Reward processing in depression: A conceptual and meta-analytic review across fMRI and EEG studies

American Journal of Psychiatry

Volumn 175, Issue 11, 2018, Pages 1111-1120

  Keren, Hanna ^a   O'Callaghan, Georgia ^a   Vidal Ribas, Pablo ^a   Buzzell, George A ^a   Brotman, Melissa A ^a   Leibenluft, Ellen ^a   Pan, Pedro M ^a   Meffert, Liana ^a   Kaiser, Ariela ^a   Wolke, Selina ^a   Pine, Daniel S ^a   Stringaris, Argyris ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEHAVIOR; CORPUS STRIATUM; DEPRESSION; ELECTROENCEPHALOGRAM; EVENT RELATED POTENTIAL; FEEDBACK SYSTEM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; PATHOGENESIS; PRIORITY JOURNAL; REWARD; TASK PERFORMANCE; ELECTROENCEPHALOGRAPHY; META ANALYSIS; NUCLEAR MAGNETIC RESONANCE IMAGING; PSYCHOLOGICAL FEEDBACK; PSYCHOLOGY;

DEPRESSION; ELECTROENCEPHALOGRAPHY; FEEDBACK, PSYCHOLOGICAL; HUMANS; MAGNETIC RESONANCE IMAGING; REWARD;

EID: 85056342442     PISSN: 0002953X     EISSN: 15357228     Source Type: Journal    
DOI: 10.1176/appi.ajp.2018.17101124     Document Type: Article

References (110)

1. Kessler RC, Bromet EJ: The epidemiology of depression across cultures. Annu Rev Public Health 2013; 34: 119-138
2. World Health Organization: Depression: A Global Crisis. Geneva, World Health Organization, 2012
3. Treadway MT, Zald DH: Reconsidering anhedonia in depression: lessons from translational neuroscience. Neurosci Biobehav Rev 2011; 35: 537-555
4. Whitton AE, Treadway MT, Pizzagalli DA: Reward processing dysfunction in major depression, bipolar disorder, and schizophrenia. Curr Opin Psychiatry 2015; 28: 7-12
5. Insel T, Cuthbert B, Garvey M, et al: Research Domain Criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatry 2010; 167: 748-751
6. Zhang WN, Chang SH, Guo LY, et al: The neural correlates of reward-related processing in major depressive disorder: a meta-analysis of functional magnetic resonance imaging studies. J Affect Disord 2013; 151: 531-539
7. Hamilton JP, Etkin A, Furman DJ, et al: Functional neuroimaging of major depressive disorder: a meta-analysis and new integration of baseline activation and neural response data. Am J Psychiatry 2012; 169: 693-703
8. Huys QJ, Pizzagalli DA, Bogdan R, et al: Mapping anhedonia onto reinforcement learning: a behavioural meta-analysis. Biol Mood Anxiety Disord 2013; 3: 12
9. Miller CH, Hamilton JP, Sacchet MD, et al: Meta-analysis of functional neuroimaging of major depressive disorder in youth. JAMA Psychiatry 2015; 72: 1045-1053
10. Müller VI, Cieslik EC, Serbanescu I, et al: Altered brain activity in unipolar depression revisited: meta-analyses of neuroimaging studies. JAMA Psychiatry 2017; 74: 47-55
11. Proudfit GH: The reward positivity: from basic research on reward to a biomarker for depression. Psychophysiology 2015; 52: 449-459
12. Hajcak G, Moser JS, Holroyd CB, et al: It's worse than you thought: the feedback negativity and violations of reward prediction in gambling tasks. Psychophysiology 2007; 44: 905-912
13. Bress JN, Meyer A, Proudfit GH: The stability of the feedback negativity and its relationship with depression during childhood and adolescence. Dev Psychopathol 2015; 27: 1285-1294
14. Braams BR, van Duijvenvoorde AC, Peper JS, et al: Longitudinal changes in adolescent risk-taking: a comprehensive study of neural responses to rewards, pubertal development, and risk-taking behavior. J Neurosci 2015; 35: 7226-7238
15. Luking KR, Pagliaccio D, Luby JL, et al: Reward processing and risk for depression across development. Trends Cogn Sci 2016; 20: 456-468
16. Kendler KS: The phenomenology of major depression and the representativeness and nature of DSM criteria. Am J Psychiatry 2016; 173: 771-780
17. Berrios GE: The History of Mental Symptoms: Descriptive Psychopathology Since the Nineteenth Century. Cambridge, UK, Cambridge University Press, 1996
18. Kessel EM, Klein DN: Depressivity and anhedonia, in The Dark Side of Personality: Science and Practice in Social, Personality, and Clinical Psychology. Edited by Ziegler-Hill V, Marcus DK. Washington, DC, American Psychological Association, 2016
19. Schultz W: Dopamine reward prediction-error signalling: a two-component response. Nat Rev Neurosci 2016; 17: 183-195
20. Admon R, Pizzagalli DA: Dysfunctional reward processing in depression. Curr Opin Psychol 2015; 4: 114-118
21. Kring AM, Barch DM. The motivation and pleasure dimension of negative symptoms: neural substrates and behavioral outputs. European neuropsychopharmacology: the journal of the European College of Neuropsychopharmacology. 2014; 24: 725-736
22. Rizvi SJ, Pizzagalli DA, Sproule BA, et al: Assessing anhedonia in depression: potentials and pitfalls. Neurosci Biobehav Rev 2016; 65: 21-35
23. Knutson B, Westdorp A, Kaiser E, et al: fMRI visualization of brain activity during a monetary incentive delay task. Neuroimage 2000; 12: 20-27
24. Kendler KS: The genealogy of major depression: symptoms and signs of melancholia from 1880 to 1900. Mol Psychiatry 2017; 22: 1539-1553
25. Beesdo K, Höfler M, Leibenluft E, et al: Mood episodes and mood disorders: patterns of incidence and conversion in the first three decades of life. Bipolar Disord 2009; 11: 637-649
26. Richards JM, Plate RC, Ernst M: A systematic review of fMRI reward paradigms in adolescents versus adults: the impact of task design and implications for understanding neurodevelopment. Neurosci Biobehav Rev 2013; 37: 976-991
27. Corfield EC, Yang Y, Martin NG, et al: A continuum of genetic liability for minor and major depression. Transl Psychiatry 2017; 7: e1131
28. Turkeltaub PE, Eden GF, Jones KM, et al: Meta-analysis of the functional neuroanatomy of single-word reading: method and validation. Neuroimage 2002; 16: 765-780
29. Laird AR, Fox PM, Price CJ, et al: ALE meta-analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp 2005; 25: 155-164
30. Bartra O, McGuire JT, Kable JW: The valuation system: a coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. Neuroimage 2013; 76: 412-427
31. Stoy M, Schlagenhauf F, Sterzer P, et al: Hyporeactivity of ventral striatum towards incentive stimuli in unmedicated depressed patients normalizes after treatment with escitalopram. J Psychopharmacol 2012; 26: 677-688
32. Admon R, Nickerson LD, Dillon DG, et al: Dissociable corticostriatal connectivity abnormalities in major depression in response to monetary gains and penalties. Psychol Med 2015; 45: 121-131
33. Stringaris A, Vidal-Ribas Belil P, Artiges E, et al: The brain's response to reward anticipation and depression in adolescence: dimensionality, specificity, and longitudinal predictions in a community-based sample. Am J Psychiatry 2015; 172: 1215-1223
34. Mori A, Okamoto Y, Okada G, et al: Behavioral activation can normalize neural hypoactivation in subthreshold depression during a monetary incentive delay task. J Affect Disord 2016; 189: 254-262
35. Satterthwaite TD, Kable JW, Vandekar L, et al: Common and dissociable dysfunction of the reward system in bipolar and unipolar depression. Neuropsychopharmacology 2015; 40: 2258-2268
36. Hägele C, Schlagenhauf F, Rapp M, et al: Dimensional psychiatry: reward dysfunction and depressive mood across psychiatric disorders. Psychopharmacology (Berl) 2015; 232: 331-341
37. Arrondo G, Segarra N, Metastasio A, et al: Reduction in ventral striatal activity when anticipating a reward in depression and schizophrenia: a replicated cross-diagnostic finding. Front Psychol 2015; 6: 1280
38. Casement MD, Keenan KE, Hipwell AE, et al: Neural reward processing mediates the relationship between insomnia symptoms and depression in adolescence. Sleep 2016; 39: 439-447
39. Chan RC, Li Z, Li K, et al: Distinct processing ofsocial and monetary rewards in late adolescents with trait anhedonia. Neuropsychology 2016; 30: 274-280
40. Chandrasekhar Pammi VS, Pillai Geethabhavan Rajesh P, Kesavadas C, et al: Neural loss aversion differences between depression patients and healthy individuals: a functional MRI investigation. Neuroradiol J 2015; 28: 97-105
41. Chung YS, Barch D: Anhedonia is associated with reduced incentive cue related activation in the basal ganglia. Cogn Affect Behav Neurosci 2015; 15: 749-767
42. Dichter GS, Kozink RV, McClernon FJ, et al: Remitted major depression is characterized by reward network hyperactivation during reward anticipation and hypoactivation during reward outcomes. J Affect Disord 2012; 136: 1126-1134
43. Dillon DG, Dobbins IG, Pizzagalli DA: Weakrewardsource memory in depression reflects blunted activation of VTA/SN and parahippocampus. Soc Cogn Affect Neurosci 2014; 9: 1576-1583
44. Felder JN, Smoski MJ, Kozink RV, et al: Neural mechanisms of subclinical depressive symptoms in women: a pilot functional brain imaging study. BMC psychiatry 2012; 12: 152
45. Forbes E, Hariri A, Martin S, et al: Altered striatal activation predicting real-world positive affect in adolescent major depressive disorder. Am J Psychiatry 2009; 166: 64-73
46. Forbes EE, Ryan ND, Phillips ML, et al: Healthy adolescents' neural response to reward: associations with puberty, positive affect, and depressive symptoms. J Am Acad Child Adolesc Psychiatry 2010; 49: 162-172e5
47. Gorka SM, Huggins AA, Fitzgerald DA, et al: Neural response to reward anticipation in those with depression with and without panic disorder. J Affect Disord 2014; 164: 50-56
48. Gotlib IH, Hamilton JP, Cooney RE, et al: Neural processing of reward and loss in girls at risk for major depression. Arch Gen Psychiatry 2010; 67: 380-387
49. Gradin VB, Kumar P, Waiter G, et al: Expected value and prediction error abnormalities in depression and schizophrenia. Brain 2011; 134: 1751-1764
50. Johnston BA, Tolomeo S, Gradin V, et al: Failure of hippocampal deactivation during loss events in treatment-resistant depression. Brain 2015; 138: 2766-2776
51. Knutson B, Bhanji JP, Cooney RE, et al: Neural responses to monetary incentives in major depression. Biol Psychiatry 2008; 63: 686-692
52. Luking KR, Pagliaccio D, Luby JL, et al: Depression risk predicts blunted neural responsesto gains and enhanced responses to losses in healthy children. J Am Acad Child Adolesc Psychiatry 2016; 55: 328-337
53. Olino TM, McMakin DL, Dahl RE, et al: "I won, but I'm not getting my hopes up": depression moderates the relationship of outcomes and reward anticipation. Psychiatry Res 2011; 194: 393-395
54. Olino TM, McMakin DL, Morgan JK, et al: Reduced reward anticipation in youth at high-risk for unipolar depression: a preliminary study. Dev Cogn Neurosci 2014; 8: 55-64
55. Pizzagalli DA, Holmes AJ, Dillon DG, et al: Reduced caudate and nucleus accumbens response to rewards in unmedicated individuals with major depressive disorder. Am J Psychiatry 2009; 166: 702-710
56. Redlich R, Dohm K, Grotegerd D, et al: Reward processing in unipolar and bipolar depression: a functional MRI study. Neuropsychopharmacology 2015; 40: 2623-2631
57. Remijnse PL, Nielen MM, van Balkom AJ, et al: Differential frontalstriatal and paralimbic activity during reversal learning in major depressive disorder and obsessive-compulsive disorder. Psychol Med 2009; 39: 1503-1518
58. Robinson OJ, Cools R, Carlisi CO, et al: Ventral striatum response during reward and punishment reversal learning in unmedicated major depressive disorder. Am J Psychiatry 2012; 169: 152-159
59. Rzepa E, Fisk J, McCabe C: Blunted neural response to anticipation, effort, and consummation of reward and aversion in adolescents with depression symptomatology. J Psychopharmacol 2017; 31: 303-311
60. Schiller CE, Minkel J, Smoski MJ, et al: Remitted major depression is characterized by reduced prefrontal cortex reactivity to reward loss. J Affect Disord 2013; 151: 756-762
61. Segarra N, Metastasio A, Ziauddeen H, et al: Abnormal fronto striatal activity during unexpected reward receipt in depression and schizophrenia: relationship to anhedonia. Neuropsychopharmacology 2016; 41: 2001-2010
62. Sharp C, Kim S, Herman L, et al: Major depression in mothers predicts reduced ventral striatum activation in adolescent female offspring with and without depression. J Abnorm Psychol 2014; 123: 298-309
63. Smoski MJ, Felder J, Bizzell J, et al: fMRI of alterations in reward selection, anticipation, and feedback in major depressive disorder. J Affect Disord 2009; 118: 69-78
64. Smoski MJ, Rittenberg A, Dichter GS: Major depressive disorder is characterized by greater reward network activation to monetary than pleasant image rewards. Psychiatry Res 2011; 194: 263-270
65. Steele JD, Kumar P, Ebmeier KP: Blunted response to feedback information in depressive illness. Brain 2007; 130: 2367-2374
66. Ubl B, Kuehner C, Kirsch P, et al: Altered neural reward and loss processing and prediction error signalling in depression. Soc Cogn Affect Neurosci 2015; 10: 1102-1112
67. Ubl B, Kuehner C, Kirsch P, et al: Neural reward processing in individuals remitted from major depression. Psychol Med 2015; 45: 3549-3558
68. Yang XH, Huang J, Lan Y, et al: Diminished caudate and superior temporal gyrus responses to effort-based decision making in patients with first-episode major depressive disorder. Prog Neuropsychopharmacol Biol Psychiatry 2016; 64: 52-59
69. Nelson BD, Perlman G, Klein DN, et al: Blunted neural response to rewards as a prospective predictor of the development of depression in adolescent girls. Am J Psychiatry 2016; 173: 1223-1230
70. Bress JN, Smith E, Foti D, et al: Neural response to reward and depressive symptoms in late childhood to early adolescence. Biol Psychol 2012; 89: 156-162
71. Bress JN, Foti D, Kotov R, et al: Blunted neural response to rewards prospectively predicts depression in adolescent girls. Psychophysiology 2013; 50: 74-81
72. Webb CA, Auerbach RP, Bondy E, et al: Abnormal neural responses to feedback in depressed adolescents. J Abnorm Psychol 2017; 126: 19-31
73. Padrão G, Mallorquí A, Cucurell D, et al: Neurophysiological differences in reward processing in anhedonics. Cogn Affect Behav Neurosci 2013; 13: 102-115
74. Liu WH, Wang LZ, Shang HR, et al: The influence of anhedonia on feedback negativity in major depressive disorder. Neuropsychologia 2014; 53: 213-220
75. Foti D, Carlson JM, Sauder CL, et al: Reward dysfunction in major depression: multimodal neuroimaging evidence for refining the melancholic phenotype. Neuroimage 2014; 101: 50-58
76. Weinberg A, Shankman SA: Blunted reward processing in remitted melancholic depression. Clin Psychol Sci 2017; 5: 14-25
77. Mueller EM, Panitz C, Pizzagalli DA, et al: Midline theta dissociates agentic extraversion and anhedonic depression. Pers Individ Diff 2015; 79: 172-177
78. Bress JN, Meyer A, Hajcak G: Differentiating anxiety and depression in children and adolescents: evidence from event-related brain potentials. J Clin Child Adolesc Psychol 2015; 44: 238-249
79. Ait Oumeziane B, Foti D: Reward-related neural dysfunction across depression and impulsivity: a dimensional approach. Psychophysiology 2016; 53: 1174-1184
80. Borenstein M, Hedges LV, Higgins JPT, et al: Introduction to Meta-Analysis. Chichester, UK, John Wiley and Sons, 2009
81. Morgan JK, Olino TM, McMakin DL, et al: Neural response to reward as a predictor of increases in depressive symptoms in adolescence. Neurobiol Dis 2013; 52: 66-74
82. Telzer EH, Fuligni AJ, Lieberman MD, et al: Neural sensitivity to eudaimonic and hedonic rewards differentially predict adolescent depressive symptoms over time. Proc Natl Acad Sci USA 2014; 111: 6600-6605
83. Morgan JK, Shaw DS, Olino TM, et al: History of depression and frontostriatal connectivity during reward processing in late adolescent boys. J Clin Child Adolescent Psychol 2016; 45: 59-68
84. Carl H, Walsh E, Eisenlohr-Moul T, et al: Sustained anterior cingulate cortex activation during reward processing predicts response to psychotherapy in major depressive disorder. J Affect Disord 2016; 203: 204-212
85. Walsh E, Carl H, Eisenlohr-Moul T, et al: Attenuation of frontostriatal connectivity during reward processing predicts response to psychotherapy in major depressive disorder. Neuropsychopharmacology 2017; 42: 831-843
86. Di Chiara G, North RA: Neurobiology of opiate abuse. Trends Pharmacol Sci 1992; 13: 185-193
87. Bressan RA, Crippa JA: The role of dopamine in reward and pleasure behaviour: review of data from preclinical research. Acta Psychiatr Scand Suppl 2005; (427): 14-21
88. Eickhoff SB, Nichols TE, Laird AR, et al: Behavior, sensitivity, and power of activation likelihood estimation characterized by massive empirical simulation. Neuroimage 2016; 137: 70-85
89. Pan PM, Sato JR, Salum GA, et al: Ventral striatum functional connectivity as a predictor of adolescent depressive disorder in a longitudinal community-based. Am J Psychiatry 2017; 174: 1112-1119
90. Schultz W, Dayan P, Montague PR: A neural substrate of prediction and reward. Science 1997; 275: 1593-1599
91. Robbins TW, Everitt BJ: Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol 1996; 6: 228-236
92. Heimer L, deOlmos JS, Alheid GF, et al: The human basal forebrain, part II, in Handbook of Chemical Neuroanatomy, The Primate Nervous System, Part III. Edited by Bloom FE, Björklund A, Hökfelt T. Amsterdam, Elsevier, 1999; 15: 57-226
93. Haber SN: Neuroanatomy of reward: a view from the ventral striatum, in Neurobiology of sensation and reward. Edited by Gottfried JA. Boca Raton, Fla, CRC Press, 2011, pp 235-262
94. Rolls ET: The orbitofrontal cortex and emotion in health and disease, including depression. Neuropsychologia (Epub ahead of print, Sept 24, 2017)
95. Carlson JM, Foti D, Mujica-Parodi LR, et al: Ventral striatal and medial prefrontal BOLD activation is correlated with reward-related electrocortical activity: a combined ERP and fMRI study. Neuroimage 2011; 57: 1608-1616
96. Foti D, Weinberg A, Dien J, et al: Event-related potential activity in the basal ganglia differentiates rewards from nonrewards: temporospatial principal components analysis and source localization of the feedback negativity. Hum Brain Mapp 2011; 32: 2207-2216
97. Holroyd CB, Coles MGH: The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 2002; 109: 679-709
98. Luu P, Tucker DM, Derryberry D, et al: Electrophysiological responses to errors and feedback in the process of action regulation. Psychol Sci 2003; 14: 47-53
99. Crowley MJ, Wu J, Hommer RE, et al: A developmental study of the feedback-related negativity from 10-17 years: age and sex effects for reward versus non-reward. Dev Neuropsychol 2013; 38: 595-612
100. Zottoli TM, Grose-Fifer J: The feedback-related negativity (FRN) in adolescents. Psychophysiology 2012; 49: 413-420
101. Conway KP, Compton W, Stinson FS, et al: Lifetime comorbidity of DSM-IV mood and anxiety disorders and specific drug use disorders: results from the National Epidemiologic Survey on Alcohol and Related Conditions. J Clin Psychiatry 2006; 67: 247-257
102. Zhang B, Lin P, Shi H, et al: Mapping anhedonia-specific dysfunction in a transdiagnostic approach: an ALE meta-analysis. Brain Imaging Behav 2016; 10: 920-939
103. National Advisory Mental Health Council Workgroup on Tasks and Measures for Research Domain Criteria (RDoC, National Institutes of Health): Behavioral Assessment Methods for RDoC Constructs. Bethesda, Md, National Institute of Mental Health, August 2016 (https://www.nimh.nih.gov/about/advisory-boards-and-groups/namhc/reports/rdoc-council-workgroup-report-153440.pdf)
104. Han G, Klimes-Dougan B, Jepsen S, et al: Selective neurocognitive impairments in adolescents with major depressive disorder. J Adolesc 2012; 35: 11-20
105. Malone DA Jr, Dougherty DD, Rezai AR, et al: Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol Psychiatry 2009; 65: 267-275
106. Schlaepfer TE, Cohen MX, Frick C, et al: Deep brain stimulation to reward circuitry alleviates anhedonia in refractory major depression. Neuropsychopharmacology 2008; 33: 368-377
107. Dougherty DD, Rezai AR, Carpenter LL, et al: A randomized sham-controlled trial of deep brain stimulation of the ventral capsule/ventral striatum for chronic treatment-resistant depression. Biol Psychiatry 2015; 78: 240-248
108. Admon R, Kaiser RH, Dillon DG, et al: Dopaminergic enhancement of striatal response to reward in major depression. Am J Psychiatry 2017; 174: 378-386
109. Lally N, Nugent AC, Luckenbaugh DA, et al: Neural correlates of change in major depressive disorder anhedonia following open-label ketamine. J Psychopharmacol 2015; 29: 596-607
110. Rice F, Rawal A, Riglin L, et al: Examining reward-seeking, negative self-beliefs, and over-general autobiographical memory as mechanisms of change in classroom prevention programs for adolescent depression. J Affect Disord 2015; 186: 320-327