Skip to main content
Top
Published in: BMC Psychiatry 1/2008

Open Access 01-12-2008 | Research article

Incentive motivation in first-episode psychosis: A behavioural study

Authors: Graham K Murray, Luke Clark, Philip R Corlett, Andrew D Blackwell, Roshan Cools, Peter B Jones, Trevor W Robbins, Luise Poustka

Published in: BMC Psychiatry | Issue 1/2008

Login to get access

Abstract

Background:

It has been proposed that there are abnormalities in incentive motivational processing in psychosis, possibly secondary to subcortical dopamine abnormalities, but few empirical studies have addressed this issue.

Methods:

We studied incentive motivation in 18 first-episode psychosis patients from the Cambridge early psychosis service CAMEO and 19 control participants using the Cued Reinforcement Reaction Time Task, which measures motivationally driven behaviour. We also gathered information on participants' attentional, executive and spatial working memory function in order to determine whether any incentive motivation deficits were secondary to generalised cognitive impairment.

Results:

We demonstrated the anticipated "reinforcement-related speeding" effect in controls (17 out of 19 control participants responded faster during an "odd-one-out" task in response to a cue that indicated a high likelihood of a large points reward). Only 4 out of 18 patients showed this effect and there was a significant interaction effect between reinforcement probability and diagnosis on reaction time (F1,35 = 14.2, p = 0.001). This deficit was present in spite of preserved executive and attentional function in patients, and persisted even in antipsychotic medication free patients.

Conclusion:

There are incentive motivation processing abnormalities in first-episode psychosis; these may be secondary to dopamine dysfunction and are not attributable to generalised cognitive impairment.
Appendix
Available only for authorised users
Literature
1.
go back to reference Bleuler E: Dementia Praecox or the group of schizophrenias. New York , International University Press, 1911/1950 Bleuler E: Dementia Praecox or the group of schizophrenias. New York , International University Press, 1911/1950
2.
go back to reference Krystal JH, D'Souza DC, Gallinat J, Driesen N, Abi-Dargham A, Petrakis I, Heinz A, Pearlson G: The vulnerability to alcohol and substance abuse in individuals diagnosed with schizophrenia. Neurotox Res. 2006, 10 (3-4): 235-252.CrossRefPubMed Krystal JH, D'Souza DC, Gallinat J, Driesen N, Abi-Dargham A, Petrakis I, Heinz A, Pearlson G: The vulnerability to alcohol and substance abuse in individuals diagnosed with schizophrenia. Neurotox Res. 2006, 10 (3-4): 235-252.CrossRefPubMed
3.
go back to reference Stein L, Wise CD: Possible etiology of schizophrenia: progressive damage to the noradrenergic reward system by 6-hydroxydopamine. Science. 1971, 171 (975): 1032-1036. 10.1126/science.171.3975.1032.CrossRefPubMed Stein L, Wise CD: Possible etiology of schizophrenia: progressive damage to the noradrenergic reward system by 6-hydroxydopamine. Science. 1971, 171 (975): 1032-1036. 10.1126/science.171.3975.1032.CrossRefPubMed
4.
go back to reference Drew MR, Simpson EH, Kellendonk C, Herzberg WG, Lipatova O, Fairhurst S, Kandel ER, Malapani C, Balsam PD: Transient overexpression of striatal D2 receptors impairs operant motivation and interval timing. J Neurosci. 2007, 27 (29): 7731-7739. 10.1523/JNEUROSCI.1736-07.2007.CrossRefPubMed Drew MR, Simpson EH, Kellendonk C, Herzberg WG, Lipatova O, Fairhurst S, Kandel ER, Malapani C, Balsam PD: Transient overexpression of striatal D2 receptors impairs operant motivation and interval timing. J Neurosci. 2007, 27 (29): 7731-7739. 10.1523/JNEUROSCI.1736-07.2007.CrossRefPubMed
5.
go back to reference Crow TJ: Catecholamine-containing neurones and electrical self-stimulation. 2. A theoretical interpretation and some psychiatric implications. Psychol Med. 1973, 3 (1): 66-73.CrossRefPubMed Crow TJ: Catecholamine-containing neurones and electrical self-stimulation. 2. A theoretical interpretation and some psychiatric implications. Psychol Med. 1973, 3 (1): 66-73.CrossRefPubMed
6.
go back to reference Berridge KC, Robinson TE: What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Brain Res Rev. 1998, 28 (3): 309-369. 10.1016/S0165-0173(98)00019-8.CrossRefPubMed Berridge KC, Robinson TE: What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?. Brain Res Brain Res Rev. 1998, 28 (3): 309-369. 10.1016/S0165-0173(98)00019-8.CrossRefPubMed
7.
go back to reference Schultz W, Dayan P, Montague PR: A neural substrate of prediction and reward. Science. 1997, 275 (5306): 1593-1599. 10.1126/science.275.5306.1593.CrossRefPubMed Schultz W, Dayan P, Montague PR: A neural substrate of prediction and reward. Science. 1997, 275 (5306): 1593-1599. 10.1126/science.275.5306.1593.CrossRefPubMed
8.
go back to reference Robbins TW: Relationship between reward-enhancing and stereotypical effects of psychomotor stimulant drugs. Nature. 1976, 264 (5581): 57-59. 10.1038/264057a0.CrossRefPubMed Robbins TW: Relationship between reward-enhancing and stereotypical effects of psychomotor stimulant drugs. Nature. 1976, 264 (5581): 57-59. 10.1038/264057a0.CrossRefPubMed
9.
go back to reference Beninger RJ: The slow therapeutic action of antipsychotic drugs. A possible mechanism involving the role of dopamine in incentive learning. Selected Models of Anxiety, Depression and Psychosis. Edited by: Simon P, Soubrie P, Widlocher D. 1988, Basel , Karger, 36-51. Beninger RJ: The slow therapeutic action of antipsychotic drugs. A possible mechanism involving the role of dopamine in incentive learning. Selected Models of Anxiety, Depression and Psychosis. Edited by: Simon P, Soubrie P, Widlocher D. 1988, Basel , Karger, 36-51.
10.
go back to reference Kapur S: Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiatry. 2003, 160 (1): 13-23. 10.1176/appi.ajp.160.1.13.CrossRefPubMed Kapur S: Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiatry. 2003, 160 (1): 13-23. 10.1176/appi.ajp.160.1.13.CrossRefPubMed
11.
go back to reference Miller R: Schizophrenic psychology, associative learning and the role of forebrain dopamine. Med Hypotheses. 1976, 2 (5): 203-211. 10.1016/0306-9877(76)90040-2.CrossRefPubMed Miller R: Schizophrenic psychology, associative learning and the role of forebrain dopamine. Med Hypotheses. 1976, 2 (5): 203-211. 10.1016/0306-9877(76)90040-2.CrossRefPubMed
12.
go back to reference McKenna PJ: Pathology, phenomenology and the dopamine hypothesis of schizophrenia. Br J Psychiatry. 1987, 151: 288-301.CrossRefPubMed McKenna PJ: Pathology, phenomenology and the dopamine hypothesis of schizophrenia. Br J Psychiatry. 1987, 151: 288-301.CrossRefPubMed
13.
go back to reference Crow TJ: Catecholamine reward pathways and schizophrenia: the mechanism of the antipsychotic effect and the site of the primary disturbance. Fed Proc. 1979, 38: 2462-2467.PubMed Crow TJ: Catecholamine reward pathways and schizophrenia: the mechanism of the antipsychotic effect and the site of the primary disturbance. Fed Proc. 1979, 38: 2462-2467.PubMed
14.
go back to reference Miller R: Striatal dopamine in reward and attention: a system for understanding the symptomatology of acute schizophrenia and mania. Int Rev Neurobiol. 1993, 35: 161-278.CrossRefPubMed Miller R: Striatal dopamine in reward and attention: a system for understanding the symptomatology of acute schizophrenia and mania. Int Rev Neurobiol. 1993, 35: 161-278.CrossRefPubMed
16.
go back to reference Corlett PR, Murray GK, Honey GD, Aitken MR, Shanks DR, Robbins TW, Bullmore ET, Dickinson A, Fletcher PC: Disrupted prediction-error signal in psychosis: evidence for an associative account of delusions. Brain. 2007, 130 (Pt 9): 2387-2400. 10.1093/brain/awm173.CrossRefPubMed Corlett PR, Murray GK, Honey GD, Aitken MR, Shanks DR, Robbins TW, Bullmore ET, Dickinson A, Fletcher PC: Disrupted prediction-error signal in psychosis: evidence for an associative account of delusions. Brain. 2007, 130 (Pt 9): 2387-2400. 10.1093/brain/awm173.CrossRefPubMed
17.
go back to reference Ritter LM, Meador-Woodruff JH, Dalack GW: Neurocognitive measures of prefrontal cortical dysfunction in schizophrenia. Schizophr Res. 2004, 68 (1): 65-73. 10.1016/S0920-9964(03)00086-0.CrossRefPubMed Ritter LM, Meador-Woodruff JH, Dalack GW: Neurocognitive measures of prefrontal cortical dysfunction in schizophrenia. Schizophr Res. 2004, 68 (1): 65-73. 10.1016/S0920-9964(03)00086-0.CrossRefPubMed
18.
go back to reference Beninger RJ, Wasserman J, Zanibbi K, Charbonneau D, Mangels J, Beninger BV: Typical and atypical antipsychotic medications differentially affect two nondeclarative memory tasks in schizophrenic patients: a double dissociation. Schizophr Res. 2003, 61 (2-3): 281-292. 10.1016/S0920-9964(02)00315-8.CrossRefPubMed Beninger RJ, Wasserman J, Zanibbi K, Charbonneau D, Mangels J, Beninger BV: Typical and atypical antipsychotic medications differentially affect two nondeclarative memory tasks in schizophrenic patients: a double dissociation. Schizophr Res. 2003, 61 (2-3): 281-292. 10.1016/S0920-9964(02)00315-8.CrossRefPubMed
19.
go back to reference Cavallaro R, Cavedini P, Mistretta P, Bassi T, Angelone SM, Ubbiali A, Bellodi L: Basal-corticofrontal circuits in schizophrenia and obsessive-compulsive disorder: a controlled, double dissociation study. Biol Psychiatry. 2003, 54 (4): 437-443. 10.1016/S0006-3223(02)01814-0.CrossRefPubMed Cavallaro R, Cavedini P, Mistretta P, Bassi T, Angelone SM, Ubbiali A, Bellodi L: Basal-corticofrontal circuits in schizophrenia and obsessive-compulsive disorder: a controlled, double dissociation study. Biol Psychiatry. 2003, 54 (4): 437-443. 10.1016/S0006-3223(02)01814-0.CrossRefPubMed
20.
go back to reference Cools R, Blackwell A, Clark L, Menzies L, Cox S, Robbins TW: Tryptophan depletion disrupts the motivational guidance of goal-directed behavior as a function of trait impulsivity. Neuropsychopharmacology. 2005, 30 (7): 1362-1373.PubMed Cools R, Blackwell A, Clark L, Menzies L, Cox S, Robbins TW: Tryptophan depletion disrupts the motivational guidance of goal-directed behavior as a function of trait impulsivity. Neuropsychopharmacology. 2005, 30 (7): 1362-1373.PubMed
21.
go back to reference McGorry PD, Edwards J, Mihalopoulos C, Harrigan SM, Jackson HJ: EPPIC: an evolving system of early detection and optimal management. Schizophr Bull. 1996, 22 (2): 305-326.CrossRefPubMed McGorry PD, Edwards J, Mihalopoulos C, Harrigan SM, Jackson HJ: EPPIC: an evolving system of early detection and optimal management. Schizophr Bull. 1996, 22 (2): 305-326.CrossRefPubMed
22.
go back to reference Schimmelmann BG, Conus P, Cotton S, McGorry PD, Lambert M: Pre-treatment, baseline, and outcome differences between early-onset and adult-onset psychosis in an epidemiological cohort of 636 first-episode patients. Schizophr Res. 2007, 95 (1-3): 1-8. 10.1016/j.schres.2007.06.004.CrossRefPubMed Schimmelmann BG, Conus P, Cotton S, McGorry PD, Lambert M: Pre-treatment, baseline, and outcome differences between early-onset and adult-onset psychosis in an epidemiological cohort of 636 first-episode patients. Schizophr Res. 2007, 95 (1-3): 1-8. 10.1016/j.schres.2007.06.004.CrossRefPubMed
23.
go back to reference Downes JJ, Roberts AC, Sahakian BJ, Evenden JL, Morris RG, Robbins TW: Impaired extra-dimensional shift performance in medicated and unmedicated Parkinson's disease: evidence for a specific attentional dysfunction. Neuropsychologia. 1989, 27 (11-12): 1329-1343. 10.1016/0028-3932(89)90128-0.CrossRefPubMed Downes JJ, Roberts AC, Sahakian BJ, Evenden JL, Morris RG, Robbins TW: Impaired extra-dimensional shift performance in medicated and unmedicated Parkinson's disease: evidence for a specific attentional dysfunction. Neuropsychologia. 1989, 27 (11-12): 1329-1343. 10.1016/0028-3932(89)90128-0.CrossRefPubMed
24.
go back to reference Park SB, Coull JT, McShane RH, Young AH, Sahakian BJ, Robbins TW, Cowen PJ: Tryptophan depletion in normal volunteers produces selective impairments in learning and memory. Neuropharmacology. 1994, 33 (3-4): 575-588. 10.1016/0028-3908(94)90089-2.CrossRefPubMed Park SB, Coull JT, McShane RH, Young AH, Sahakian BJ, Robbins TW, Cowen PJ: Tryptophan depletion in normal volunteers produces selective impairments in learning and memory. Neuropharmacology. 1994, 33 (3-4): 575-588. 10.1016/0028-3908(94)90089-2.CrossRefPubMed
25.
go back to reference Owen AM, Downes JJ, Sahakian BJ, Polkey CE, Robbins TW: Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia. 1990, 28 (10): 1021-1034. 10.1016/0028-3932(90)90137-D.CrossRefPubMed Owen AM, Downes JJ, Sahakian BJ, Polkey CE, Robbins TW: Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia. 1990, 28 (10): 1021-1034. 10.1016/0028-3932(90)90137-D.CrossRefPubMed
26.
go back to reference Altman DG: Practical Statistics for Medical Research. 1990, London , Chapman and Hall Altman DG: Practical Statistics for Medical Research. 1990, London , Chapman and Hall
27.
go back to reference Rosenthal R, Rosnow RL, Rubin DB: Contrasts and Effect Sizes in Behavioral Research: A Correlational Approach. 2000, Cambridge , Cambridge University Press Rosenthal R, Rosnow RL, Rubin DB: Contrasts and Effect Sizes in Behavioral Research: A Correlational Approach. 2000, Cambridge , Cambridge University Press
28.
go back to reference Niv Y: Cost, benefit, tonic, phasic: what do response rates tell us about dopamine and motivation?. Ann N Y Acad Sci. 2007, 1104: 357-376. 10.1196/annals.1390.018.CrossRefPubMed Niv Y: Cost, benefit, tonic, phasic: what do response rates tell us about dopamine and motivation?. Ann N Y Acad Sci. 2007, 1104: 357-376. 10.1196/annals.1390.018.CrossRefPubMed
29.
go back to reference Crespi LP: Quantatative variation of incentive and performance in the white rat. American Journal of Psychology. 1942, 55: 467-517. 10.2307/1417120.CrossRef Crespi LP: Quantatative variation of incentive and performance in the white rat. American Journal of Psychology. 1942, 55: 467-517. 10.2307/1417120.CrossRef
30.
go back to reference Roiser JP, Blackwell AD, Cools R, Clark L, Rubinsztein DC, Robbins TW, Sahakian BJ: Serotonin transporter polymorphism mediates vulnerability to loss of incentive motivation following acute tryptophan depletion. Neuropsychopharmacology. 2006, 31 (10): 2264-2272. 10.1038/sj.npp.1301084.CrossRefPubMedPubMedCentral Roiser JP, Blackwell AD, Cools R, Clark L, Rubinsztein DC, Robbins TW, Sahakian BJ: Serotonin transporter polymorphism mediates vulnerability to loss of incentive motivation following acute tryptophan depletion. Neuropsychopharmacology. 2006, 31 (10): 2264-2272. 10.1038/sj.npp.1301084.CrossRefPubMedPubMedCentral
31.
go back to reference Wood SJ, Pantelis C, Proffitt T, Phillips LJ, Stuart GW, Buchanan JA, Mahony K, Brewer W, Smith DJ, McGorry PD: Spatial working memory ability is a marker of risk-for-psychosis. Psychol Med. 2003, 33 (7): 1239-1247. 10.1017/S0033291703008067.CrossRefPubMed Wood SJ, Pantelis C, Proffitt T, Phillips LJ, Stuart GW, Buchanan JA, Mahony K, Brewer W, Smith DJ, McGorry PD: Spatial working memory ability is a marker of risk-for-psychosis. Psychol Med. 2003, 33 (7): 1239-1247. 10.1017/S0033291703008067.CrossRefPubMed
32.
go back to reference Heerey EA, Gold JM: Patients with schizophrenia demonstrate dissociation between affective experience and motivated behavior. J Abnorm Psychol. 2007, 116 (2): 268-278. 10.1037/0021-843X.116.2.268.CrossRefPubMed Heerey EA, Gold JM: Patients with schizophrenia demonstrate dissociation between affective experience and motivated behavior. J Abnorm Psychol. 2007, 116 (2): 268-278. 10.1037/0021-843X.116.2.268.CrossRefPubMed
33.
go back to reference Juckel G, Schlagenhauf F, Koslowski M, Filonov D, Wustenberg T, Villringer A, Knutson B, Kienast T, Gallinat J, Wrase J, Heinz A: Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology (Berl). 2006, 187 (2): 222-228. 10.1007/s00213-006-0405-4.CrossRef Juckel G, Schlagenhauf F, Koslowski M, Filonov D, Wustenberg T, Villringer A, Knutson B, Kienast T, Gallinat J, Wrase J, Heinz A: Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology (Berl). 2006, 187 (2): 222-228. 10.1007/s00213-006-0405-4.CrossRef
34.
go back to reference Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD: Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature. 2006, 442 (7106): 1042-1045. 10.1038/nature05051.CrossRefPubMedPubMedCentral Pessiglione M, Seymour B, Flandin G, Dolan RJ, Frith CD: Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature. 2006, 442 (7106): 1042-1045. 10.1038/nature05051.CrossRefPubMedPubMedCentral
35.
go back to reference Robbins TW, Everitt BJ: Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol. 1996, 6 (2): 228-236. 10.1016/S0959-4388(96)80077-8.CrossRefPubMed Robbins TW, Everitt BJ: Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol. 1996, 6 (2): 228-236. 10.1016/S0959-4388(96)80077-8.CrossRefPubMed
36.
go back to reference Berridge KC: The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl). 2007, 191 (3): 391-431. 10.1007/s00213-006-0578-x.CrossRef Berridge KC: The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl). 2007, 191 (3): 391-431. 10.1007/s00213-006-0578-x.CrossRef
37.
go back to reference Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, Honey G, Jones PB, Bullmore ET, Robbins TW, Fletcher PC: Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry. 2008, 13 (3): 239-276. 10.1038/sj.mp.4002157.CrossRefPubMed Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, Honey G, Jones PB, Bullmore ET, Robbins TW, Fletcher PC: Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry. 2008, 13 (3): 239-276. 10.1038/sj.mp.4002157.CrossRefPubMed
38.
go back to reference Juckel G, Schlagenhauf F, Koslowski M, Wustenberg T, Villringer A, Knutson B, Wrase J, Heinz A: Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage. 2006, 29 (2): 409-416. 10.1016/j.neuroimage.2005.07.051.CrossRefPubMed Juckel G, Schlagenhauf F, Koslowski M, Wustenberg T, Villringer A, Knutson B, Wrase J, Heinz A: Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage. 2006, 29 (2): 409-416. 10.1016/j.neuroimage.2005.07.051.CrossRefPubMed
39.
go back to reference Gard DE, Kring AM, Gard MG, Horan WP, Green MF: Anhedonia in schizophrenia: distinctions between anticipatory and consummatory pleasure. Schizophr Res. 2007, 93 (1-3): 253-260. 10.1016/j.schres.2007.03.008.CrossRefPubMedPubMedCentral Gard DE, Kring AM, Gard MG, Horan WP, Green MF: Anhedonia in schizophrenia: distinctions between anticipatory and consummatory pleasure. Schizophr Res. 2007, 93 (1-3): 253-260. 10.1016/j.schres.2007.03.008.CrossRefPubMedPubMedCentral
40.
go back to reference Barch DM: The relationships among cognition, motivation, and emotion in schizophrenia: how much and how little we know. Schizophr Bull. 2005, 31 (4): 875-881. 10.1093/schbul/sbi040.CrossRefPubMed Barch DM: The relationships among cognition, motivation, and emotion in schizophrenia: how much and how little we know. Schizophr Bull. 2005, 31 (4): 875-881. 10.1093/schbul/sbi040.CrossRefPubMed
Metadata
Title
Incentive motivation in first-episode psychosis: A behavioural study
Authors
Graham K Murray
Luke Clark
Philip R Corlett
Andrew D Blackwell
Roshan Cools
Peter B Jones
Trevor W Robbins
Luise Poustka
Publication date
01-12-2008
Publisher
BioMed Central
Published in
BMC Psychiatry / Issue 1/2008
Electronic ISSN: 1471-244X
DOI
https://doi.org/10.1186/1471-244X-8-34

Other articles of this Issue 1/2008

BMC Psychiatry 1/2008 Go to the issue