Dissociable Effects of Dopamine and Serotonin on Reversal Learning

Neuron

Volumn 80, Issue 4, 2013, Pages 1090-1100

  DenOuden, Hanneke E M ^a,b   Daw, Nathaniel D ^b   Fernandez, Guillén ^a,c   Elshout, Joris A ^a,c   Rijpkema, Mark ^a   Hoogman, Martine ^c   Franke, Barbara ^a,c   Cools, Roshan ^a,c  

^a RADBOUD UNIVERSITY   (Netherlands)

^b NEW YORK UNIVERSITY   (United States)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DOPAMINE; SEROTONIN; SEROTONIN TRANSPORTER;

ADULT; ALLELE; ARTICLE; DAT1 GENE; DOUBLE DISSOCIATION; FEMALE; GENE; GENETIC POLYMORPHISM; GENOTYPE; HOMOZYGOSITY; HUMAN; HUMAN EXPERIMENT; LEARNING; MALE; NEGATIVE FEEDBACK; NORMAL HUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; REINFORCEMENT; SEROTONIN TRANSPORTER GENE;

ADAPTATION, PSYCHOLOGICAL; ADULT; ALGORITHMS; ALLELES; COMPUTER SIMULATION; DATA INTERPRETATION, STATISTICAL; DNA; DOPAMINE; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; FEMALE; GAMBLING; GENOTYPE; HUMANS; MALE; MODELS, NEUROLOGICAL; POLYMORPHISM, GENETIC; PSYCHOMOTOR PERFORMANCE; REINFORCEMENT (PSYCHOLOGY); REVERSAL LEARNING; SEROTONIN; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; YOUNG ADULT;

EID: 84888068462     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.08.030     Document Type: Article

References (68)

1. Aarts E., Roelofs A., Franke B., Rijpkema M., Fernández G., Helmich R.C., Cools R. Striatal dopamine mediates the interface between motivational and cognitive control in humans: evidence from genetic imaging. Neuropsychopharmacology 2010, 35:1943-1951.
2. Balleine B.W., O'Doherty J.P. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 2010, 35:48-69.
3. Bari A., Theobald D.E., Caprioli D., Mar A.C., Aidoo-Micah A., Dalley J.W., Robbins T.W. Serotonin modulates sensitivity to reward and negative feedback in a probabilistic reversal learning task in rats. Neuropsychopharmacology 2010, 35:1290-1301.
4. Boulougouris V., Robbins T.W. Enhancement of spatial reversal learning by 5-HT2C receptor antagonism is neuroanatomically specific. J.Neurosci. 2010, 30:930-938.
5. Boulougouris V., Glennon J.C., Robbins T.W. Dissociable effects of selective 5-HT2A and 5-HT2C receptor antagonists on serial spatial reversal learning in rats. Neuropsychopharmacology 2008, 33:2007-2019.
6. Boulougouris V., Castañé A., Robbins T.W. Dopamine D2/D3 receptor agonist quinpirole impairs spatial reversal learning in rats: investigation of D3 receptor involvement in persistent behavior. Psychopharmacology (Berl.) 2009, 202:611-620.
7. Boureau Y.L., Dayan P. Opponency revisited: competition and cooperation between dopamine and serotonin. Neuropsychopharmacology 2011, 36:74-97.
8. Camerer C., Ho T. Experience-weighted attraction learning in normal form games. Econometrica 1999, 67:827-874.
9. Caspi A., Hariri A.R., Holmes A., Uher R., Moffitt T.E. Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am. J. Psychiatry 2010, 167:509-527.
10. Chamberlain S.R., Müller U., Blackwell A.D., Clark L., Robbins T.W., Sahakian B.J. Neurochemical modulation of response inhibition and probabilistic learning in humans. Science 2006, 311:861-863.
11. Clarke H.F., Walker S.C., Dalley J.W., Robbins T.W., Roberts A.C. Cognitive inflexibility after prefrontal serotonin depletion is behaviorally and neurochemically specific. Cereb. Cortex 2007, 17:18-27.
12. Clatworthy P.L., Lewis S.J., Brichard L., Hong Y.T., Izquierdo D., Clark L., Cools R., Aigbirhio F.I., Baron J.C., Fryer T.D., Robbins T.W. Dopamine release in dissociable striatal subregions predicts the different effects of oral methylphenidate on reversal learning and spatial working memory. J.Neurosci. 2009, 29:4690-4696.
13. Collins A.G., Frank M.J. How much of reinforcement learning is working memory, not reinforcement learning? A behavioral, computational, and neurogenetic analysis. Eur. J. Neurosci. 2012, 35:1024-1035.
14. Cools R., Barker R.A., Sahakian B.J., Robbins T.W. Enhanced or impaired cognitive function in Parkinson's disease as a function of dopaminergic medication and task demands. Cereb. Cortex 2001, 11:1136-1143.
15. 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.
16. Cools R., Lewis S.J.G., Clark L., Barker R.A., Robbins T.W. L-DOPA disrupts activity in the nucleus accumbens during reversal learning in Parkinson's disease. Neuropsychopharmacology 2007, 32:180-189.
17. Cools R., Roberts A.C., Robbins T.W. Serotoninergic regulation of emotional and behavioural control processes. Trends Cogn. Sci. 2008, 12:31-40.
18. Cools R., Robinson O.J., Sahakian B. Acute tryptophan depletion in healthy volunteers enhances punishment prediction but does not affect reward prediction. Neuropsychopharmacology 2008, 33:2291-2299.
19. Cools R., Frank M.J., Gibbs S.E., Miyakawa A., Jagust W., D'Esposito M. Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. J.Neurosci. 2009, 29:1538-1543.
20. Cools R., Nakamura K., Daw N.D. Serotonin and dopamine: unifying affective, activational, and decision functions. Neuropsychopharmacology 2011, 36:98-113.
21. Costa A., Riedel M., Müller U., Möller H.J., Ettinger U. Relationship between SLC6A3 genotype and striatal dopamine transporter availability: a meta-analysis of human single photon emission computed tomography studies. Synapse 2011, 65:998-1005.
22. Crockett M.J., Clark L., Robbins T.W. Reconciling the role of serotonin in behavioral inhibition and aversion: acute tryptophan depletion abolishes punishment-induced inhibition in humans. J.Neurosci. 2009, 29:11993-11999.
23. Daw N.D., Kakade S., Dayan P. Opponent interactions between serotonin and dopamine. Neural Netw. 2002, 15:603-616.
24. Daw N.D., Niv Y., Dayan P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat. Neurosci. 2005, 8:1704-1711.
25. Daw N.D. Trial by trial data analysis using computational models. Decision Making, Affect, and Learning: Attention and Performance XXIII 2011, 3-48. Oxford University Press, Oxford. M.R. Delgado, E.A. Phelps, T.W. Robbins (Eds.).
26. Dayan P., Huys Q.J. Serotonin, inhibition, and negative mood. PLoS Comput. Biol. 2008, 4:e4.
27. Dayan P., Kakade S., Montague P.R. Learning and selective attention. Nat. Neurosci. 2000, 3(Suppl):1218-1223.
28. Deakin J.F.W., Graeff F.G. 5-HT and mechanisms of defence. J.Psychopharmacol. (Oxford) 1991, 5:305-315.
29. Dodds C.M., Müller U., Clark L., van Loon A., Cools R., Robbins T.W. Methylphenidate has differential effects on blood oxygenation level-dependent signal related to cognitive subprocesses of reversal learning. J.Neurosci. 2008, 28:5976-5982.
30. Dreher J.C., Kohn P., Kolachana B., Weinberger D.R., Berman K.F. Variation in dopamine genes influences responsivity of the human reward system. Proc. Natl. Acad. Sci. USA 2009, 106:617-622.
31. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 2005, 8:1481-1489.
32. Fiorillo C.D., Tobler P.N., Schultz W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 2003, 299:1898-1902.
33. Forbes E.E., Brown S.M., Kimak M., Ferrell R.E., Manuck S.B., Hariri A.R. Genetic variation in components of dopamine neurotransmission impacts ventral striatal reactivity associated with impulsivity. Mol. Psychiatry 2009, 14:60-70.
34. Frank M.J., Seeberger L.C., O'Reilly R. By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 2004, 306:1940-1943.
35. 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. USA 2007, 104:16311-16316.
36. Franke B., Vasquez A.A., Johansson S., Hoogman M., Romanos J., Boreatti-Hümmer A., Heine M., Jacob C.P., Lesch K.P., Casas M., et al. Multicenter analysis of the SLC6A3/DAT1 VNTR haplotype in persistent ADHD suggests differential involvement of the gene in childhood and persistent ADHD. Neuropsychopharmacology 2010, 35:656-664.
37. Gizer I.R., Ficks C., Waldman I.D. Candidate gene studies of ADHD: a meta-analytic review. Hum. Genet. 2009, 126:51-90.
38. Goto Y., Grace A.A. Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat. Neurosci. 2005, 8:805-812.
39. Hariri A.R., Holmes A. Genetics of emotional regulation: the role of the serotonin transporter in neural function. Trends Cogn. Sci. 2006, 10:182-191.
40. Houk J.C., Adams J.L., Barto A.G. A model of how the basal ganglia generate and use neural signals that predict reinforcement. Models of Information Processing in the Basal Ganglia 1995, 249-270. MIT Press, Cambridge, MA. J.C. Houk, J.L. Davis, D.G. Beiser (Eds.).
41. Hu X.Z., Lipsky R.H., Zhu G., Akhtar L.A., Taubman J., Greenberg B.D., Xu K., Arnold P.D., Richter M.A., Kennedy J.L., et al. Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. Am. J. Hum. Genet. 2006, 78:815-826.
42. Izquierdo A., Newman T.K., Higley J.D., Murray E.A. Genetic modulation of cognitive flexibility and socioemotional behavior in rhesus monkeys. Proc. Natl. Acad. Sci. USA 2007, 104:14128-14133.
43. Jedema H.P., Gianaros P.J., Greer P.J., Kerr D.D., Liu S., Higley J.D., Suomi S.J., Olsen A.S., Porter J.N., Lopresti B.J., et al. Cognitive impact of genetic variation of the serotonin transporter in primates is associated with differences in brain morphology rather than serotonin neurotransmission. Mol. Psychiatry 2010, 15:512-522.
44. Kass R.E., Raftery A.E. Bayes Factors. J.Am. Stat. Assoc. 1995, 90:773-795.
45. Lawrence A.D., Sahakian B.J., Rogers R.D., Hodge J.R., Robbins T.W. Discrimination, reversal, and shift learning in Huntington's disease: mechanisms of impaired response selection. Neuropsychologia 1999, 37:1359-1374.
46. Lesch K.P., Bengel D., Heils A., Sabol S.Z., Greenberg B.D., Petri S., Benjamin J., Müller C.R., Hamer D.H., Murphy D.L. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 1996, 274:1527-1531.
47. Maia T.V., Frank M.J. From reinforcement learning models to psychiatric and neurological disorders. Nat. Neurosci. 2011, 14:154-162.
48. Mill J., Asherson P., Browes C., D'Souza U., Craig I. Expression of the dopamine transporter gene is regulated by the 3' UTR VNTR: evidence from brain and lymphocytes using quantitative RT-PCR. Am. J. Med. Genet. 2002, 114:975-979.
49. Montague P.R., Dayan P., Sejnowski T.J. A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J.Neurosci. 1996, 16:1936-1947.
50. Murphy F.C., Michael A., Robbins T.W., Sahakian B.J. Neuropsychological impairment in patients with major depressive disorder: the effects of feedback on task performance. Psychol. Med. 2003, 33:455-467.
51. Palminteri S., Clair A.H., Mallet L., Pessiglione M. Similar improvement of reward and punishment learning by serotonin reuptake inhibitors in obsessive-compulsive disorder. Biol. Psychiatry 2012, 72:244-250.
52. Parkinson J.A., Olmstead M.C., Burns L.H., Robbins T.W., Everitt B.J. Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by D-amphetamine. J.Neurosci. 1999, 19:2401-2411.
53. Praschak-Rieder N., Kennedy J., Wilson A.A., Hussey D., Boovariwala A., Willeit M., Ginovart N., Tharmalingam S., Masellis M., Houle S., Meyer J.H. Novel 5-HTTLPR allele associates with higher serotonin transporter binding in putamen: a [(11)C] DASB positron emission tomography study. Biol. Psychiatry 2007, 62:327-331.
54. Robinson O.J., Standing H.R., DeVito E.E., Cools R., Sahakian B.J. Dopamine precursor depletion improves punishment prediction during reversal learning in healthy females but not males. Psychopharmacology (Berl.) 2010, 211:187-195.
55. Roiser J.P., de Martino B., Tan G.C., Kumaran D., Seymour B., Wood N.W., Dolan R.J. A genetically mediated bias in decision making driven by failure of amygdala control. J.Neurosci. 2009, 29:5985-5991.
56. Rutledge R.B., Lazzaro S.C., Lau B., Myers C.E., Gluck M.A., Glimcher P.W. Dopaminergic drugs modulate learning rates and perseveration in Parkinson's patients in a dynamic foraging task. J.Neurosci. 2009, 29:15104-15114.
57. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
58. Schwarz G. Estimating dimensions of a model. Ann. Stat. 1978, 6:461-464.
59. Soubrie P. Reconciling the role of central serotonin neurons in human and animal behavior. Behav. Brain Sci. 1986, 9:319-335.
60. Spencer T.J., Biederman J., Faraone S.V., Madras B.K., Bonab A.A., Dougherty D.D., Batchelder H., Clarke A., Fischman A.J. Functional genomics of attention-deficit/hyperactivity disorder (ADHD) risk alleles on dopamine transporter binding in ADHD and healthy control subjects. Biol. Psychiatry 2013, 74:84-89.
61. Stephan K.E., Penny W.D., Daunizeau J., Moran R.J., Friston K.J. Bayesian model selection for group studies. Neuroimage 2009, 46:1004-1017.
62. Suri R.E., Schultz W. A neural network model with dopamine-likereinforcement signal that learns a spatial delayed response task. Neuroscience 1999, 91:871-890.
63. Thorndike E. Animal Intelligence: Experimental Studies 1911, Macmillan, New York.
64. Vallender E.J., Lynch L., Novak M.A., Miller G.M. Polymorphisms in the 3' UTR of the serotonin transporter are associated with cognitive flexibility in rhesus macaques. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 2009, 150B:467-475.
65. van de Giessen E., de Win M.M., Tanck M.W., van den Brink W., Baas F., Booij J. Striatal dopamine transporter availability associated with polymorphisms in the dopamine transporter gene SLC6A3. J.Nucl. Med. 2009, 50:45-52.
66. van Dyck C.H., Malison R.T., Jacobsen L.K., Seibyl J.P., Staley J.K., Laruelle M., Baldwin R.M., Innis R.B., Gelernter J. Increased dopamine transporter availability associated with the 9-repeat allele of the SLC6A3 gene. J.Nucl. Med. 2005, 46:745-751.
67. Walker S.C., Robbins T.W., Roberts A.C. Differential contributions of dopamine and serotonin to orbitofrontal cortex function in the marmoset. Cereb. Cortex 2009, 19:889-898.
68. Willeit M., Praschak-Rieder N. Imaging the effects of genetic polymorphisms on radioligand binding in the living human brain: a review on genetic neuroreceptor imaging of monoaminergic systems in psychiatry. Neuroimage 2010, 53:878-892.