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Impaired subjective well-being in schizophrenia is associated with reduced anterior cingulate activity during reward processing

Published online by Cambridge University Press:  28 July 2014

J. Gilleen*
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, King's College London, UK
S. S. Shergill
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, King's College London, UK
S. Kapur
Affiliation:
Department of Psychosis Studies, Institute of Psychiatry, King's College London, UK
*
* Address for correspondence: J. Gilleen, Ph.D., Department of Psychosis Studies, Institute of Psychiatry, King's College London, PO Box 63, De Crespigny Park, Denmark Hill, London SE5 8AF, UK. (Email: james.1.gilleen@kcl.ac.uk)

Abstract

Background

Patients with schizophrenia have substantially reduced subjective well-being (SW) compared to healthy individuals. It has been suggested that diminished SW may be related to deficits in the neural processing of reward but this has not been shown directly. We hypothesized that, in schizophrenia, lower SW would be associated with attenuated reward-related activation in the reward network.

Method

Twenty patients with schizophrenia with a range of SW underwent a functional magnetic resonance imaging (fMRI) reward task. The brain activity underlying reward anticipation and outcome in schizophrenia was examined and compared to that of 12 healthy participants using a full factorial analysis. Region of interest (ROI) analyses of areas within the reward network and whole-brain analyses were conducted to reveal neural correlates of SW.

Results

Reward-related neural activity in schizophrenia was not significantly different from that of healthy participants; however, the patients with schizophrenia showed significantly diminished SW. Both ROI and whole-brain analyses confirmed that SW scores in the patients correlated significantly with activity, specifically in the dorsal anterior cingulate cortex (dACC), during both reward anticipation and reward outcome. This association was not seen in the healthy participants.

Conclusions

In patients with schizophrenia, reduced activation of the dACC during multiple aspects of reward processing is associated with lower SW. As the dACC has been widely linked to coupling of reward and action, and the link to SW is apparent over anticipation and outcome, these findings suggest that SW deficits in schizophrenia may be attributable to reduced integration of environmental rewarding cues, motivated behaviour and reward outcome.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2014 

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References

Abler, B, Erk, S, Walter, H (2007). Human reward system activation is modulated by a single dose of olanzapine in healthy subjects in an event-related, double-blind, placebo-controlled fMRI study. Psychopharmacology 191, 823833.Google Scholar
Abler, B, Kammerer, H, Frasch, K, Spitzer, M, Walter, H (2008). Altered reward processing in schizophrenic patients treated with olanzapine. Schizophrenia Research 98 (Suppl.), 116.Google Scholar
Averbeck, B, Evans, S, Chouhan, V, Bristow, E, Shergill, SS (2011). Probabilistic learning and inference in schizophrenia. Schizophrenia Research 127, 115122.Google Scholar
Barnes, TR (1989). A rating scale for drug-induced akathisia. British Journal of Psychiatry 154, 672676.Google Scholar
Beck, AT, Steer, RA, Ball, R, Ranieri, W (1996). Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. Journal of Personality Assessment 67, 588597.Google Scholar
Bench, CJ, Friston, KJ, Brown, RG, Scott, LC, Frackowiak, RS, Dolan, RJ (1992). The anatomy of melancholia – focal abnormalities of cerebral blood flow in major depression. Psychological Medicine 22, 607615.Google Scholar
Chouinard, G, Ross-Chouinard, A, Annable, L, Jones, B (1980). The extrapyramidal symptom rating scale. Canadian Journal of Neurological Sciences 7, 233239.Google Scholar
Critchley, HD, Mathias, CJ, Dolan, RJ (2001). Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29, 537545.CrossRefGoogle ScholarPubMed
da Silva Alves, D, Schmitz, N, Figee, M, Abeling, N, Hasler, G, van der Meer, J, Nederveen, A, de Haan, L, Linszen, D, van Amelsvoort, T (2010). Dopaminergic modulation of the human reward system: a placebo-controlled dopamine depletion fMRI study. Journal of Psychopharmacology 25, 538549.Google Scholar
de Haan, L, Lavalaye, J, Linszen, D, Dingemans, PM, Booij, J (2000). Subjective experience and striatal dopamine D(2) receptor occupancy in patients with schizophrenia stabilized by olanzapine or risperidone. American Journal of Psychiatry 157, 10191020.Google Scholar
Dolan, RJ, Fletcher, P, Frith, CD, Friston, KJ, Frackowiak, RS, Grasby, PM (1995). Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia. Nature 378, 180182.Google Scholar
Friston, KJ, Fletcher, P, Josephs, O, Holmes, A, Rugg, MD, Turner, R (1998). Event-related fMRI: characterizing differential responses. NeuroImage 17, 3040.Google Scholar
Gard, DE, Kring, AM, Gard, MG, Horan, WP, Green, MF (2007). Anhedonia in schizophrenia: distinctions between anticipatory and consummatory pleasure. Schizophrenia Research 93, 253260.CrossRefGoogle ScholarPubMed
Haber, SN, Knutson, B (2010). The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35, 426.Google Scholar
Harvey, PO, Pruessner, J, Czechowska, Y, Lepage, M (2007). Individual differences in trait anhedonia: a structural and functional magnetic resonance imaging study in non-clinical subjects. Molecular Psychiatry 12, 767775.Google Scholar
Juckel, G, Schlagenhauf, F, Koslowski, M, Filonov, D, Wustenberg, 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 187, 222228.CrossRefGoogle Scholar
Karow, A, Czekalla, J, Dittmann, RW, Schacht, A, Wagner, T, Lambert, M, Schimmelmann, BG, Naber, D (2007). Association of subjective well-being, symptoms, and side effects with compliance after 12 months of treatment in schizophrenia. Journal of Clinical Psychiatry 68, 7580.Google Scholar
Karow, A, Naber, D (2002). Subjective well-being and quality of life under atypical antipsychotic treatment. Psychopharmacology 162, 310.Google Scholar
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261276.Google Scholar
Keedwell, PA, Andrew, C, Williams, SCR, Brammer, MJ, Phillips, ML (2005). The neural correlates of anhedonia in major depressive disorder. Biological Psychiatry 58, 843853.Google Scholar
Kirsch, P, Schienle, A, Stark, R, Sammer, G, Blecker, C, Walter, B, Ott, U, Burkart, J, Vaitl, D (2003). Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. NeuroImage 20, 10861095.Google Scholar
Knutson, B, Adams, CM, Fong, GW, Hommer, D (2001). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience 21, 159.Google Scholar
Knutson, B, Bhanji, JP, Cooney, RE, Atlas, LY, Gotlib, IH (2008). Neural responses to monetary incentives in major depression. Biological Psychiatry 63, 686692.Google Scholar
Knutson, B, Gibbs, SEB (2007). Linking nucleus accumbens dopamine and blood oxygenation. Psychopharmacology 191, 812822.CrossRefGoogle ScholarPubMed
Lambert, M, Naber, D (2004). Current issues in schizophrenia: overview of patient acceptability, functioning capacity and quality of life. CNS Drugs 18 (Suppl. 2), 517.Google Scholar
Larisch, R, Klimke, A, Vosberg, H, Loffler, S, Gaebel, W, Muller-Gartner, HW (1997). In vivo evidence for the involvement of dopamine-D2 receptors in striatum and anterior cingulate gyrus in major depression. NeuroImage 5 (Pt 1), 251260.Google Scholar
Lataster, J, van Os, J, de Haan, L, Thewissen, B, Bak, M, Lataster, T, Lardinois, M, Delespaul, PA, Myin-Germeys, I (2010). Emotional experience and estimates of D2 receptor occupancy in psychotic patients treated with haloperidol, risperidone, or olanzapine: an experience sampling study. Journal of Clinical Psychiatry 72, 13971404.Google Scholar
Maldjian, JA, Laurienti, PJ, Kraft, RA, Burdette, JH (2003). An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 19, 12331239.Google Scholar
Mawlawi, O, Martinez, D, Slifstein, M, Broft, A, Chatterjee, R, Hwang, DR, Huang, Y, Simpson, N, Ngo, K, Van Heertum, R, Laruelle, M (2001). Imaging human mesolimbic dopamine transmission with positron emission tomography: I. Accuracy and precision of D(2) receptor parameter measurements in ventral striatum. Journal of Cerebral Blood Flow and Metabolism 21, 10341057.Google Scholar
Miller, DD, Andreasen, NC, O'Leary, DS, Rezai, K, Watkins, GL, Ponto, LL, Hichwa, RD (1997). Effect of antipsychotics on regional cerebral blood flow measured with positron emission tomography. Neuropsychopharmacology 17, 230240.Google Scholar
Mizrahi, R, Mamo, D, Rusjan, P, Graff, A, Houle, S, Kapur, S (2009). The relationship between subjective well-being and dopamine D2 receptors in patients treated with a dopamine partial agonist and full antagonist antipsychotics. International Journal of Neuropsychopharmacology 12, 715721.Google Scholar
Mizrahi, R, Rusjan, P, Agid, O, Graff, A, Mamo, DC, Zipursky, RB, Kapur, S (2007). Adverse subjective experience with antipsychotics and its relationship to striatal and extrastriatal D2 receptors: a PET study in schizophrenia. American Journal of Psychiatry 164, 630637.Google Scholar
Naber, D (1995). A self-rating to measure subjective effects of neuroleptic drugs, relationships to objective psychopathology, quality of life, compliance and other clinical variables. International Clinical Psychopharmacology 10 (Suppl. 3), 133138.Google Scholar
Naber, D, Karow, A, Lambert, M (2005). Subjective well-being under the neuroleptic treatment and its relevance for compliance. Acta Psychiatrica Scandinavica. Supplementum 427, 2934.CrossRefGoogle Scholar
Naber, D, Moritz, S, Lambert, M, Pajonk, FG, Holzbach, R, Mass, R, Andresen, B (2001). Improvement of schizophrenic patients’ subjective well-being under atypical antipsychotic drugs. Schizophrenia Research 50, 7988.Google Scholar
Nelson, HE, Willison, JR (1991). The Revised National Adult Reading Test (NART): Test Manual. NFER-Nelson: Windsor.Google Scholar
Ochsner, KN, Kosslyn, SM, Cosgrove, GR, Cassem, EH, Price, BH, Nierenberg, AA, Rauch, SL (2001). Deficits in visual cognition and attention following bilateral anterior cingulotomy. Neuropsychologia 39, 219230.Google Scholar
Quintana, J, Wong, T, Ortiz-Portillo, E, Marder, SR, Mazziotta, JC (2004). Anterior cingulated dysfunction during choice anticipation in schizophrenia. Psychiatry Research 132, 117130.Google Scholar
Schlagenhauf, F, Juckel, G, Koslowski, M, Kahnt, T, Knutson, B, Dembler, T, Kienast, T, Gallinat, J, Wrase, J, Heinz, A (2007). Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine. Psychopharmacology 196, 673684.Google Scholar
Schlagenhauf, F, Sterzer, P, Schmack, K, Ballmaier, M, Rapp, M, Wrase, J, Juckel, G, Gallinat, J, Heinz, A (2009). Reward feedback alterations in unmedicated schizophrenia patients: relevance for delusions. Biological Psychiatry 65, 10321039.Google Scholar
Schott, BH, Minuzzi, L, Krebs, RM, Elmenhorst, D, Lang, M, Winz, OH, Seidenbecher, CI, Coenen, HH, Heinze, HJ, Zilles, K, Düzel, E, Bauer, A (2008). Mesolimbic functional magnetic resonance imaging activations during reward anticipation correlate with reward-related ventral striatal dopamine release. Journal of Neuroscience 28, 1431114319.Google Scholar
Simpson, GM, Angus, JW (1970). A rating scale for extrapyramidal side effects. Acta Psychiatrica Scandinavica. Supplementum 212, 1119.Google Scholar
Voruganti, L, Awad, AG (2004). Neuroleptic dysphoria: towards a new synthesis. Psychopharmacology 171, 121132.Google Scholar
Voruganti, L, Slomka, P, Zabel, P, Costa, G, So, A, Mattar, A, Awad, G (2001). Subjective effects of AMPT-induced dopamine depletion in schizophrenia: correlation between dysphoric responses and striatal D(2) binding ratios on SPECT imaging. Neuropsychopharmacology 25, 642650.CrossRefGoogle ScholarPubMed
Vothknecht, S, Meijer, C, Zwinderman, A, Kikkert, M, Dekker, J, van Beveren, N, Schoevers, R, de Haan, L; for GROUP (Genetic Risk and Outcome of Psychosis) (2012). Psychometric evaluation of the Subjective Well-being Under Neuroleptic Treatment Scale (SWN) in patients with schizophrenia, their relatives and controls. Psychiatry Research 206, 6267.Google Scholar
Williams, ZM, Bush, G, Rauch, SL, Cosgrove, GR, Eskandar, EN (2004). Human anterior cingulated neurons and the integration of monetary reward with motor responses. Nature Neuroscience 7, 13701375.Google Scholar