Brain activations associated with anticipation and delivery of monetary reward: A systematic review and meta-analysis of fMRI studies.
Journal
PloS one
ISSN: 1932-6203
Titre abrégé: PLoS One
Pays: United States
ID NLM: 101285081
Informations de publication
Date de publication:
2021
2021
Historique:
received:
23
11
2020
accepted:
13
07
2021
entrez:
5
8
2021
pubmed:
6
8
2021
medline:
25
11
2021
Statut:
epublish
Résumé
While multiple studies have examined the brain functional correlates of reward, meta-analyses have either focused on studies using the monetary incentive delay (MID) task, or have adopted a broad strategy, combining data from studies using both monetary and non-monetary reward, as probed using a wide range of tasks. To meta-analyze fMRI studies that used monetary reward and in which there was a definable cue-reward contingency. Studies were limited to those using monetary reward in order to avoid potential heterogeneity from use of other rewards, especially social rewards. Studies using gambling or delay discounting tasks were excluded on the grounds that reward anticipation is not easily quantifiable. English-language fMRI studies (i) that reported fMRI findings on healthy adults; (ii) that used monetary reward; and (iii) in which a cue that was predictive of reward was compared to a no win (or lesser win) condition. Only voxel-based studies were included; those where brain coverage was incomplete were excluded. Ovid, Medline and PsycInfo, from 2000 to 2020, plus checking of review articles and meta-analyses. Data were pooled using Seed-based d Mapping with Permutation of Subject Images (SDM-PSI). Heterogeneity among studies was examined using the I2 statistic. Publication bias was examined using funnel plots and statistical examination of asymmetries. Moderator variables including whether the task was pre-learnt, sex distribution, amount of money won and width of smoothing kernel were examined. Pooled data from 45 studies of reward anticipation revealed activations in the ventral striatum, the middle cingulate cortex/supplementary motor area and the insula. Pooled data from 28 studies of reward delivery again revealed ventral striatal activation, plus cortical activations in the anterior and posterior cingulate cortex. There was relatively little evidence of publication bias. Among moderating variables, only whether the task was pre-learnt exerted an influence. According to this meta-analysis monetary reward anticipation and delivery both activate the ventral but not the dorsal striatum, and are associated with different patterns of cortical activation.
Sections du résumé
BACKGROUND
While multiple studies have examined the brain functional correlates of reward, meta-analyses have either focused on studies using the monetary incentive delay (MID) task, or have adopted a broad strategy, combining data from studies using both monetary and non-monetary reward, as probed using a wide range of tasks.
OBJECTIVE
To meta-analyze fMRI studies that used monetary reward and in which there was a definable cue-reward contingency. Studies were limited to those using monetary reward in order to avoid potential heterogeneity from use of other rewards, especially social rewards. Studies using gambling or delay discounting tasks were excluded on the grounds that reward anticipation is not easily quantifiable.
STUDY ELIGIBILITY
English-language fMRI studies (i) that reported fMRI findings on healthy adults; (ii) that used monetary reward; and (iii) in which a cue that was predictive of reward was compared to a no win (or lesser win) condition. Only voxel-based studies were included; those where brain coverage was incomplete were excluded.
DATA SOURCES
Ovid, Medline and PsycInfo, from 2000 to 2020, plus checking of review articles and meta-analyses.
DATA SYNTHESIS
Data were pooled using Seed-based d Mapping with Permutation of Subject Images (SDM-PSI). Heterogeneity among studies was examined using the I2 statistic. Publication bias was examined using funnel plots and statistical examination of asymmetries. Moderator variables including whether the task was pre-learnt, sex distribution, amount of money won and width of smoothing kernel were examined.
RESULTS
Pooled data from 45 studies of reward anticipation revealed activations in the ventral striatum, the middle cingulate cortex/supplementary motor area and the insula. Pooled data from 28 studies of reward delivery again revealed ventral striatal activation, plus cortical activations in the anterior and posterior cingulate cortex. There was relatively little evidence of publication bias. Among moderating variables, only whether the task was pre-learnt exerted an influence.
CONCLUSIONS
According to this meta-analysis monetary reward anticipation and delivery both activate the ventral but not the dorsal striatum, and are associated with different patterns of cortical activation.
Identifiants
pubmed: 34351957
doi: 10.1371/journal.pone.0255292
pii: PONE-D-20-35918
pmc: PMC8341642
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Meta-Analysis
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0255292Déclaration de conflit d'intérêts
The authors have declared that no competing interest exist.
Références
Hum Brain Mapp. 2007 Nov;28(11):1194-205
pubmed: 17266101
J Neurosci. 2001 Aug 15;21(16):RC159
pubmed: 11459880
Neuroreport. 2001 Dec 4;12(17):3683-7
pubmed: 11726774
J Neurosci. 2008 Dec 24;28(52):14311-9
pubmed: 19109512
Soc Cogn Affect Neurosci. 2009 Dec;4(4):409-16
pubmed: 19843618
Hum Brain Mapp. 2015 Jan;36(1):187-98
pubmed: 25158155
Neuropsychopharmacology. 2010 Jan;35(1):4-26
pubmed: 19812543
Science. 2004 Oct 15;306(5695):443-7
pubmed: 15486290
Nat Rev Neurosci. 2006 Apr;7(4):268-77
pubmed: 16552413
Exp Brain Res. 2001 Aug;139(3):278-86
pubmed: 11545466
Neuroimage. 2014 Jan 1;84:279-89
pubmed: 24001457
Neuropsychol Rev. 2018 Dec;28(4):496-506
pubmed: 30255220
Neurosci Biobehav Rev. 2021 Mar;122:1-17
pubmed: 33421544
J Urol. 2006 Aug;176(2):679-83
pubmed: 16813919
Addict Biol. 2015 May;20(3):557-69
pubmed: 24754423
Cereb Cortex. 2000 Mar;10(3):272-84
pubmed: 10731222
Proc Natl Acad Sci U S A. 2011 Sep 13;108 Suppl 3:15647-54
pubmed: 21389268
Psychol Med. 2015 Jun;45(8):1765-78
pubmed: 25577954
PLoS One. 2013 May 15;8(5):e61470
pubmed: 23690923
J Neurophysiol. 1998 Jul;80(1):1-27
pubmed: 9658025
Nat Neurosci. 2007 Jun;10(6):787-91
pubmed: 17468751
Addict Biol. 2014 Sep;19(5):885-94
pubmed: 23445167
J Neurosci. 2009 Apr 8;29(14):4531-41
pubmed: 19357278
Neuroimage. 2019 Feb 1;186:174-184
pubmed: 30389629
Biol Mood Anxiety Disord. 2014 Jul 23;4:7
pubmed: 25075275
Philos Trans R Soc Lond B Biol Sci. 2008 Dec 12;363(1511):3771-86
pubmed: 18829428
Int J Neuropsychopharmacol. 2013 Aug;16(7):1461-71
pubmed: 23406545
Annu Rev Neurosci. 2000;23:473-500
pubmed: 10845072
Nature. 2006 Aug 31;442(7106):1042-5
pubmed: 16929307
Hum Brain Mapp. 2018 Aug;39(8):3398-3418
pubmed: 29696725
World J Biol Psychiatry. 2005;6(2):113-20
pubmed: 16156484
J Neurosci. 2007 Feb 28;27(9):2349-56
pubmed: 17329432
Cereb Cortex. 2003 Mar;13(3):318-27
pubmed: 12571121
Neuron. 2005 Feb 3;45(3):459-67
pubmed: 15694331
Psychiatry Res. 1999 Jul 30;91(1):1-10
pubmed: 10496688
Brain Behav. 2012 Nov;2(6):741-53
pubmed: 23170237
J Neurosci. 2011 Dec 14;31(50):18266-74
pubmed: 22171031
Hum Brain Mapp. 2000 Nov;11(3):162-77
pubmed: 11098795
Neuroimage Clin. 2016 Aug 11;12:724-736
pubmed: 27766203
Exp Brain Res. 1991;85(3):491-500
pubmed: 1915708
Front Behav Neurosci. 2016 Nov 15;10:220
pubmed: 27895564
Neuropsychologia. 2004;42(12):1585-97
pubmed: 15327927
Behav Brain Res. 2007 Feb 12;177(1):165-70
pubmed: 17140674
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15106-11
pubmed: 18794529
Neuroimage. 2013 Feb 1;66:270-7
pubmed: 23110886
Neuroimage. 2010 Apr 1;50(2):657-64
pubmed: 19969090
Hum Brain Mapp. 2020 Aug 15;41(12):3318-3341
pubmed: 32500968
J Neurosci. 2011 Mar 16;31(11):4178-87
pubmed: 21411658
Neuroimage. 2000 Jul;12(1):20-7
pubmed: 10875899
Cereb Cortex. 2011 Apr;21(4):769-76
pubmed: 20732900
Biol Psychiatry. 2012 Apr 15;71(8):749-57
pubmed: 22336565
Curr Top Behav Neurosci. 2016;27:199-230
pubmed: 26276036
Prog Brain Res. 2000;126:193-215
pubmed: 11105648
Neuroimage. 2003 Oct;20(2):1086-95
pubmed: 14568478
Front Psychiatry. 2014 Feb 10;5:13
pubmed: 24575054
Brain Cogn. 2004 Nov;56(2):129-40
pubmed: 15518930
J Affect Disord. 2016 Oct;203:204-212
pubmed: 27295377
Brain Res. 1978 Aug 25;152(2):215-47
pubmed: 354753
J Neurosci. 2013 Jun 12;33(24):9905-12
pubmed: 23761885
Neurol Res. 1985 Mar;7(1):2-10
pubmed: 2860583
Soc Cogn Affect Neurosci. 2015 Aug;10(8):1102-12
pubmed: 25567763
Eur Psychiatry. 2012 Nov;27(8):605-11
pubmed: 21658917
Biol Psychiatry. 2013 Feb 1;73(3):280-8
pubmed: 22939991
J Comp Physiol Psychol. 1954 Dec;47(6):419-27
pubmed: 13233369
Cereb Cortex. 2000 Mar;10(3):284-94
pubmed: 10731223
BMC Med Res Methodol. 2008 Nov 27;8:79
pubmed: 19036172
Trends Cogn Sci. 2007 Nov;11(11):489-97
pubmed: 17988930
J Cogn Neurosci. 2009 Mar;21(3):489-510
pubmed: 18510452
Neuroimage. 2013 Aug 1;76:412-27
pubmed: 23507394
Psychiatry Res Neuroimaging. 2016 Aug 30;254:127-36
pubmed: 27419380
Learn Mem. 2008 Oct 02;15(10):728-32
pubmed: 18832559
Neurosci Biobehav Rev. 2011 Apr;35(5):1219-36
pubmed: 21185861
Psychophysiology. 2008 Jan;45(1):36-49
pubmed: 17850241
Neuropsychologia. 2012 Jun;50(7):1252-66
pubmed: 22366111
Neuroimage. 2007 Jul 1;36(3):830-42
pubmed: 17493836
Science. 2019 Jan 18;363(6424):
pubmed: 30655412
J Comp Neurol. 1996 Jul 22;371(2):179-207
pubmed: 8835726
Psychophysiology. 2018 Mar;55(3):
pubmed: 29044552
Trends Neurosci. 2007 May;30(5):194-202
pubmed: 17408759
Neuroimage. 2005 May 1;25(4):1279-91
pubmed: 15850746
Schizophr Res. 2010 May;118(1-3):154-61
pubmed: 20005675
Schizophr Res. 2015 Aug;166(1-3):17-23
pubmed: 25999039
Psychiatry Res. 2014 Sep 30;223(3):244-52
pubmed: 24969539
Brain Struct Funct. 2010 Jun;214(5-6):655-67
pubmed: 20512370
J Neurosci. 2012 Feb 15;32(7):2544-51
pubmed: 22396427
J Vis Exp. 2019 Nov 27;(153):
pubmed: 31840658
Acta Psychiatr Scand. 2011 May;123(5):376-86
pubmed: 21175552
Eur J Neurosci. 2013 Aug;38(3):2399-407
pubmed: 23617942
Neuroreport. 1997 Mar 24;8(5):1225-8
pubmed: 9175118
Neuroimage. 2018 Aug 1;176:550-553
pubmed: 29729389
Neuroscientist. 2004 Jun;10(3):260-8
pubmed: 15155064
Neuroimage Clin. 2013 Jan 17;2:212-20
pubmed: 24179774
Mol Autism. 2014 Jan 31;5(1):7
pubmed: 24485285
Brain. 2014 Jan;137(Pt 1):12-32
pubmed: 23869106
Nat Rev Neurosci. 2019 Oct;20(10):593-608
pubmed: 31492945
Prog Brain Res. 2012;195:123-63
pubmed: 22230626
Neuroimage. 2010 Mar;50(1):223-32
pubmed: 20006717
J Neurosci. 2005 Sep 21;25(38):8650-6
pubmed: 16177032
Ann N Y Acad Sci. 2007 May;1104:108-22
pubmed: 17347332
Psychopharmacology (Berl). 2014 Aug;231(16):3217-28
pubmed: 24682502