Striatal D1 and D2 signaling differentially predict learning from positive and negative outcomes

NeuroImage

Volumn 109, Issue , 2015, Pages 95-101

  Cox, Sylvia M L ^a,b   Frank, Michael J ^c   Larcher, Kevin ^a,b   Fellows, Lesley K ^a   Clark, Crystal A ^a   Leyton, Marco ^b   Dagher, Alain ^a  

^a MCGILL UNIVERSITY   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c BROWN UNIVERSITY   (United States)

Author keywords

Dopamine; Learning; Positron emission tomography; Reinforcement; Striatum

Indexed keywords

DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; RADIOLIGAND; TYROSINE;

ADULT; ARTICLE; AVOIDANCE BEHAVIOR; CAUDATE NUCLEUS; CORPUS STRIATUM; DECISION MAKING; FEMALE; HUMAN; LEARNING; MALE; MATHEMATICAL ANALYSIS; MEASUREMENT ACCURACY; MENTAL TASK; NEUROIMAGING; NORMAL HUMAN; POSITRON EMISSION TOMOGRAPHY; PREDICTIVE VALUE; PROBABILISTIC SELECTION TASK; PUTAMEN; RECEPTOR BINDING; REWARD; SIGNAL TRANSDUCTION; METABOLISM; NEOSTRIATUM; PHYSIOLOGY; REINFORCEMENT; SCINTISCANNING; YOUNG ADULT;

ADULT; AVOIDANCE LEARNING; CHOICE BEHAVIOR; FEMALE; HUMANS; MALE; NEOSTRIATUM; POSITRON-EMISSION TOMOGRAPHY; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; REINFORCEMENT (PSYCHOLOGY); YOUNG ADULT;

EID: 84921728992     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.12.070     Document Type: Article

References (62)

1. Ad-Dab'bagh Y., Einarson D., Lyttelton O., Muehlboeck J.-S., Mok K., Ivanov O., Vincent R.D., Lepage C., Lerch J., Fombonne E., Evans A.C. The CIVET image-processing environment: a fully automated comprehensive pipeline for anatomical neuroimaging research. Organization for Human Brain Mapping 2006, (Florence).
2. Bayer H.M., Glimcher P.W. Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 2005, 47:129-141.
3. Beeler J.A., Frank M.J., McDaid J., Alexander E., Turkson S., Bernandez M.S., McGehee D.S., Zhuang X. A role for dopamine-mediated learning in the pathophysiology and treatment of Parkinson's disease. Cell Rep. 2012, 2:1747-1761.
4. Brodnik Z., Double M., Jaskiw G.E. Presynaptic regulation of extracellular dopamine levels in the medial prefrontal cortex and striatum during tyrosine depletion. Psychopharmacology 2013, 227:363-371.
5. Bromberg-Martin E.S., Matsumoto M., Hikosaka O. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 2010, 68:815-834.
6. Chou Y.H., Karlsson P., Halldin C., Olsson H., Farde L. A PET study of D1-like dopamine receptor ligand binding. Psychopharmacology 1999, 146:220-227.
7. Clark L., Stokes P.R., Wu K., Michalczuk R., Benecke A., Watson B.J., Egerton A., Piccini P., Nutt D.J., Bowden-Jones H., Lingford-Hughes A.R. Striatal dopamine D2/D3 receptor binding in pathological gambling is correlated with mood-related impulsivity. NeuroImage 2012, 63:40-46.
8. Collins D.L., Evans A.C. Animal: validation and applications of nonlinear registration-based segmentation. Int. J. Pattern Recognit. Artif. Intell. 1997, 11.
9. Collins A.G., Frank M.J. Opponent actor learning (OpAL): modeling interactive effects of striatal dopamine on reinforcement learning and choice incentive. Psychol. Rev. 2014, 121:337-366.
10. Collins G.T., Woods J.H. Influence of conditioned reinforcement on the response-maintaining effects of quinpirole in rats. Behav. Pharmacol. 2009, 20:492-504.
11. Collins D.L., Neelin P., Peters T.M., Evans A.C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 1994, 18:192-205.
12. Comtat C., Bataille F., Michel C., Jones J.P., Sibomana M., Janeiro L., Trebossen R. OSEM-3D reconstruction strategies for the ECAT HRRT. IEEE Nucleur Science Symposium Conference Record 2004, 6:3492-3496.
13. Cools R., Altamirano L., D'Esposito M. Reversal learning in Parkinson's disease depends on medication status and outcome valence. Neuropsychologia 2006, 44:1663-1673.
14. Costes N., Dagher A., Larcher K., Evans A.C., Collins D.L., Reilhac A. Motion correction of multi-frame PET data in neuroreceptor mapping: simulation based validation. NeuroImage 2009, 47:1496-1505.
15. Dagher A., Robbins T. Personality, addiction, dopamine: insights from Parkinson's disease. Neuron 2009, 61:502-510.
16. Daw N.D., Kakade S., Dayan P. Opponent interactions between serotonin and dopamine. Neural Netw. 2002, 15:603-616.
17. Doll B.B., Hutchison K.E., Frank M.J. Dopaminergic genes predict individual differences in susceptibility to confirmation bias. J. Neurosci. 2011, 31:6188-6198.
18. Dreyer J.K., Herrik K.F., Berg R.W., Hounsgaard J.D. Influence of phasic and tonic dopamine release on receptor activation. J. Neurosci. 2010, 30:14273-14283.
19. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structural Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-patient Edition (SCID-I/NP) 2002, Biometrics Research, New York State Psychiatric Institute, New York, (November).
20. Fonov V.S., Evans A.C., McKinstry R.C., Almli C.R., Collins D.L. Unbiased nonlinear average age-appropriate brain templates from birth to adulthood. Organization for Human Brain Mapping 2009, S102.
21. Frank M.J. Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. J. Cogn. Neurosci. 2005, 17:51-72.
22. Frank M.J., Hutchison K. Genetic contributions to avoidance-based decisions: striatal D2 receptor polymorphisms. Neuroscience 2009, 164:131-140.
23. Frank M.J., O'Reilly R.C. A mechanistic account of striatal dopamine function in human cognition: psychopharmacological studies with cabergoline and haloperidol. Behav. Neurosci. 2006, 120:497-517.
24. Frank M.J., Seeberger L.C., O'Reilly R.C. By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 2004, 306:1940-1943.
25. Frank M.J., Scheres A., Sherman S.J. Understanding decision-making deficits in neurological conditions: insights from models of natural action selection. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2007, 362:1641-1654.
26. Frank M.J., Moustafa A.A., Haughey H.M., Curran T., Hutchison K.E. Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:16311-16316.
27. Frank M.J., Doll B.B., Oas-Terpstra J., Moreno F. Prefrontal and striatal dopaminergic genes predict individual differences in exploration and exploitation. Nat. Neurosci. 2009, 12:1062-1068.
28. Gjedde A., Kumakura Y., Cumming P., Linnet J., Moller A. Inverted-U-shaped correlation between dopamine receptor availability in striatum and sensation seeking. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3870-3875.
29. 2+ currents and excitability via a novel PLCβ1-IP3-calcineurin-signaling cascade. J. Neurosci. 2000, 20:8987-8995.
30. Jocham G., Klein T., Neumann J., von Cramon D., Reuter M., Ullsperger M. Dopamine DRD2 polymorphism alters reversal learning and associated neural activity. J. Neurosci. 2009, 29:3695-3704.
31. Kravitz A., Tye L., Kreitzer A. Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat. Neurosci. 2012, 15:816-818.
32. Lammertsma A.A., Hume S.P. Simplified reference tissue model for PET receptor studies. NeuroImage 1996, 4:153-158.
33. Laruelle M., D'Souza C., Baldwin R., Abi-Dargham A., Kanes S., Fingado C., Seibyl J., Zoghbi S., Bowers M., Jatlow P., Charney D., Innis R. Imaging D2 receptor occupancy by endogenous dopamine in humans. Neuropsychopharmacology 1997, 17:162-174.
34. Le Masurier M., Zetterström T., Cowen P., Sharp T. Tyrosine-free amino acid mixtures reduce physiologically-evoked release of dopamine in a selective and activity-dependent manner. J. Psychopharmacol. 2013, 28:561-569.
35. Leyton M., Young S., Pihl R., Etezadi S., Lauze C., Blier P., Baker G., Benkelfat C. Effects on mood of acute phenylalanine/tyrosine depletion in healthy women. Neuropsychopharmacology 2000, 22:52-63.
36. Leyton M., Dagher A., Boileau I., Casey K., Baker G., Diksic M., Gunn R.N., Young S., Benkelfat C. Decreasing amphetamine-induced dopamine release by acute phenylalanine/tyrosine depletion: a PET/[11C]raclopride study in healthy men. Neuropsychopharmacology 2004, 29:427-432.
37. Lobo M.K., Covington H.E., Chaudhury D., Friedman A.K., Sun H., Damez-Werno D., Dietz D.M., Zaman S., Koo J.W., Kennedy P.J., Mouzon E., Mogri M., Neve R.L., Deisseroth K., Han M.H., Nestler E.J. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 2010, 330:385-390.
38. Lorr M., McNair D.M., Fisher S.U. Evidence for bipolar mood states. J. Pers. Assess. 1982, 46:432-436.
39. Maia T.V., Frank M.J. From reinforcement learning models to psychiatric and neurological disorders. Nat. Neurosci. 2011, 14:154-162.
40. Marcellino D., Kehr J., Agnati L.F., Fuxe K. Increased affinity of dopamine for D(2)-like versus D(1)-like receptors. Relevance for volume transmission in interpreting PET findings. Synapse 2012, 66:196-203.
41. McTavish S., Cowen P., Sharp T. Effect of a tyrosine-free amino acid mixture on regional brain catecholamine synthesis and release. Psychopharmacology 1999, 141:182-188.
42. Mintun M.A., Raichle M.E., Kilbourn M.R., Wooten G.F., Welch M.J. A quantitative model for the in vivo assessment of drug binding sites with positron emission tomography. Ann. Neurol. 1984, 15:217-227.
43. Montague P., Dayan P., Sejnowski T. A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J. Neurosci. 1996, 16:1936-1947.
44. Montgomery A.J., McTavish S.F., Cowen P.J., Grasby P.M. Reduction of brain dopamine concentration with dietary tyrosine plus phenylalanine depletion: an [11C]raclopride PET study. Am. J. Psychiatry 2003, 160:1887-1889.
45. Moustafa A.A., Cohen M.X., Sherman S.J., Frank M.J. A role for dopamine in temporal decision making and reward maximization in parkinsonism. J. Neurosci. 2008, 28:12294-12304.
46. Palmour R.M., Ervin F.R., Baker G.B., Young S.N. An amino acid mixture deficient in phenylalanine and tyrosine reduces cerebrospinal fluid catecholamine metabolites and alcohol consumption in vervet monkeys. Psychopharmacology 1998, 136:1-7.
47. Pessiglione M., Seymour B., Flandin G., Dolan R., Frith C. Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 2006, 442:1042-1045.
48. Potenza M., Voon V., Weintraub D. Drug insight: impulse control disorders and dopamine therapies in Parkinson's disease. Nat. Clin. Pract. Neurol. 2007, 3:664-672.
49. Reynolds J., Wickens J. Dopamine-dependent plasticity of corticostriatal synapses. Neural Netw. 2002, 15:507-521.
50. Reynolds J., Hyland B., Wickens J. A cellular mechanism of reward-related learning. Nature 2001, 413:67-70.
51. Schultz W. Getting formal with dopamine and reward. Neuron 2002, 36:241-263.
52. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
53. Shen W., Flajolet M., Greengard P., Surmeier D.J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 2008, 321:848-851.
54. Sled J.G., Zijdenbos A.P., Evans A.C. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging 1998, 17:87-97.
55. Smittenaar P., Chase H., Aarts E., Nusselein B., Bloem B., Cools R. Decomposing effects of dopaminergic medication in Parkinson's disease on probabilistic action selection-learning or performance?. Eur. J. Neurosci. 2012, 35:1144-1151.
56. Spielberger C.D., Gorsuch R.L., Lushene R., Vagg P.R., Jacobs G.A. Manual for the State-Trait Anxiety Inventory 1983, Consulting Psychologists Press, Palo Alto, CA.
57. Surmeier D., Carrillo-Reid L., Bargas J. Dopaminergic modulation of striatal neurons, circuits, and assemblies. Neuroscience 2011, 198:3-18.
58. Thibaut F., Vaugeois J.-M., Bonnet J.-J., Costentin J. In vivo striatal binding of the D1 antagonist SCH 23390 is not modified by changes in dopaminergic transmission. Neuropharmacology 1996, 35:267-272.
59. Voon V., Schoerling A., Wenzel S., Ekanayake V., Reiff J., Trenkwalder C., Sixel-D[U+04E7]ring F. Frequency of impulse control behaviours associated with dopaminergic therapy in restless legs syndrome. BMC Neurol. 2011, 11:117.
60. Worsley K.J., Marrett S., Neelin P., Vandal A.C., Friston K.J., Evans A.C. A unified statistical approach for determining significant signals in images of cerebral activation. Hum. Brain Mapp. 1996, 4:58-73.
61. Zhang Y., Bertolino A., Fazio L., Blasi G., Rampino A., Romano R., Lee M.L., Xiao T., Papp A., Wang D., Sadee W. Polymorphisms in human dopamine D2 receptor gene affect gene expression, splicing, and neuronal activity during working memory. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20552-20557.
62. Zuckerman M., Kuhlman D. Personality and risk-taking: common biosocial factors. J. Pers. 2000, 68:999-1029.