Hostname: page-component-7b9c58cd5d-dkgms Total loading time: 0 Render date: 2025-03-15T21:54:05.425Z Has data issue: false hasContentIssue false
  • English
  • Français

Increased salience of gains versus decreased associative learning differentiate bipolar disorder from schizophrenia during incentive decision making

Published online by Cambridge University Press:  12 June 2012

P. Brambilla ,
C. Perlini ,
M. Bellani ,
L. Tomelleri ,
A. Ferro ,
S. Cerruti ,
V. Marinelli ,
G. Rambaldelli ,
T. Christodoulou  and
J. Jogia
...Show all authors
P. Brambilla
Affiliation:
DISM, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Udine, Italy IRCCS ‘E. Medea’ Scientific Institute, Udine, Italy
C. Perlini
Affiliation:
Section of Psychiatry and Clinical Psychology, DMSP, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Verona, Italy
M. Bellani
Affiliation:
Section of Psychiatry and Clinical Psychology, DMSP, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Verona, Italy
L. Tomelleri
Affiliation:
Section of Psychiatry and Clinical Psychology, DMSP, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Verona, Italy
A. Ferro
Affiliation:
Section of Psychiatry and Clinical Psychology, DMSP, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Verona, Italy
S. Cerruti
Affiliation:
Section of Psychiatry and Clinical Psychology, DMSP, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Verona, Italy
V. Marinelli
Affiliation:
Section of Psychiatry and Clinical Psychology, DMSP, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Verona, Italy
G. Rambaldelli
Affiliation:
Section of Psychiatry and Clinical Psychology, DMSP, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Verona, Italy
T. Christodoulou
Affiliation:
Section of Neurobiology of Psychosis, Institute of Psychiatry, King's College London, UK
J. Jogia
Affiliation:
Section of Neurobiology of Psychosis, Institute of Psychiatry, King's College London, UK
D. Dima
Affiliation:
Section of Neurobiology of Psychosis, Institute of Psychiatry, King's College London, UK
M. Tansella
Affiliation:
Section of Psychiatry and Clinical Psychology, DMSP, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Verona, Italy
M. Balestrieri
Affiliation:
DISM, Inter-University Centre for Behavioural Neurosciences (ICBN), University of Udine, Italy
S. Frangou*
Affiliation:
Section of Neurobiology of Psychosis, Institute of Psychiatry, King's College London, UK
*
*Address for correspondence: Dr S. Frangou, Section of Neurobiology of Psychosis, Department of Psychosis Studies, Institute of Psychiatry, King's College London, De Crespigny Park, London SE5 8AF, UK. (Email: sophia.frangou@kcl.ac.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Abnormalities in incentive decision making, typically assessed using the Iowa Gambling Task (IGT), have been reported in both schizophrenia (SZ) and bipolar disorder (BD). We applied the Expectancy–Valence (E–V) model to determine whether motivational, cognitive and response selection component processes of IGT performance are differentially affected in SZ and BD.

Method

Performance on the IGT was assessed in 280 individuals comprising 70 remitted patients with SZ, 70 remitted patients with BD and 140 age-, sex- and IQ-matched healthy individuals. Based on the E–V model, we extracted three parameters, ‘attention to gains or loses’, ‘expectancy learning’ and ‘response consistency’, that respectively reflect motivational, cognitive and response selection influences on IGT performance.

Results

Both patient groups underperformed in the IGT compared to healthy individuals. However, the source of these deficits was diagnosis specific. Associative learning underlying the representation of expectancies was disrupted in SZ whereas BD was associated with increased incentive salience of gains. These findings were not attributable to non-specific effects of sex, IQ, psychopathology or medication.

Conclusions

Our results point to dissociable processes underlying abnormal incentive decision making in BD and SZ that could potentially be mapped to different neural circuits.

Keywords

Bipolar disorderdecision makingexpectancy–valencegamblingmotivationrewardsalienceschizophrenia
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 3 , March 2013 , pp. 571 - 580
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adida, M, Clark, L, Pomietto, P, Kaladjian, A, Besnier, N, Azorin, JM, Jeanningros, R, Goodwin, GM (2008). Lack of insight may predict impaired decision making in manic patients. Bipolar Disorders 10, 829–837.CrossRefGoogle ScholarPubMed
Adida, M, Jollant, F, Clark, L, Besnier, N, Guillaume, S, Kaladjian, A, Mazzola-Pomietto, P, Jeanningros, R, Goodwin, GM, Azorin, JM, Courtet, P (2011). Trait-related decision-making impairment in the three phases of bipolar disorder. Biological Psychiatry 70, 357–365.CrossRefGoogle ScholarPubMed
APA (1994). Diagnostic and Statistical Manual of Mental Disorders: DSM-IV. American Psychiatric Association: Washington, DC.Google Scholar
Barch, DM (2005). The relationships among cognition, motivation, and emotion in schizophrenia: how much and how little we know. Schizophrenia Bulletin 31, 875–881.CrossRefGoogle ScholarPubMed
Bechara, A, Damasio, AR, Damasio, H, Anderson, SW (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15.CrossRefGoogle ScholarPubMed
Bechara, A, Damasio, H, Tranel, D, Anderson, WS (1998). Dissociation of working memory from decision making within the human prefrontal cortex. Journal of Neuroscience 18, 426–437.CrossRefGoogle ScholarPubMed
Bellani, M, Tomelleri, L, Brambilla, P (2009). Emotion-based decision making in schizophrenia: evidence from the Iowa Gambling Task. Epidemiologia e Psichiatria Sociale 18, 104–106.CrossRefGoogle ScholarPubMed
Beninger, RJ, Wasserman, J, Zanibbi, K, Charbonneau, D, Mangels, J, Beninger, BV (2003). Typical and atypical antipsychotic medications differentially affect two nondeclarative memory tasks in schizophrenic patients: a double dissociation. Schizophrenia Research 61, 281–292.CrossRefGoogle ScholarPubMed
Bermpohl, F, Kahnt, T, Dalanay, U, Hägele, C, Sajonz, B, Wegner, T, Stoy, M, Adli, M, Krüger, S, Wrase, J, Ströhle, A, Bauer, M, Heinz, A (2010). Altered representation of expected value in the orbitofrontal cortex in mania. Human Brain Mapping 31, 958–969.CrossRefGoogle ScholarPubMed
Berridge, KC, Kringelbach, ML (2008). Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berlin) 199, 457–480.CrossRefGoogle ScholarPubMed
Bezchlibnyk-Butler, KZ, Jeffries, JJ (2000). Clinical Handbook of Psychotropic Drugs, 10th edn.Hogrefe & Huber: Seattle, pp. 84–88.Google Scholar
Busemeyer, JR, Johnson, JG (2004). Computational models of decision making. In Blackwell Handbook of Judgment and Decision Making(ed. Koehler, D. and Harvey, N.), pp. 133–154. Blackwell Publishing Co.: New York.CrossRefGoogle Scholar
Busemeyer, JR, Stout, JC (2002). A contribution of cognitive decision models to clinical assessment. Decomposing performance on the Bechara gambling task. Psychological Assessment 14, 253–262.CrossRefGoogle ScholarPubMed
Cavallaro, R, Cavedini, P, Mistretta, P, Bassi, T, Angelone, SM, Ubbiali, A, Bellodi, L (2003). Basal-corticofrontal circuits in schizophrenia and obsessive-compulsive disorder: a controlled, double dissociation study. Biological Psychiatry 54, 437–443.CrossRefGoogle ScholarPubMed
Chandler, RA, Wakeley, J, Goodwin, GM, Rogers, RD (2009). Altered risk-aversion and risk-seeking behavior in bipolar disorder. Biological Psychiatry 66, 840–846.CrossRefGoogle ScholarPubMed
Christodoulou, T, Lewis, M, Ploubidis, GB, Frangou, S (2006). The relationship of impulsivity to response inhibition and decision-making in remitted patients with bipolar disorder. European Psychiatry 21, 270–273.CrossRefGoogle ScholarPubMed
Clark, L, Iversen, SD, Goodwin, GM (2001). A neuropsychological investigation of prefrontal cortex involvement in acute mania. American Journal of Psychiatry 158, 1605–1611.CrossRefGoogle ScholarPubMed
Cohen, J (1998). Statistical Power Analysis for the Behavioral Sciences, 2nd edn.Lawrence Erlbaum Associates: Hillsdale, NJ.Google Scholar
Corlett, PR, Murray, GK, Honey, GD, Aitken, MR, Shanks, DR, Robbins, TW, Bullmore, ET, Dickinson, A, Fletcher, PC (2007). Disrupted prediction-error signal in psychosis: evidence for an associative account of delusions. Brain 130, 2387–2400.CrossRefGoogle ScholarPubMed
Donaldson, S, Goldstein, LH, Landau, S, Raymont, V, Frangou, S (2003). The Maudsley Bipolar Disorder Project: the effect of medication, family history, and duration of illness on IQ and memory in bipolar I disorder. Journal of Clinical Psychiatry 64, 86–93.CrossRefGoogle Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002 a). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Patient Edition (SCID-I/P). Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
First, MB, Spitzer, RL, Gibbon, M, Williams, JBW (2002 b). Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version, Non-Patient Edition (SCID-I/NP). Biometrics Research, New York State Psychiatric Institute: New York.Google Scholar
Frangou, S, Dakhil, N, Landau, S, Kumari, V (2006). Fronto-temporal function may distinguish bipolar disorder from schizophrenia. Bipolar Disorders 8, 47–55.CrossRefGoogle ScholarPubMed
Frangou, S, Donaldson, S, Hadjulis, M, Landau, S, Goldstein, LH (2005). The Maudsley Bipolar Disorder Project: executive dysfunction in bipolar disorder I and its clinical correlates. Biological Psychiatry 58, 859–864.CrossRefGoogle ScholarPubMed
Frangou, S, Kington, J, Raymont, V, Shergill, SS (2008). Examining ventral and dorsal prefrontal function in bipolar disorder: a functional magnetic resonance imaging study. European Psychiatry 23, 300–308.CrossRefGoogle ScholarPubMed
Frank, MJ, Claus, ED (2006). Anatomy of a decision: striato-orbitofrontal interactions in reinforcement learning, decision making, and reversal. Psychological Review 113, 300–326.CrossRefGoogle ScholarPubMed
Gold, JM, Waltz, JA, Prentice, KJ, Morris, SE, Heerey, EA (2008). Reward processing in schizophrenia: a deficit in the representation of value. Schizophrenia Bulletin 34, 835–847.CrossRefGoogle ScholarPubMed
Hamilton, MA (1960). Rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry 23, 56–62.CrossRefGoogle ScholarPubMed
Jogia, J, Dima, D, Kumari, V, Frangou, S (2011). Frontopolar cortical inefficiency may underpin reward and working memory dysfunction in bipolar disorder. World Journal of Biological Psychiatry. Published online: 3 August 2011. doi:10.3109/15622975.2011.585662.Google ScholarPubMed
Juckel, G, Schlagenhauf, F, Koslowski, M, Filonov, D, Wüstenberg, T, Villringer, A, Knutson, B, Kienast, T, Gallinat, J, Wrase, J, Heinz, A (2006). Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology (Berlin) 187, 222–228.CrossRefGoogle Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Lawrie, SM, Hall, J, McIntosh, AM, Owens, DG, Johnstone, EC (2010). The ‘continuum of psychosis’: scientifically unproven and clinically impractical. British Journal of Psychiatry 197, 423–425.CrossRefGoogle ScholarPubMed
Lukoff, D, Nuechterlien, K, Ventura, J (1986). Manual for the expanded Brief Psychiatric Rating Scale. Schizophrenia Bulletin 12, 594–608.Google Scholar
Martino, DJ, Strejilevich, SA, Torralva, T, Manes, F (2011). Decision making in euthymic bipolar I and bipolar II disorders. Psychological Medicine 41, 1319–1327.CrossRefGoogle ScholarPubMed
Minassian, A, Paulus, MP, Perry, W (2004). Increased sensitivity error during decision-making in bipolar disorder patients acute mania. Journal of Affective Disorders 82, 203–208.CrossRefGoogle ScholarPubMed
Nelson, HE (1976). A modified card sorting test sensitive to frontal lobe defects. Cortex 12, 313–324.CrossRefGoogle ScholarPubMed
Nuechterlein, KH, Miklowitz, DJ, Ventura, J, Gitlin, MJ, Stoddard, M, Lukoff, D (2006). Classifying episodes in schizophrenia and bipolar disorder: criteria for relapse and remission applied to recent-onset samples. Psychiatry Research 144, 153–165.CrossRefGoogle ScholarPubMed
Orsini, A, Laicardi, C (1997). WAIS-R. Contributo alla Taratura Italiana. Organizzazioni Speciali: Firenze.Google Scholar
Peruzzo, D, Rambaldelli, G, Bertoldo, A, Bellani, M, Cerini, R, Silvia, M, Pozzi Mucelli, R, Tansella, M, Brambilla, P (2011). The impact of schizophrenia on frontal perfusion parameters: a DSC-MRI study. Journal of Neural Transmission 118, 563–570.CrossRefGoogle ScholarPubMed
Premkumar, P, Fannon, D, Kuipers, E, Simmons, A, Frangou, S, Kumari, V (2008). Emotional decision-making and its dissociable components in schizophrenia and schizoaffective disorder: a behavioural and MRI investigation. Neuropsychologia 46, 2002–2012.CrossRefGoogle ScholarPubMed
Reavis, R, Overman, WH (2001). Adult sex differences on a decision-making task previously shown to depend on the orbital prefrontal cortex. Behavioral Neuroscience 115, 196–206.CrossRefGoogle ScholarPubMed
Ritter, LM, Meador-Woodruff, JH, Dalack, GW (2004). Neurocognitive measures of prefrontal cortical dysfunction in schizophrenia. Schizophrenia Research 68, 65–73.CrossRefGoogle ScholarPubMed
Roiser, JP, Cannon, DM, Gandhi, SK, Taylor Tavares, J, Erickson, K, Wood, S, Klaver, JM, Clark, L, Zarate, CA Jr., Sahakian, BJ, Drevets, WC (2009). Hot and cold cognition in unmedicated depressed subjects with bipolar disorder. Bipolar Disorders 11, 178–189.CrossRefGoogle ScholarPubMed
Ruberto, G, Vassos, E, Lewis, CM, Tatarelli, R, Girardi, P, Collier, D, Frangou, S (2011). The cognitive impact of the ANK3 risk variant for bipolar disorder: initial evidence of selectivity to signal detection during sustained attention. PLoS ONE 6, e16671.CrossRefGoogle ScholarPubMed
Schlagenhauf, F, Juckel, G, Koslowski, M, Kahnt, T, Knutson, B, Dembler, T, Kienast, T, Gallinat, J, Wrase, J, Heinz, A (2008). Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine. Psychopharmacology (Berlin) 196, 673–684.CrossRefGoogle ScholarPubMed
Schultz, W (1998). Predictive reward signal of dopamine neurons. Journal of Neurophysiology 80, 1–27.CrossRefGoogle ScholarPubMed
Schultz, W (2002). Getting formal with dopamine and reward. Neuron 36, 241–263.CrossRefGoogle ScholarPubMed
Sevy, S, Hassoun, Y, Bechara, A, Yechiam, E, Napolitano, B, Burdick, K, Delman, H, Malhotra, A (2006). Emotion-based decision-making in healthy subjects: short-term effects of reducing dopamine levels. Psychopharmacology (Berlin) 188, 228–235.CrossRefGoogle ScholarPubMed
Sevy, S, Burdick, KE, Visweswaraiah, H, Abdelmessih, S, Lukin, M, Yechiam, E, Bechara, A (2007). Iowa Gambling Task in schizophrenia: a review and new data in patients with schizophrenia and co-occurring cannabis use disorders. Schizophrenia Research 92, 74–84.CrossRefGoogle ScholarPubMed
Shurman, B, Horan, WP, Nuechterlein, KH (2005). Schizophrenia patients demonstrate a distinctive pattern of decision-making impairment on the Iowa Gambling Task. Schizophrenia Research 72, 215–224.CrossRefGoogle ScholarPubMed
Stefanopoulou, E, Manoharan, A, Landau, S, Geddes, JR, Goodwin, G, Frangou, S (2009). Cognitive functioning in patients with affective disorders and schizophrenia: a meta-analysis. International Reviews of Psychiatry 21, 336–356.CrossRefGoogle ScholarPubMed
Tomelleri, L, Jogia, J, Perlini, C, Bellani, M, Ferro, A, Rambaldelli, G, Tansella, M, Frangou, S, Brambilla, P; Neuroimaging Network of the ECNP networks initiative (2009). Brain structural changes associated with chronicity and antipsychotic treatment in schizophrenia. European Neuropsychopharmacology 19, 835–840.CrossRefGoogle ScholarPubMed
Toplak, ME, Sorge, GB, Benoit, A, West, RF, Stanovich, KE (2010). Decision-making and cognitive abilities: a review of associations between Iowa Gambling Task performance, executive functions, and intelligence. Clinical Psychology Review 30, 562–581.CrossRefGoogle ScholarPubMed
Ursu, S, Carter, CS (2005). Outcome representations, counterfactual comparisons and the human orbitofrontal cortex: implications for neuroimaging studies of decision-making. Cognitive Brain Research 23, 51–60.CrossRefGoogle ScholarPubMed
Wechsler, D (1981). Wechsler Adult Intelligence Scale-Revised (WAIS-R) Manual. Psychological Corporation: New York.Google Scholar
Yechiam, E, Hayden, EP, Bodkins, M, O'Donnell, BF, Hetrick, WP (2008). Decision making in bipolar disorder: a cognitive modelling approach. Psychiatry Research 161, 142–152.CrossRefGoogle Scholar
Young, R, Biggs, J, Zieglar, V, Meyer, D (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429–435.CrossRefGoogle ScholarPubMed
Ziauddeen, H, Murray, GK (2010). The relevance of reward pathways for schizophrenia. Current Opinion in Psychiatry 23, 91–96.CrossRefGoogle ScholarPubMed
Supplementary material: File

Brambilla supplementary material

Appendix

Download Brambilla supplementary material(File)
File 27.6 KB