Disambiguating ventral striatum fMRI-related bold signal during reward prediction in schizophrenia
Open accessAbstract
Reward detection, surprise detection and prediction-error signaling have all been proposed as roles for the ventral striatum (vStr). Previous neuroimaging studies of striatal function in schizophrenia have found attenuated neural responses to reward-related prediction errors; however, as prediction errors represent a discrepancy in mesolimbic neural activity between expected and actual events, it is critical to examine responses to both expected and unexpected rewards (URs) in conjunction with expected and UR omissions in order to clarify the nature of ventral striatal dysfunction in schizophrenia. In the present study, healthy adults and people with schizophrenia were tested with a reward-related prediction-error task during functional magnetic resonance imaging to determine whether schizophrenia is associated with altered neural responses in the vStr to rewards, surprise prediction errors or all three factors. In healthy adults, we found neural responses in the vStr were correlated more specifically with prediction errors than to surprising events or reward stimuli alone. People with schizophrenia did not display the normal differential activation between expected and URs, which was partially due to exaggerated ventral striatal responses to expected rewards (right vStr) but also included blunted responses to unexpected outcomes (left vStr). This finding shows that neural responses, which typically are elicited by surprise, can also occur to well-predicted events in schizophrenia and identifies aberrant activity in the vStr as a key node of dysfunction in the neural circuitry used to differentiate expected and unexpected feedback in schizophrenia.
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Individuals with schizophrenia have reduced activation of the ventral striatum to unexpected reward outcomes, but enhanced responses to expected rewards.
“individuals with schizophrenia have reduced activation of the ventral striatum to unexpected reward outcomes, but have enhanced responses to expected rewards [421].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [421]
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Cites
The Positive and Negative Syndrome Scale (PANSS) for schizophrenia.
Kay, S. R., Fiszbein, A., & Opler, L. A. (1987) · Schizophrenia Bulletin · doi:10.1093/schbul/13.2.261 · Cited by 21,378 · see citing works
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002) · NeuroImage · doi:10.1006/nimg.2001.0978 · Cited by 16,319 · see citing works
A neural substrate of prediction and reward
Schultz, W., Dayan, P., & Montague, P. R. (1997) · Science · doi:10.1126/science.275.5306.1593 · Cited by 9,388 · see citing works
Thresholding of statistical maps in functional neuroimaging using the false discovery rate
Genovese, C. R., Lazar, N. A., & Nichols, T. (2002) · NeuroImage · doi:10.1006/nimg.2001.1037 · Cited by 4,923 · see citing works
Holroyd, C. B., & Coles, M. G. H. (2002) · Psychological Review · doi:10.1037/0033-295x.109.4.679 · Cited by 4,027 · see citing works
Wechsler Adult Intelligence Scale-III
Ryan, J. J., & Lopez, S. J. (2001) · Springer eBooks · doi:10.1007/978-1-4615-1185-4_2 · Cited by 3,680 · see citing works
Anterior Cingulate Cortex, Error Detection, and the Online Monitoring of Performance
Carter, C. S., Braver, T. S., Barch, D. M., Botvinick, M. M., Noll, D., & Cohen, J. D. (1998) · Science · doi:10.1126/science.280.5364.747 · Cited by 3,273 · see citing works
Kapur, S. (2003) · American Journal of Psychiatry · doi:10.1176/appi.ajp.160.1.13 · Cited by 2,813 · see citing works
Chlorpromazine Equivalent Doses for the Newer Atypical Antipsychotics
Woods, S. W. (2003) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.v64n0607 · Cited by 2,056 · see citing works
Temporal difference models and reward-related learning in the human brain
O'Doherty, J. P., Dayan, P., Friston, K., Critchley, H., & Dolan, R. J. (2003) · Neuron · doi:10.1016/s0896-6273(03)00169-7 · Cited by 1,522 · see citing works
Neuronal Coding of Prediction Errors
Schultz, W., & Dickinson, A. (2000) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.23.1.473 · Cited by 1,427 · see citing works
Jeurgen, K., Assheuer, J., & Paxinos, G. (1997) · Medical Entomology and Zoology · Cited by 1,416 · see citing works
The neuropsychology of schizophrenia
Gray, J. A., Feldon, J., Rawlins, J. N. P., Hemsley, D. R., & Smith, A. D. (1991) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00065055 · Cited by 1,350 · see citing works
Controlling the familywise error rate in functional neuroimaging: a comparative review
Nichols, T. E., & Hayasaka, S. (2003) · Statistical Methods in Medical Research · doi:10.1191/0962280203sm341ra · Cited by 1,210 · see citing works
Temporal Prediction Errors in a Passive Learning Task Activate Human Striatum
McClure, S. M., Berns, G. S., & Montague, P. R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00154-5 · Cited by 917 · see citing works
Hare, T. A., O'Doherty, J., Camerer, C. F., Schultz, W., & Rangel, A. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.1309-08.2008 · Cited by 792 · see citing works
Elevated Striatal Dopamine Function Linked to Prodromal Signs of Schizophrenia
Howes, O. D., Montgomery, A. J., Asselin, M.-C., Murray, R. M., Valli, I., Tabraham, P., Bramon-Bosch, E., Valmaggia, L., Johns, L., Broome, M., et al. (2009) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2008.514 · Cited by 744 · see citing works
Leucht, S., Wahlbeck, K., Hamann, J., & Kissling, W. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13306-5 · Cited by 729 · see citing works
Predictability modulates human brain response to reward
Berns, G. S., McClure, S. M., Pagnoni, G., & Montague, P. R. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02793.2001 · Cited by 711 · see citing works
BOLD responses reflecting dopaminergic signals in the human ventral tegmental area
D'Ardenne, K., McClure, S. M., Nystrom, L. E., & Cohen, J. D. (2008) · Science · doi:10.1126/science.1150605 · Cited by 661 · see citing works
Wechsler Test of Adult Reading
(2001) · PsycTESTS Dataset · doi:10.1037/t15180-000 · Cited by 616 · see citing works
The Left Striato-pallidal Hyperactivity Model of Schizophrenia
Early, T. S., Haller, J., Posner, M. I., & Raichle, M. (2019) · Psychology Press eBooks · doi:10.4324/9781315785004-2 · Cited by 598 · see citing works
Dopamine and reward: The anhedonia hypothesis 30 years on
Wise, R. A. (2008) · Neurotoxicity Research · doi:10.1007/bf03033808 · Cited by 580 · see citing works
Dysfunction of ventral striatal reward prediction in schizophrenia
Juckel, G., Schlagenhauf, F., Koslowski, M., Wüstenberg, T., Villringer, A., Knutson, B., Wrase, J., & Heinz, A. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.07.051 · Cited by 578 · see citing works
Increased Synaptic Dopamine Function in Associative Regions of the Striatum in Schizophrenia
Kegeles, L. S., Abi-Dargham, A., Frankle, W. G., Gil, R., Cooper, T. B., Slifstein, M., Hwang, D.-R., Huang, Y., Haber, S. N., & Laruelle, M. (2010) · Archives of General Psychiatry · doi:10.1001/archgenpsychiatry.2010.10 · Cited by 565 · see citing works
Substantia nigra/ventral tegmental reward prediction error disruption in psychosis
Murray, G. K., Corlett, P. R., Clark, L., Pessiglione, M., Blackwell, A. D., Honey, G., Jones, P. B., Bullmore, E. T., Robbins, T. W., & Fletcher, P. C. (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002058 · Cited by 532 · see citing works
Reward Processing in Schizophrenia: A Deficit in the Representation of Value
Gold, J. M., Waltz, J. A., Prentice, K. J., Morris, S. E., & Heerey, E. A. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn068 · Cited by 521 · see citing works
Dorsal anterior cingulate cortex shows fMRI response to internal and external error signals
Holroyd, C. B., Nieuwenhuis, S., Yeung, N., Nystrom, L. E., Mars, R. B., COLES, M. G. H., & Cohen, J. D. (2004) · Nature Neuroscience · doi:10.1038/nn1238 · Cited by 487 · see citing works
Barch, D. M., & Dowd, E. C. (2010) · Schizophrenia Bulletin · doi:10.1093/schbul/sbq068 · Cited by 478 · see citing works
Wechsler Adult Intelligence Scale
Szczepkowski, K. V., & Demakis, G. J. (2017) · Springer eBooks · doi:10.1007/978-3-319-28099-8_1034-1 · Cited by 452 · see citing works
Dialogues on prediction errors
Niv, Y., & Schoenbaum, G. M. (2008) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2008.03.006 · Cited by 355 · see citing works
Waltz, J. A., & Gold, J. M. (2007) · Schizophrenia Research · doi:10.1016/j.schres.2007.03.010 · Cited by 331 · see citing works
Juckel, G., Schlagenhauf, F., Koslowski, M., Filonov, D., Wüstenberg, T., Villringer, A., Knutson, B., Kienast, T., Gallinat, J., Wrase, J., et al. (2006) · Psychopharmacology · doi:10.1007/s00213-006-0405-4 · Cited by 323 · see citing works
Coding of Predicted Reward Omission by Dopamine Neurons in a Conditioned Inhibition Paradigm
Tobler, P. N., Dickinson, A., & Schultz, W. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10402.2003 · Cited by 300 · see citing works
Abolition of latent inhibition by a single 5 mg dose ofd-amphetamine in man
Gray, N. S., Pickering, A. D., Hemsley, D. R., Dawling, S., & Gray, J. A. (1992) · Psychopharmacology · doi:10.1007/bf02245170 · Cited by 261 · see citing works
Testing the Reward Prediction Error Hypothesis with an Axiomatic Model
Rutledge, R. B., Dean, M., Caplin, A., & Glimcher, P. W. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1747-10.2010 · Cited by 244 · see citing works
The formation of abnormal associations in schizophrenia: Neural and behavioral evidence
Jensen, J., Willeit, M., Zipursky, R. B., Savina, I., Smith, A. J., Menon, M., Crawley, A. P., & Kapur, S. (2008) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301437 · Cited by 225 · see citing works
Neural correlates of reward processing in schizophrenia — Relationship to apathy and depression
Simon, J. J., Biller, A., Walther, S., Roesch-Ely, D., Stippich, C., Weisbrod, M., & Kaiser, S. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.11.007 · Cited by 222 · see citing works
Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine
Schlagenhauf, F., Juckel, G., Koslowski, M., Kahnt, T., Knutson, B., Dembler, T., Kienast, T., Gallinat, J., Wrase, J., & Heinz, A. (2008) · Psychopharmacology · doi:10.1007/s00213-007-1016-4 · Cited by 204 · see citing works
Gray, J. A. (1998) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033324 · Cited by 196 · see citing works
Waltz, J. A., Schweitzer, J. B., Gold, J. M., Kurup, P. K., Ross, T. J., Jo Salmeron, B., Rose, E. J., McClure, S. M., & Stein, E. A. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.214 · Cited by 186 · see citing works
Walter, H., Kammerer, H., Frasch, K., Spitzer, M., & Abler, B. (2009) · Psychopharmacology · doi:10.1007/s00213-009-1586-4 · Cited by 127 · see citing works
Ventral–striatal/nucleus–accumbens sensitivity to prediction errors during classification learning
Rodriguez, P. F., Aron, A. R., & Poldrack, R. A. (2006) · Human Brain Mapping · doi:10.1002/hbm.20186 · Cited by 122 · see citing works
Weickert, T. W., Terrazas, A., Bigelow, L. B., Malley, J. D., Hyde, T. M., Egan, M. F., Weinberger, D. R., & Goldberg, T. E. (2002) · Learning & Memory · doi:10.1101/lm.49102 · Cited by 110 · see citing works
Self-citationKoch, K., Schachtzabel, C., Wagner, G., Schikora, J., Schultz, C., Reichenbach, J. R., Sauer, H., & Schlösser, R. G. M. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.12.031 · Cited by 101 · see citing works
The relevance of reward pathways for schizophrenia
Ziauddeen, H., & Murray, G. K. (2010) · Current Opinion in Psychiatry · doi:10.1097/yco.0b013e328336661b · Cited by 83 · see citing works
Neural Correlates of Probabilistic Category Learning in Patients with Schizophrenia
Weickert, T. W., Goldberg, T. E., Callicott, J. H., Chen, Q., Apud, J. A., Das, S., Zoltick, B. J., Egan, M. F., Meeter, M., Myers, C. E., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4341-08.2009 · Cited by 78 · see citing works
Self-citationSerra, A. M., Jones, S. H., Toone, B., & Gray, J. A. (2001) · Schizophrenia Research · doi:10.1016/s0920-9964(00)00141-9 · Cited by 77 · see citing works
Dopamine, prediction error and associative learning: A model-based account
Smith, A. J., Li, M., Becker, S., & Kapur, S. (2006) · Network Computation in Neural Systems · doi:10.1080/09548980500361624 · Cited by 73 · see citing works
Opioid Receptors in the Nucleus Accumbens Regulate Attentional Learning in the Blocking Paradigm
Iordanova, M. D., McNally, G. P., & Westbrook, R. F. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4679-05.2006 · Cited by 63 · see citing works
Dopaminergic Modulation of Appetitive and Aversive Predictive Learning
Iordanova, M. D. (2009) · Reviews in the Neurosciences · doi:10.1515/revneuro.2009.20.5-6.383 · Cited by 50 · see citing works
Sensitivity of the nucleus accumbens to violations in expectation of reward
Spicer, J., Galván, A., Hare, T. A., Voss, H. U., Glover, G. H., & Casey, B. J. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.09.012 · Cited by 50 · see citing works
Molina, V., Hernandez-Tamames, J. A., Sanz, J., Paniagua, J. C., Hernández, A. I., Martín, C., Matías, J., Calama, J., & Bonaechea, B. B. (2010) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2010.06.006 · Cited by 38 · see citing works
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Fornito, A., Harrison, B. J., Goodby, E., Dean, A., Ooi, C., Nathan, P. J., Lennox, B. R., Jones, P. B., Suckling, J., & Bullmore, E. T. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.1976 · Cited by 279 · see citing works
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- Authors
- Morris, R. W., Vercammen, A., Lenroot, R., Moore, L., Langton, J. M., Short, B., Kulkarni, J., Curtis, J., O'Donnell, M., Weickert, C. S., & Weickert, T. W.
- Affiliations
- Schizophrenia Research Institute (AU)
- UNSW Sydney (AU)
- Monash Alfred Psychiatry Research centre (AU)
- Prince of Wales Hospital (AU)
- Corresponding author
- Morris, R W
- ORCID
- Venue
- Molecular Psychiatry
- Published
- 2011-06-28
- Volume
- 17
- Issue
- 3
- Pages
- 280-289
- ISSN
- 1359-4184 (ISSN-L)
- 1476-5578
- PMC
- PMC3284694
- OpenAlex
- W2073806182
- Cited by
- 149
- References
- 53
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 4 · 2023: 4 · 2022: 7 · 2021: 8 · 2020: 8 · 2019: 8 · 2018: 11 · 2017: 11 · 2016: 20 · 2015: 23 · 2014: 21 · 2013: 11 · 2012: 6
- FWCI
- 8.81
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- www.springer.com/tdm (unspecified)
- Locations
- Molecular Psychiatry (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- Research Bank (Australian Catholic University) (submittedVersion)
- Funders
- Pratt Foundation
- Neuroscience Research Australia
- University of New South Wales
- Ramsay Health Care
- Australian Schizophrenia Research Bank
- Medical Research Council
- National Health and Medical Research Council (568807)
- Topics
- Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- ventral striatum, schizophrenia, prediction error, reward prediction, surprise, expected reward, BOLD signal
- MeSH terms
- Adult, Basal Ganglia, Brain Mapping, Female, Forecasting, Games, Experimental, Humans, Magnetic Resonance Imaging, Male, Models, Psychological, Psychotic Disorders, Reward, Schizophrenia, Schizophrenic Psychology
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