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Patients with schizophrenia show increased aversion to angry faces in an associative learning task

Published online by Cambridge University Press:  20 October 2010

S. Evans
Affiliation:
Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, UCL, London, UK
S. S. Shergill
Affiliation:
Cognition, Schizophrenia and Imaging Laboratory, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
V. Chouhan
Affiliation:
Cognition, Schizophrenia and Imaging Laboratory, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
E. Bristow
Affiliation:
Cognition, Schizophrenia and Imaging Laboratory, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
T. Collier
Affiliation:
Cognition, Schizophrenia and Imaging Laboratory, Department of Psychosis Studies, Institute of Psychiatry, King's College London, London, UK
B. B. Averbeck*
Affiliation:
Sobell Department of Motor Neuroscience and Movement Disorders, Institute of Neurology, UCL, London, UK Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, MD, USA
*
*Address for correspondence: B. B. Averbeck, Ph.D., Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, MD 20892, USA. (Email: averbeckbb@mail.nih.gov)

Abstract

Background

We were interested in examining the relationship between socially relevant stimuli and decision processes in patients with schizophrenia.

Method

We tested patients with schizophrenia and healthy controls on a stochastically rewarded associative learning task. Participants had to determine, through trial and error, which of two faces was associated with a higher chance of reward: one face was angry, the other happy.

Results

Both patients and healthy controls were able to perform the task at above-chance accuracy, and there was no significant difference in overall accuracy between the groups. Both groups also reliably preferred the happy face, such that they selected it more often than the angry face on the basis of the same amount of positive versus negative feedback. However, patients were significantly more averse to the angry face, such that they chose it less often than control participants when the reward feedback strongly supported the angry face as the best choice.

Conclusions

Patients show an increased aversion to angry faces, in a task in which they must learn to associate rewards with expressions.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2010

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References

Abi-Dargham, A, Gil, R, Krystal, J, Baldwin, RM, Seibyl, JP, Bowers, M, van Dyck, CH, Charney, DS, Innis, RB, Laruelle, M (1998). Increased striatal dopamine transmission in schizophrenia: confirmation in a second cohort. American Journal of Psychiatry 155, 761767.Google Scholar
APA (1994). Diagnostic and Statistical Manual of Mental Disorders, 4th edn. American Psychiatric Association: Washington, DC.Google Scholar
Archer, J, Hay, DC, Young, AW (1994). Movement, face processing and schizophrenia: evidence of a differential deficit in expression analysis. British Journal of Clinical Psychology 33 (Pt 4), 517528.Google Scholar
Averbeck, BB, Duchaine, B (2009). Integration of social and utilitarian factors in decision making. Emotion 9, 599608.Google Scholar
Bortolozzi, A, Díaz-Mataix, L, Artigas, F (2007). Pharmacology. In Antidepressants, Antipsychotics, Anxiolytics (ed. Buschmann, H., Diaz, J. L., Holenz, J., Parraga, A., Torrens, A. and Vela, J. M.), pp. 389448. Wiley-VCH: Weinheim.Google Scholar
Breier, A, Su, TP, Saunders, R, Carson, RE, Kolachana, BS, de Bartolomeis, A, Weinberger, DR, Weisenfeld, N, Malhotra, AK, Eckelman, WC, Pickar, D (1997). Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. Proceedings of the National Academy of Sciences USA 94, 25692574.Google Scholar
Chen, Y, Norton, D, McBain, R, Ongur, D, Heckers, S (2009). Visual and cognitive processing of face information in schizophrenia: detection, discrimination and working memory. Schizophrenia Research 107, 9298.CrossRefGoogle Scholar
Cools, R, Altamirano, L, D'Esposito, M (2006). Reversal learning in Parkinson's disease depends on medication status and outcome valence. Neuropsychologia 44, 16631673.Google Scholar
Cools, R, Frank, MJ, Gibbs, SE, Miyakawa, A, Jagust, W, D'Esposito, M (2009). Striatal dopamine predicts outcome-specific reversal learning and its sensitivity to dopaminergic drug administration. Journal of Neuroscience 29, 15381543.Google Scholar
Davis, KL, Kahn, RS, Ko, G, Davidson, M (1991). Dopamine in schizophrenia: a review and reconceptualization. American Journal of Psychiatry 148, 14741486.Google Scholar
Djamshidian, A, Jha, A, O'Sullivan, SS, Silveira-Moriyama, L, Jacobson, C, Brown, P, Lees, AJ, Averbeck, BB (2010). Risk and learning in impulsive and nonimpulsive patients with Parkinson's disease. Movement Disorders. Published online: 18 August 2010. doi:10.1002/mds.23247.Google Scholar
Done, DJ, Crow, TJ, Johnstone, EC, Sacker, A (1994). Childhood antecedents of schizophrenia and affective illness: social adjustment at ages 7 and 11. Briitish Medical Journal 309, 699703.CrossRefGoogle Scholar
Edwards, J, Jackson, HJ, Pattison, PE (2002). Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clinical Psychology Review 22, 789832.Google Scholar
Ekman, P, Friesen, WV (1971). Constants across cultures in the face and emotion. Journal of Personality and Social Psychology 17, 124129.Google Scholar
Feinberg, TE, Rifkin, A, Schaffer, C, Walker, E (1986). Facial discrimination and emotional recognition in schizophrenia and affective disorders. Archives of General Psychiatry 43, 276279.Google Scholar
Frank, MJ, Moustafa, AA, Haughey, HM, Curran, T, Hutchison, KE (2007). Genetic triple dissociation reveals multiple roles for dopamine in reinforcement learning. Proceedings of the National Academy of Sciences USA 104, 1631116316.Google Scholar
Frank, MJ, Seeberger, LC, O'Reilly, RC (2004). By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science 306, 19401943.Google Scholar
Gaebel, W, Wolwer, W (1992). Facial expression and emotional face recognition in schizophrenia and depression. European Archives of Psychiatry and Clinical Neuroscience 242, 4652.Google Scholar
Gosselin, P, Kirouac, G, Dore, FY (1995). Components and recognition of facial expression in the communication of emotion by actors. Journal of Personality and Social Psychology 68, 8396.Google Scholar
Herbener, ES (2009). Impairment in long-term retention of preference conditioning in schizophrenia. Biological Psychiatry 65, 10861090.Google Scholar
Herbener, ES, Rosen, C, Khine, T, Sweeney, JA (2007). Failure of positive but not negative emotional valence to enhance memory in schizophrenia. Journal of Abnormal Psychology 116, 4355.Google Scholar
Holmes, AP, Friston, KJ (1998). Generalisability, random effects and population inference. NeuroImage 7, s754.Google Scholar
Kahneman, D, Slovic, P, Tversky, A (1982). Judgment Under Uncertainty: Heuristics and Biases. Cambridge University Press: Cambridge.CrossRefGoogle Scholar
Laroi, F, Fonteneau, B, Mourad, H, Raballo, A (2010). Basic emotion recognition and psychopathology in schizophrenia. Journal of Nervous and Mental Disease 198, 7981.Google Scholar
Laruelle, M, Abi-Dargham, A, van Dyck, CH, Gil, R, D'Souza, CD, Erdos, J, McCance, E, Rosenblatt, W, Fingado, C, Zoghbi, SS, Baldwin, RM, Seibyl, JP, Krystal, JH, Charney, DS, Innis, RB (1996). Single photon emission computerized tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. Proceedings of the National Academy of Sciences USA 93, 92359240.Google Scholar
Linden, SC, Jackson, MC, Subramanian, L, Wolf, C, Green, P, Healy, D, Linden, DE (2010). Emotion-cognition interactions in schizophrenia: implicit and explicit effects of facial expression. Neuropsychologia 48, 997–1002.Google Scholar
Mandal, MK (1987). Decoding of facial emotions, in terms of expressiveness, by schizophrenics and depressives. Psychiatry 50, 371376.Google Scholar
Meyer, MB, Kurtz, MM (2009). Elementary neurocognitive function, facial affect recognition and social-skills in schizophrenia. Schizophrenia Research 110, 173179.CrossRefGoogle Scholar
Mueser, KT, Doonan, R, Penn, DL, Blanchard, JJ, Bellack, AS, Nishith, P, DeLeon, J (1996). Emotion recognition and social competence in chronic schizophrenia. Journal of Abnormal Psychology 105, 271275.Google Scholar
Murray, GK, Cheng, F, Clark, L, Barnett, JH, Blackwell, AD, Fletcher, PC, Robbins, TW, Bullmore, ET, Jones, PB (2008). Reinforcement and reversal learning in first-episode psychosis. Schizophrenia Bulletin 34, 848855.Google Scholar
Norton, D, McBain, R, Holt, DJ, Ongur, D, Chen, Y (2009). Association of impaired facial affect recognition with basic facial and visual processing deficits in schizophrenia. Biological Psychiatry 65, 10941098.Google Scholar
Penn, DL, Sanna, LJ, Roberts, DL (2008). Social cognition in schizophrenia: an overview. Schizophrenia Bulletin 34, 408411.Google Scholar
Pessiglione, M, Seymour, B, Flandin, G, Dolan, RJ, Frith, CD (2006). Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442, 10421045.Google Scholar
Premkumar, P, Cooke, MA, Fannon, D, Peters, E, Michel, TM, Aasen, I, Murray, RM, Kuipers, E, Kumari, V (2008 a). Misattribution bias of threat-related facial expressions is related to a longer duration of illness and poor executive function in schizophrenia and schizoaffective disorder. European Psychiatry 23, 1419.Google Scholar
Premkumar, P, Fannon, D, Kuipers, E, Simmons, A, Frangou, S, Kumari, V (2008 b). Emotional decision-making and its dissociable components in schizophrenia and schizoaffective disorder: a behavioural and MRI investigation. Neuropsychologia 46, 20022012.Google Scholar
Prentice, KJ, Gold, JM, Buchanan, RW (2008). The Wisconsin Card Sorting impairment in schizophrenia is evident in the first four trials. Schizophrenia Research 106, 8187.Google Scholar
Rutledge, RB, Lazzaro, SC, Lau, B, Myers, CE, Gluck, MA, Glimcher, PW (2009). Dopaminergic drugs modulate learning rates and perseveration in Parkinson's patients in a dynamic foraging task. Journal of Neuroscience 29, 1510415114.Google Scholar
Salem, JE, Kring, AM, Kerr, SL (1996). More evidence for generalized poor performance in facial emotion perception in schizophrenia. Journal of Abnormal Psychology 105, 480483.Google Scholar
Schneider, F, Gur, RC, Gur, RE, Shtasel, DL (1995). Emotional processing in schizophrenia: neurobehavioral probes in relation to psychopathology. Schizophrenia Research 17, 6775.Google Scholar
Schultz, W (2002). Getting formal with dopamine and reward. Neuron 36, 241263.Google Scholar
Voon, V, Reynolds, B, Brezing, C, Gallea, C, Skaljic, M, Ekanayake, V, Fernandez, H, Potenza, MN, Dolan, RJ, Hallett, M (2010). Impulsive choice and response in dopamine agonist-related impulse control behaviors. Psychopharmacology 207, 645659.Google Scholar
Waltz, JA, Frank, MJ, Robinson, BM, Gold, JM (2007). Selective reinforcement learning deficits in schizophrenia support predictions from computational models of striatal-cortical dysfunction. Biological Psychiatry 62, 756764.Google Scholar
Waltz, JA, Gold, JM (2007). Probabilistic reversal learning impairments in schizophrenia: further evidence of orbitofrontal dysfunction. Schizophrenia Research 93, 296303.Google Scholar
Weinberger, DR (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry 44, 660669.Google Scholar
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