Altered Probabilistic Learning and Response Biases in Schizophrenia: Behavioral Evidence and Neurocomputational Modeling

Neuropsychology

Volumn 25, Issue 1, 2011, Pages 86-97

  Waltz, James A ^a   Frank, Michael J ^b   Wiecki, Thomas V ^b   Gold, James M ^c  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b BROWN UNIVERSITY   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

Basal ganglia; Dopamine; Procedural learning; Reinforcement learning; Schizophrenia

Indexed keywords

ADULT; ARTICLE; BASAL GANGLION; CLINICAL ARTICLE; CONTROLLED STUDY; DOPAMINERGIC TRANSMISSION; FEMALE; HUMAN; LEARNING DISORDER; MALE; NEGATIVE FEEDBACK; POSITIVE FEEDBACK; PRIORITY JOURNAL; REINFORCEMENT; SCHIZOPHRENIA;

ADULT; ANALYSIS OF VARIANCE; BIAS (EPIDEMIOLOGY); CHOICE BEHAVIOR; COMPUTER SIMULATION; FEMALE; HUMANS; MALE; MIDDLE AGED; MODELS, NEUROLOGICAL; NEUROPSYCHOLOGICAL TESTS; PROBABILITY LEARNING; PSYCHIATRIC STATUS RATING SCALES; REACTION TIME; REINFORCEMENT (PSYCHOLOGY); SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; STATISTICS AS TOPIC;

EID: 78751639884     PISSN: 08944105     EISSN: 19311559     Source Type: Journal    
DOI: 10.1037/a0020882     Document Type: Article

References (74)

1. Abi-Dargham A., Gil R., Krystal J., Baldwin R.M., Seibyl J.P., Bowers M., van Dyck C.H., et al. Increased striatal dopamine transmission in schizophrenia: Confirmation in a second cohort. American Journal of Psychiatry 1998, 155:761-767.
2. Abi-Dargham A., Mawlawi O., Lombardo I., Gil R., Martinez D., Huang Y., Hwang D.R., et al. Prefrontal dopamine D1 receptors and working memory in schizophrenia. Journal of Neuroscience 2002, 22:3708-3719.
3. Abi-Dargham A., Moore H. Prefrontal DA transmission at D1 receptors and the pathology of schizophrenia. Neuroscientist 2003, 9:404-416.
4. Abi-Dargham A., Rodenhiser J., Printz D., Zea-Ponce Y., Gil R., Kegeles L.S., Weiss R., et al. Increased baseline occupancy of D2 receptors by dopamine in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:8104-8109.
5. Addington D., Addington J., Maticka-Tyndale E., Joyce J. Reliability and validity of a depression rating scale for schizophrenics. Schizophrenia Research 1992, 6:201-208.
6. Andreasen N.C. The Scale for the Assessment of Negative Symptoms (SANS) 1984, University of Iowa, Iowa City, IA.
7. Bodi N., Keri S., Nagy H., Moustafa A., Myers C.E., Daw N., Dibo G., et al. 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 2009, 132:2385-2395.
8. Brandt J., Benedict R.H.B. The Hopkins Verbal Learning Test-Revised 2001, FL, Psychological Assessment Resources, Inc., Odessa.
9. Burt D.R., Creese I., Snyder S.H. Antischizophrenic drugs: Chronic treatment elevates dopamine receptor binding in brain. Science 1977, 196:326-328.
10. Centonze D., Usiello A., Costa C., Picconi B., Erbs E., Bernardi G., Borrelli E., et al. Chronic haloperidol promotes corticostriatal long-term potentiation by targeting dopamine D2L receptors. Journal of Neuroscience 2004, 24:8214-8222.
11. Cohen M.X., Frank M.J. Neurocomputational models of basal ganglia function in learning, memory and choice. Behavioural Brain Research 2009, 199:141-156.
12. Danion J.M., Meulemans T., Kauffmann-Muller F., Vermaat H. Intact implicit learning in schizophrenia. American Journal of Psychiatry 2001, 158:944-948.
13. Day M., Wokosin D., Plotkin J.L., Tian X., Surmeier D.J. Differential excitability and modulation of striatal medium spiny neuron dendrites. Journal of Neuroscience 2008, 28:11603-11614.
14. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured Clinical Interview for DSM-IV-Axis I Disorders (SCID-I) 1997, American Psychiatric Press, Washington, DC.
15. Foerde K., Poldrack R.A., Khan B.J., Sabb F.W., Bookheimer S.Y., Bilder R.M., Guthrie D., et al. Selective corticostriatal dysfunction in schizophrenia: Examination of motor and cognitive skill learning. Neuropsychology 2008, 22:100-109.
16. Frank M.J. Dynamic dopamine modulation in the basal ganglia: A neurocomputational account of cognitive deficits in medicated and nonmedicated Parkinsonism. Journal of Cognitive Neuroscience 2005, 17:51-72.
17. Frank M.J. Hold your horses: A dynamic computational role for the subthalamic nucleus in decision making. Neural Network 2006, 19:1120-1136.
18. Frank M.J., Claus E.D. Anatomy of a decision: Striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychological Review 2006, 113:300-326.
19. Frank M.J., Doll B.B., Oas-Terpstra J., Moreno F. Prefrontal and striatal dopaminergic genes predict individual differences in exploration and exploitation. Nature Neuroscience 2009, 12:1062-1068.
20. Frank M.J., Hutchison K. Genetic contributions to avoidance-based decisions: Striatal D2 receptor polymorphisms. Neuroscience 2009, 164:131-140.
21. 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. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:16311-16316.
22. Frank M.J., O'Reilly R.C. A mechanistic account of striatal dopamine function in cognition: Psychopharmacological studies with cabergoline and haloperidol. Behavioral Neuroscience 2006, 120:497-517.
23. 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.
24. Galderisi S., Quarantelli M., Volpe U., Mucci A., Cassano G.B., Invernizzi G., Rossi A., et al. Patterns of structural MRI abnormalities in deficit and nondeficit schizophrenia. Schizophrenia Bulletin 2008, 34:393-401.
25. Gold J.M., Bish J.A., Iannone V.N., Hobart M.P., Queern C.A., Buchanan R.W. Effects of contextual processing on visual conditional associative learning in schizophrenia. Biological Psychiatry 2000, 48:406-414.
26. Gold J.M., Carpenter C., Randolph C., Goldberg T.E., Weinberger D.R. Auditory working memory and Wisconsin Card Sorting Test performance in schizophrenia. Archives of General Psychiatry 1997, 54:159-165.
27. Gold J.M., Waltz J.A., Prentice K.J., Morris S.E., Heerey E.A. Reward processing in schizophrenia: A deficit in the representation of value. Schizophrenia Bulletin 2008, 34:835-847.
28. Gong S., Zheng C., Doughty M.L., Losos K., Didkovsky N., Schambra U.B., Nowak N.J., et al. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 2003, 425:917-925.
29. Graybiel A.M. Habits, rituals, and the evaluative brain. Annual Review of Neuroscience 2008, 31:359-387.
30. Hakansson K., Galdi S., Hendrick J., Snyder G., Greengard P., Fisone G. Regulation of phosphorylation of the GluR1 AMPA receptor by dopamine D2 receptors. Journal of Neurochemistry 2006, 96:482-488.
31. Horan W.P., Green M.F., Knowlton B.J., Wynn J.K., Mintz J., Nuechterlein K.H. Impaired implicit learning in schizophrenia. Neuropsychology 2008, 22:606-617.
32. Joyce J.N. D2 but not D3 receptors are elevated after 9 or 11 months chronic haloperidol treatment: Influence of withdrawal period. Synapse 2001, 40:137-144.
33. Kelly D.L., Kreyenbuhl J., Buchanan R.W., Malhotra A.K. Why not clozapine?. Clinical Schizophrenia & Related Psychoses 2007, 1:92-95.
34. Kemali D., Maj M., Galderisi S., Monteleone P., Mucci A. Conditional associative learning in drug-free schizophrenic patients. Neuropsychobiology 1987, 17:30-34.
35. Keri S., Kelemen O., Szekeres G., Bagoczky N., Erdelyi R., Antal A., Benedek G., Janka Z. Schizophrenics know more than they can tell: Probabilistic classification learning in schizophrenia. Psychological Medicine 2000, 30:149-155.
36. Kirkpatrick B., Buchanan R.W. The neural basis of the deficit syndrome of schizophrenia. Journal of Nervous and Mental Disease 1990, 178:545-555.
37. Knowlton B.J., Mangels J.A., Squire L.R. A neostriatal habit learning system in humans. Science 1996, 273:1399-1402.
38. Koch, K., Schachtzabel, C., Wagner, G., Schikora, J., Schultz, C., Reichenbach, J. R., Sauer, H., & Schlosser, R. G. (in press). Altered activation in association with reward-related trial-and-error learning in patients with schizophrenia. Neuroimage, 50, 223-232.
39. Laruelle M., Abi-Dargham A. Dopamine as the wind of the psychotic fire: New evidence from brain imaging studies. Journal of Psychopharmacology 1999, 13:358-371.
40. Malenka R.C., Angel R.W., Hampton B., Berger P.A. Impaired central error-correcting behavior in schizophrenia. Archives of General Psychiatry 1982, 39:101-107.
41. Mallet N., Ballion B., Le Moine C., Gonon F. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. Journal of Neuroscience 2006, 26:3875-3884.
42. McClure S.M., Daw N.D., Montague P.R. A computational substrate for incentive salience. Trends in Neurosciences 2003, 26:423-428.
43. McMahon R.P., Kelly D.L., Kreyenbuhl J., Kirkpatrick B., Love R.C., Conley R.R. Novel factor-based symptom scores in treatment resistant schizophrenia: Implications for clinical trials. Neuropsychopharmacology 2002, 26:537-545.
44. Meyer-Lindenberg A., Miletich R.S., Kohn P.D., Esposito G., Carson R.E., Quarantelli M., Weinberger D.R., et al. Reduced prefrontal activity predicts exaggerated striatal dopaminergic function in schizophrenia. Nature Neuroscience 2002, 5:267-271.
45. Miller R. A neurodynamic theory of schizophrenia (and related disorders) (New Zealand) 2008, Retrieved from Lulu.com.
46. 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. Journal of Neuroscience 2008, 28:12294-12304.
47. Overall J.E., Gorman D.R. The Brief Psychiatric Rating Scale. Psychological Reports 1962, 10:799-812.
48. Pfohl B., Blum N., Zimmerman M., Stangl D. Structured Interview for DSM-III-R Personality Disorders (SIDP-R) 1989, University of Iowa, Department of Psychiatry, Iowa City.
49. Pizzagalli D.A., Evins A.E., Schetter E.C., Frank M.J., Pajtas P.E., Santesso D.L., Culhane M. Single dose of a dopamine agonist impairs reinforcement learning in humans: Behavioral evidence from a laboratory-based measure of reward responsiveness. Psychopharmacology (Berl) 2008, 196:221-232.
50. Prentice K.J., Gold J.M., Buchanan R.W. The Wisconsin Card Sorting impairment in schizophrenia is evident in the first four trials. Schizophrenia Research 2008, 106:81-87.
51. Rolls E.T., O'Doherty J., Kringelbach M.L., Francis S., Bowtell R., McGlone F. Representations of pleasant and painful touch in the human orbitofrontal and cingulate cortices. Cerebral Cortex 2003, 13:308-317.
52. Rushe T.M., Woodruff P.W., Murray R.M., Morris R.G. Episodic memory and learning in patients with chronic schizophrenia. Schizophrenia Research 1999, 35:85-96.
53. Santesso D.L., Evins A.E., Frank M.J., Schetter E.C., Bogdan R., Pizzagalli D.A. Single dose of a dopamine agonist impairs reinforcement learning in humans: Evidence from event-related potentials and computational modeling of striatal-cortical function. Human Brain Mapping 2009, 30:1963-1976.
54. Schoenbaum G., Roesch M. Orbitofrontal cortex, associative learning, and expectancies. Neuron 2005, 47:633-636.
55. Schultz W. Predictive reward signal of dopamine neurons. Journal of Neurophysiology 1998, 80:1-27.
56. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
57. Schwartz B.L., Howard D.V., Howard J.H., Hovaguimian A., Deutsch S.I. Implicit learning of visuospatial sequences in schizophrenia. Neuropsychology 2003, 17:517-533.
58. Seeman P. Dopamine receptors and the dopamine hypothesis of schizophrenia. Synapse 1987, 1:133-152.
59. Seeman P., Weinshenker D., Quirion R., Srivastava L.K., Bhardwaj S.K., Grandy D.K., Premont R.T., et al. Dopamine supersensitivity correlates with D2High states, implying many paths to psychosis. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:3513-3518.
60. Shen W., Flajolet M., Greengard P., Surmeier D.J. Dichotomous dopaminergic control of striatal synaptic plasticity. Science 2008, 321:848-851.
61. Stroup T.S., Lieberman J.A., McEvoy J.P., Davis S.M., Swartz M.S., Keefe R.S., Miller A.L., Rosenheck R.A., Hsiao J.K., et al. Results of phase 3 of the CATIE schizophrenia trial. Schizophrenia Research 2009, 107:1-12.
62. Surmeier D.J., Ding J., Day M., Wang Z., Shen W. D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends in Neurosciences 2007, 30:228-235.
63. Surmeier D.J., Song W.J., Yan Z. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. Journal of Neuroscience 1996, 16:6579-6591.
64. Tricomi E., Balleine B.W., O'Doherty J.P. A specific role for posterior dorsolateral striatum in human habit learning. European Journal of Neuroscience 2009.
65. Vaiva G., Cottencin O., Llorca P.M., Devos P., Dupont S., Mazas O., Rascle C., et al. Regional cerebral blood flow in deficit/nondeficit types of schizophrenia according to SDS criteria. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2002, 26:481-485.
66. Valjent E., Bertran-Gonzalez J., Herve D., Fisone G., Girault J.A. Looking BAC at striatal signaling: Cell-specific analysis in new transgenic mice. Trends in Neurosciences 2009, 32:538-547.
67. Waltz J.A., Frank M.J., Robinson B.M., Gold J.M. Selective reinforcement learning deficits in schizophrenia support predictions from computational models of striatal-cortical dysfunction. Biological Psychiatry 2007, 62:756-764.
68. Waltz J.A., Gold J.M. Probabilistic reversal learning impairments in schizophrenia: Further evidence of orbitofrontal dysfunction. Schizophrenia Research 2007, 93:296-303.
69. Waltz J.A., Schweitzer J.B., Gold J.M., Kurup P.K., Ross T.J., Salmeron B.J., Rose E.J., et al. Patients with schizophrenia have a reduced neural response to both unpredictable and predictable primary reinforcers. Neuropsychopharmacology 2009, 34:1567-1577.
70. Wechsler D. Wechsler Memory Scale 1997, The Psychological Corporation, San Antonio, TX. 3rd ed.
71. Wechsler D. Wechsler Test of Adult Reading (WTAR) 2001, The Psychological Corporation, San Antonio, TX.
72. Weickert T.W., Terrazas A., Bigelow L.B., Malley J.D., Hyde T., Egan M.F., Weinberger D.R., et al. Habit and skill learning in schizophrenia: Evidence of normal striatal processing with abnormal cortical input. Learning & Memory 2002, 9:430-442.
73. Weinberger D.R. Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry 1987, 44:660-669.
74. Wiecki T.V., Riedinger K., von Ameln-Mayerhofer A., Schmidt W.J., Frank M.J. A neurocomputational account of catalepsy sensitization induced by D2 receptor blockade in rats: Context dependency, extinction, and renewal. Psychopharmacology (Berl) 2009, 204:265-277.