. 28:1208-1212.
11. Cools R, Lewis SJ, Clark L, Barker RA, Robbins TW. 2007. L-DOPA disrupts activity in the nucleus accumbens during reversal learning in Parkinson's disease. Neuropsychopharmacology. 32:180-189.
12. Deleu D, Northway MG, Hanssens Y. 2002. Clinical pharmacokinetic and pharmacodynamic properties of drugs used in the treatment of Parkinson's disease. Clin Pharmacokinet. 41:261-309.
13. Delgado MR, Li J, Schiller D, Phelps EA. 2008. The role of the striatum in aversive learning and aversive prediction errors. Philos Trans R Soc Lond B Biol Sci. 363:3787-3800.
14. Dickinson A, Smith J, Mirenowicz J. 2000. Dissociation of Pavlovian and instrumental incentive learning under dopamine antagonists. Behav Neurosci. 114:468-483.
15. Dodds CM, Clark L, Dove A, Regenthal R, Baumann F, Bullmore E, Robbins TW, Muller U. 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. Dodds CM, Muller U, Clark L, van Loon A, Cools R, Robbins TW. 2008. Methylphenidate has differential effects on blood oxygenation level-dependent signal related to cognitive subprocesses of reversal learning. J Neurosci. 28:5976-5982.
17. Duzel E, Bunzeck N, Guitart-Masip M, Wittmann B, Schott BH, Tobler PN. 2009. Functional imaging of the human dopaminergic midbrain. Trends Neurosci. 32:321-328.
18. Feldman RS, Meyer JS, Quenzer LF. 1997. Principles of neuropsychopharmacology. Sunderland (MA): Sinauer Associates, Inc.
19. Fitzgerald P, Dinan TG. 2008. Prolactin and dopamine: what is the connection? A review article. J Psychopharmacol. 22:12-19.
20. Flagel SB, Clark JJ, Robinson TE, Mayo L, Czuj A, Willuhn I, Akers CA, Clinton SM, Phillips PE, Akil H. 2011. A selective role for dopamine in stimulus-reward learning. Nature. 469:53-57.
21. Frank M, Fossella J. 2011. Neurogenetics and pharmacology of learning, motivation, and cognition. Neuropsychopharmacology. 36:133-185.
22. Frank M, O'Reilly R. 2006. A mechanistic account of striatal dopamine function in human cognition: psychopharmacological studies with cabergoline and haloperidol. Behav Neurosci. 120:497-1014.
23. 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.
24. Frank MJ, Hutchison K. 2009. Genetic contributions to avoidancebased decisions: striatal D2 receptor polymorphisms. Neuroscience. 164:131-140.
25. Frank MJ, Moustafa AA, Haughey HM, Curran T, Hutchison KE. 2007. Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning. Proc Natl Acad Sci USA. 104:16311-16316.
26. Frank MJ, Samanta J, Moustafa AA, Sherman SJ. 2007. Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science. 318:1309-1312.
27. Frank MJ, Santamaria A, O'Reilly RC, Willcutt E. 2007. Testing computational models of dopamine and noradrenaline dysfunction in attention deficit/hyperactivity disorder. Neuropsychopharmacology. 32:1583-1599.
28. Frank MJ, Seeberger LC, O'Reilly RC. 2004. By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science (New York, NY). 306:1940-1943.
29. Griswold MA, Jakob PM, Heidemann RM, Nittka M, Jellus V, Wang J, Kiefer B, Haase A. 2002. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med. 47:1202-1210.
30. Groth-Marnat G. 1997. The Wechsler Intelligence Scales. In: Handbook of psychological assessment. Hoboken, NJ, NCA: John Wiley & Sons, Inc. p. 175-176.
31. Howell DC. 1997. Statistical methods for psychology. Belmont, USA: Wadsworth Publishing Company.
32. Jensen J, Smith AJ, Willeit M, Crawley AP, Mikulis DJ, Vitcu I, Kapur S. 2007. Separate brain regions code for salience vs. valence during reward prediction in humans. Hum Brain Mapp. 28:294-302.
33. 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.
34. Kapur S, Mizrahi R, Li M. 2005. From dopamine to salience to psychosis-linking biology, pharmacology and phenomenology of psychosis. Schizophr Res. 79:59-127.
35. Kimberg DY, D'Esposito M, Farah MJ. 1997. Effects of bromocriptine on human subjects depend on working memory capacity. Neuroreport. 8:3581-3585.
36. Knutson B, Gibbs SE. 2007. Linking nucleus accumbens dopamine and blood oxygenation. Psychopharmacology (Berl). 191:813-822.
37. Landau SM, Lal R, O'Neil JP, Baker S, Jagust WJ. 2009. Striatal dopamine and working memory. Cereb Cortex. 19:445-454.
38. Matsumoto M, Hikosaka O. 2009. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature. 459:837-841.
39. Mehta M, McGowan S, Lawrence A, Aitken M, Montgomery A, Grasby P. 2003. Systemic sulpiride modulates striatal blood flow: relationships to spatial working memory and planning. Neuroimage. 20:1982-1994.
40. Mehta MA, Manes FF, Magnolfi G, Sahakian BJ, Robbins TW. 2004. Impaired set-shifting and dissociable effects on tests of spatial working memory following the dopamine D2 receptor antagonist sulpiride in human volunteers. Psychopharmacology (Berl). 176:331-342.
41. 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 (Berl). 196:157-165.
42. Miyapuram K, Tobler P, Gregorios-Pippas L, Schultz W. 2012. BOLD responses in reward regions to hypothetical and imaginary monetary rewards. Neuroimage. 59:1692-1701.
43. Morrison P, Murray R. 2009. From real-world events to psychosis: the emerging neuropharmacology of delusions. Schizophr Bull. 35:668-742.
44. Moustafa AA, Cohen MX, Sherman SJ, Frank MJ. 2008. A role for dopamine in temporal decision making and reward maximization in Parkinsonism. J Neurosci. 28:12294-12304.
45. Ott D, Ullsperger M, Jocham G, Neumann J, Klein T. 2011. Continuous theta-burst stimulation (cTBS) over the lateral prefrontal cortex alters reinforcement learning bias. Neuroimage. 57:617-640.
46. Palminteri S, Lebreton M, 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.
47. 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.
48. Redgrave P, Prescott TJ, Gurney K. 1999. Is the short-latency dopamine response too short to signal reward error? Trends Neurosci. 22:146-151.
49. Robinson OJ, Frank MJ, Sahakian BJ, Cools R. 2010. Dissociable responses to punishment in distinct striatal regions during reversal learning. Neuroimage. 51:1459-1467.
50. Salthouse TA, Babcock RL, Shaw RJ. 1991. Effects of adult age on structural and operational capacities in working memory. Psychol Aging. 6:118-127.
51. Santesso D, Evins A, Frank M, Schetter E, Bogdan R, Pizzagalli D. 2009. Single dose of a dopamine agonist impairs reinforcement learning in humans: evidence from event-related potentials and computational modeling of striatal-cortical function. Hum Brain Mapp. 30:1963-1976.
52. Schott BH, Minuzzi L, Krebs RM, Elmenhorst D, Lang M, Winz OH, Seidenbecher CI, Coenen HH, Heinze HJ, Zilles K et al. 2008. Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. J Neurosci. 28:14311-14319.
53. Seymour B, Daw N, Dayan P, Singer T, Dolan R. 2007. Differential encoding of losses and gains in the human striatum. J Neurosci. 27:4826-4831.
54. Seymour B, O'Doherty JP, Koltzenburg M, Wiech K, Frackowiak R, Friston K, Dolan R. 2005. Opponent appetitive-aversive neural processes underlie predictive learning of pain relief. Nat Neurosci. 8:1234-1240.
55. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M. 2002. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage. 15:273-289.
56. van der Schaaf ME, Warmerdam E, Crone EA, Cools R. 2011. Distinct linear and non-linear trajectories of reward and punishment reversal learning during development: relevance for dopamine's role in adolescent decision making. Dev Cogn Neurosci. 1:578-590.
57. van Holstein M, Aarts E, van der Schaaf ME, Geurts DE, Verkes RJ, Franke B, van Schouwenburg MR, Cools R. 2011. Human cognitive flexibility depends on dopamine D2 receptor signaling. Psychopharmacology (Berl). 218:578-578.
58. Verhagen L, Dijkerman H, Grol M, Toni I. 2008. Perceptuo-motor interactions during prehension movements. J Neurosci. 28:4726-4761.
59. Voon V, Pessiglione M, Brezing C, Gallea C, Fernandez HH, Dolan RJ, Hallett M. 2010. Mechanisms underlying dopamine-mediated reward bias in compulsive behaviors. Neuron. 65:135-142.
60. Voon V, Reynolds B, Brezing C, Gallea C, Skaljic M, Ekanayake V, Fernandez H, Potenza MN, Dolan RJ, Hallett M. 2010. Impulsive choice and response in dopamine agonist-related impulse control behaviors. Psychopharmacology (Berl). 207:645-659.
61. Wyvell CL, Berridge KC. 2000. Intra-accumbens amphetamine increases the conditioned incentive salience of sucrose reward: enhancement of reward "wanting" without enhanced "liking" or response reinforcement. J Neurosci. 20:8122-8130.
62. Zink CF, Pagnoni G, Martin ME, Dhamala M, Berns GS. 2003. Human striatal response to salient nonrewarding stimuli. J Neurosci. 23:8092-8097.