Reduction in ventral striatal activity when anticipating a reward in depression and schizophrenia: A replicated cross-diagnostic finding

Frontiers in Psychology

Volumn 6, Issue , 2015, Pages

  Arrondo, Gonzalo ^a   Segarra, Nuria ^a   Metastasio, Antonio ^a   Ziauddeen, Hisham ^a,b,c   Spencer, Jennifer ^a,c   Reinders, Niels R ^a   Dudas, Robert B ^a,c,d   Robbins, Trevor W ^a,e   Fletcher, Paul C ^a,b,c,e   Murray, Graham K ^a,c,e  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INSTITUTE OF METABOLIC SCIENCE   (United Kingdom)

^c CAMBRIDGESHIRE AND PETERBOROUGH NHS FOUNDATION TRUST   (United Kingdom)

^d IPSWICH HOSPITAL   (United Kingdom)

^e UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Depressive symptoms; Monetary incentive delay; Research domain framework; Reward system; Ventral striatum

Indexed keywords

EID: 85016243500     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2015.01280     Document Type: Article

References (64)

1. American Psychiatric Association. (2000). Diagnostic and Statistical Manual of Mental Disorders. Washington, DC: American Psychiatric Association.
2. Argyropoulos, S. V., and Nutt, D. J. (2013). Anhedonia revisited: is there a role for dopamine-targeting drugs for depression? J. Psychopharmacol. 27, 869-877. doi: 10.1177/0269881113494104
3. Arrondo, G., Murray, G. K., Hill, E., Szalma, B., Yathiraj, K., Denman, C., et al. (2015). Hedonic and disgust taste perception in borderline personality disorder and depression. Br. J. Psychiatry 207, 79-80. doi: 10.1192/bjp.bp.114.150433
4. Barch, D. M., and Dowd, E. C. (2010). Goal representations and motivational drive in schizophrenia: the role of prefrontal-striatal interactions. Schizophr. Bull. 36, 919-934. doi: 10.1093/schbul/sbq068
5. Barch, D. M., Treadway, M. T., and Schoen, N. (2014). Effort, anhedonia, and function in schizophrenia: reduced effort allocation predicts amotivation and functional impairment. J. Abnorm. Psychol. 123, 387-397. doi: 10.1037/a0036299
6. Beck, A. T., Steer, R. A., Ball, R., and Ranieri, W. (1996). Comparison of Beck Depression Inventories -IA and -II in psychiatric outpatients. J. Pers. Assess. 67, 588-597. doi: 10.1207/s15327752jpa6703_13
7. Bedwell, J. S., Gooding, D. C., Chan, C. C., and Trachik, B. J. (2014). Anhedonia in the age of RDoC. Schizophr. Res. 160, 226-227. doi: 10.1016/j.schres.2014.10.028
8. Bernacer, J., Corlett, P. R., Ramachandra, P., McFarlane, B., Turner, D. C., Clark, L., et al. (2013). Methamphetamine-induced disruption of frontostriatal reward learning signals: relation to psychotic symptoms. Am. J. Psychiatry 170, 1326-1334. doi: 10.1176/appi.ajp.2013.12070978
9. Berns, G. S., McClure, S. M., Pagnoni, G., and Montague, P. R. (2001). Predictability modulates human brain response to reward. J. Neurosci. 21, 2793-2798.
10. Berrios, G. E. (1996). The History of Mental Symptoms. Cambridge: Cambridge University Press.
11. Cattell, R. B., Krug, S. E., and Barton, K. (1973). Technical Supplement for the Culture Fair Intelligence Tests, Scales 2 and 3. Champaign, IL: Institute for Personality and Ability Testing.
12. Cohen, A. S., and Minor, K. S. (2010). Emotional experience in patients with schizophrenia revisited: meta-analysis of laboratory studies. Schizophr. Bull. 36, 143-150. doi: 10.1093/schbul/sbn061
13. Cools, R., Blackwell, A., Clark, L., Menzies, L., Cox, S., and Robbins, T. W. (2005). Tryptophan depletion disrupts the motivational guidance of goaldirected behavior as a function of trait impulsivity. Neuropsychopharmacology 30, 1362-1373. doi: 10.1038/sj.npp.1300704
14. Crespi, L. P. (1942). Quantitative variation of incentive and performance in the white rat. Am. J. Psychol. 55, 467-517. doi: 10.2307/1417120
15. Cuthbert, B. N. (2014a). The RDoC framework: facilitating transition from ICD/DSM to dimensional approaches that integrate neuroscience and psychopathology. World Psychiatry 13, 28-35. doi: 10.1002/wps. 20087
16. Cuthbert, B. N. (2014b). Translating intermediate phenotypes to psychopathology: the NIMH research domain criteria. Psychophysiology 51, 1205-1206. doi: 10.1111/psyp.12342
17. Der-Avakian, A., and Markou, A. (2012). The neurobiology of anhedonia and other reward-related deficits. Trends Neurosci. 35, 68-77. doi: 10.1016/j.tins.2011.11.005
18. Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., et al. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31, 968-980. doi: 10.1016/j.neuroimage.2006.01.021
19. Fletcher, P. C., and Frith, C. D. (2009). Perceiving is believing: a Bayesian approach to explaining the positive symptoms of schizophrenia. Nat. Rev. Neurosci. 10, 48-58. doi: 10.1038/nrn2536
20. Gard, D. E., Gard, M. G., Kring, A. M., and John, O. P. (2006). Anticipatory and consummatory components of the experience of pleasure: a scale development study. J. Res. Pers. 40, 1086-1102. doi: 10.1016/j.jrp.2005.11.001
21. Gard, D. E., Sanchez, A. H., Cooper, K., Fisher, M., Garrett, C., and Vinogradov, S. (2014). Do people with schizophrenia have difficulty anticipating pleasure, engaging in effortful behavior, or both? J. Abnorm. Psychol. 123, 771-782. doi: 10.1037/abn0000005
22. Gradin, V. B., Kumar, P., Waiter, G., Ahearn, T., Stickle, C., Milders, M., et al. (2011). Expected value and prediction error abnormalities in depression and schizophrenia. Brain 134, 1751-1764. doi: 10.1093/brain/awr059
23. Hägele, C., Schlagenhauf, F., Rapp, M., Sterzer, P., Beck, A., Bermpohl, F., et al. (2015). Dimensional psychiatry: reward dysfunction and depressive mood across psychiatric disorders. Psychopharmacology (Berl). 232, 331-341. doi: 10.1007/s00213-014-3662-7
24. Hui, C., Morcillo, C., Russo, D. A., Stochl, J., Shelley, G. F., Painter, M., et al. (2013). Psychiatric morbidity, functioning and quality of life in young people at clinical high risk for psychosis. Schizophr. Res. 148, 175-180. doi: 10.1016/j.schres.2013.05.026
25. Insel, T., Cuthbert, B., Garvey, M., Heinssen, R., Pine, D. S., Quinn, K., et al. (2010). Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatry 167, 748-751. doi: 10.1176/appi.ajp.2010.09091379
26. Juckel, G., Schlagenhauf, F., Koslowski, M., Filonov, D., Wustenberg, T., Villringer, A., et al. (2006a). Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology (Berl). 187, 222-228. doi: 10.1007/s00213-006-0405-4
27. Juckel, G., Schlagenhauf, F., Koslowski, M., Wüstenberg, T., Villringer, A., Knutson, B., et al. (2006b). Dysfunction of ventral striatal reward prediction in schizophrenia. Neuroimage 29, 409-416. doi: 10.1016/j.neuroimage.2005.07.051
28. Kay, S. R., Fiszbein, A., and Opler, L. A. (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 13, 261-276. doi: 10.1093/schbul/13.2.261
29. Kirsch, P., Schienle, A., Stark, R., Sammer, G., Blecker, C., Walter, B., et al. (2003). Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study. Neuroimage 20, 1086-1095. doi: 10.1016/S1053-8119(03)00381-1
30. Knutson, B., Bhanji, J. P., Cooney, R. E., Atlas, L. Y., and Gotlib, I. H. (2008). Neural responses to monetary incentives in major depression. Biol. Psychiatry 63, 686-692. doi: 10.1016/j.biopsych.2007.07.023
31. Knutson, B., Fong, G. W., Adams, C. M., Varner, J. L., and Hommer, D. (2001). Dissociation of reward anticipation and outcome with eventrelated fMRI. Neuroreport 12, 3683-3687. doi: 10.1097/00001756-200112040- 00016
32. Kring, A. M., and Barch, D. M. (2014). The motivation and pleasure dimension of negative symptoms: neural substrates and behavioral outputs. Eur. Neuropsychopharmacol. 24, 725-736. doi: 10.1016/j.euroneuro.2013. 06.007
33. Kring, A. M., and Caponigro, J. M. (2010). Emotion in schizophrenia: where feeling meets thinking. Curr. Dir. Psychol. Sci. 19, 255-259. doi: 10.1177/0963721410377599
34. Kroken, R. A., Johnsen, E., Ruud, T., Wentzel-Larsen, T., and Jørgensen, H. A. (2009). Treatment of schizophrenia with antipsychotics in Norwegian emergency wards, a cross-sectional national study. BMC Psychiatry 9:24. doi: 10.1186/1471-244X-9-24
35. Kumar, P., Waiter, G., Ahearn, T., Milders, M., Reid, I., and Steele, J. D. (2008). Abnormal temporal difference reward-learning signals in major depression. Brain 131, 2084-2093. doi: 10.1093/brain/awn136
36. Lilienfeld, S. O. (2014). The Research Domain Criteria (RDoC): an analysis of methodological and conceptual challenges. Behav. Res. Ther. 62, 129-139. doi: 10.1016/j.brat.2014.07.019
37. Murray, G. K., Clark, L., Corlett, P. R., Blackwell, A. D., Cools, R., Jones, P. B., et al. (2008a). Incentive motivation in first-episode psychosis: a behavioural study. BMC Psychiatry 8:34. doi: 10.1186/1471-244X-8-34
38. Murray, G. K., Corlett, P. R., Clark, L., Pessiglione, M., Blackwell, A. D., Honey, G., et al. (2008b). Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry 13, 239, 267-276. doi: 10.1038/sj.mp.4002058
39. Murray, G. K., and Jones, P. B. (2012). Psychotic symptoms in young people without psychotic illness: mechanisms and meaning. Br. J. Psychiatry 201, 4-6. doi: 10.1192/bjp.bp.111.107789
40. Myerson, A. (1922). Anhedonia. Am. J. Psychiatry 79, 87-103. doi: 10.1176/ajp.79.1.87
41. Nielsen, M. ø., Rostrup, E., Wulff, S., Bak, N., Lublin, H., Kapur, S., et al. (2012). Alterations of the brain reward system in antipsychotic naive schizophrenia patients. Biol. Psychiatry 71, 898-905. doi: 10.1016/j.biopsych.2012.02.007
42. O'doherty, J., Dayan, P., Schultz, J., Deichmann, R., Friston, K., and Dolan, R. J. (2004). Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452-454. doi: 10.1126/science.1094285
43. Overall, J. E., and Gorham, D. R. (1962). The brief psychiatric rating scale. Psychol. Rep. 10, 799-812. doi: 10.2466/pr0.1962.10.3.799
44. Pessiglione, M., Seymour, B., Flandin, G., Dolan, R. J., and Frith, C. D. (2006). Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 442, 1042-1045. doi: 10.1038/nature05051
45. Pizzagalli, D. A., Holmes, A. J., Dillon, D. G., Goetz, E. L., Birk, J. L., Bogdan, R., et al. (2009). Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. Am. J. Psychiatry 166, 702-710. doi: 10.1176/appi.ajp.2008.08081201
46. Rømer Thomsen, K., Whybrow, P. C., and Kringelbach, M. L. (2015). Reconceptualizing anhedonia: novel perspectives on balancing the pleasure networks in the human brain. Front. Behav. Neurosci. 9:49. doi: 10.3389/fnbeh.2015.00049
47. Schlagenhauf, F., Juckel, G., Koslowski, M., Kahnt, T., Knutson, B., Dembler, T., et al. (2008). Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine. Psychopharmacology (Berl). 196, 673-684. doi: 10.1007/s00213-007-1016-4
48. Sescousse, G., Caldú, X., Segura, B., and Dreher, J. C. (2013). Processing of primary and secondary rewards: a quantitative meta-analysis and review of human functional neuroimaging studies. Neurosci. Biobehav. Rev. 37, 681-696. doi: 10.1016/j.neubiorev.2013.02.002
49. Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., et al. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J. Clin. Psychiatry 59(Suppl. 20), 22-33; quiz: 34-57.
50. Sherdell, L., Waugh, C. E., and Gotlib, I. H. (2012). Anticipatory pleasure predicts motivation for reward in major depression. J. Abnorm. Psychol. 121, 51-60. doi: 10.1037/a0024945
51. Simon, J. J., Biller, A., Walther, S., Roesch-Ely, D., Stippich, C., Weisbrod, M., et al. (2010). Neural correlates of reward processing in schizophrenia- relationship to apathy and depression. Schizophr. Res. 118, 154-161. doi: 10.1016/j.schres.2009.11.007
52. Smoski, M. J., Felder, J., Bizzell, J., Green, S. R., Ernst, M., Lynch, T. R., et al. (2009). fMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. J. Affect. Disord. 118, 69-78. doi: 10.1016/j.jad.2009.01.034
53. Snaith, R. P., Hamilton, M., Morley, S., Humayan, A., Hargreaves, D., and Trigwell, P. (1995). A scale for the assessment of hedonic tone the Snaith- Hamilton Pleasure Scale. Br. J. Psychiatry 167, 99-103. doi: 10.1192/bjp. 167.1.99
54. Stoy, M., Schlagenhauf, F., Sterzer, P., Bermpohl, F., Hägele, C., Suchotzki, K., et al. (2012). Hyporeactivity of ventral striatum towards incentive stimuli in unmedicated depressed patients normalizes after treatment with escitalopram. J. Psychopharmacol. 26, 677-688. doi: 10.1177/0269881111416686
55. Treadway, M. T., Bossaller, N. A., Shelton, R. C., and Zald, D. H. (2012). Effort-based decision-making in major depressive disorder: a translational model of motivational anhedonia. J. Abnorm. Psychol. 121, 553-558. doi: 10.1037/a0028813
56. Treadway, M. T., and Zald, D. H. (2011). Reconsidering anhedonia in depression: lessons from translational neuroscience. Neurosci. Biobehav. Rev. 35, 537-555. doi: 10.1016/j.neubiorev.2010.06.006
57. Walter, H., Kammerer, H., Frasch, K., Spitzer, M., and Abler, B. (2009). Altered reward functions in patients on atypical antipsychotic medication in line with the revised dopamine hypothesis of schizophrenia. Psychopharmacology (Berl). 206, 121-132. doi: 10.1007/s00213-009-1586-4
58. Waltz, J. A., Schweitzer, J. B., Gold, J. M., Kurup, P. K., Ross, T. J., Salmeron, B. J., et al. (2009). Patients with schizophrenia have a reduced neural response to both unpredictable and predictable primary reinforcers. Neuropsychopharmacology 34, 1567-1577. doi: 10.1038/npp.2008.214
59. Waltz, J. A., Schweitzer, J. B., Ross, T. J., Kurup, P. K., Salmeron, B. J., Rose, E. J., et al. (2010). Abnormal responses to monetary outcomes in cortex, but not in the basal ganglia, in schizophrenia. Neuropsychopharmacology 35, 2427-2439. doi: 10.1038/npp.2010.126
60. Weinberger, D. R., and Goldberg, T. E. (2014). RDoCs redux. World Psychiatry 13, 36-38. doi: 10.1002/wps.20096
61. Whitton, A. E., Treadway, M. T., and Pizzagalli, D. A. (2015). Reward processing dysfunction in major depression, bipolar disorder and schizophrenia. Curr. Opin. Psychiatry 28, 7-12. doi: 10.1097/YCO.0000000000000122
62. Woo, C. W., Krishnan, A., and Wager, T. D. (2014). Cluster-extent based thresholding in fMRI analyses: pitfalls and recommendations. Neuroimage 91, 412-419. doi: 10.1016/j.neuroimage.2013.12.058
63. Zhang, W. N., Chang, S. H., Guo, L. Y., Zhang, K. L., and Wang, J. (2013). The neural correlates of reward-related processing in major depressive disorder: a meta-analysis of functional magnetic resonance imaging studies. J. Affect. Disord. 151, 531-539. doi: 10.1016/j.jad.2013.06.039
64. Ziauddeen, H., and Murray, G. K. (2010). The relevance of reward pathways for schizophrenia. Curr. Opin. Psychiatry 23, 91-96. doi: 10.1097/YCO.0b013e328336661b