Common and distinct neural correlates of personal and vicarious reward: A quantitative meta-analysis

NeuroImage

Volumn 112, Issue , 2015, Pages 244-253

  Morelli, Sylvia A ^a   Sacchet, Matthew D ^a   Zaki, Jamil ^a  

^a STANFORD UNIVERSITY   (United States)

Author keywords

Activation likelihood estimation; Empathy; Meta analysis; Positive empathy; Ventromedial prefrontal cortex; Vicarious reward

Indexed keywords

BRAIN; EMPATHY; HUMAN; META ANALYSIS; NERVOUS SYSTEM FUNCTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; REINFORCEMENT; REWARD;

BRAIN; EMPATHY; HUMANS; MAGNETIC RESONANCE IMAGING; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA; REINFORCEMENT (PSYCHOLOGY); REWARD;

EID: 84939956613     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2014.12.056     Document Type: Article

References (111)

1. Adolphs R. What does the amygdala contribute to social cognition?. Ann. N. Y. Acad. Sci. 2010, 1191:42-61.
2. Albrecht K., Volz K.G., Sutter M., Laibson D.I., Von Cramon D.Y. What is for me is not for you: Brain correlates of intertemporal choice for self and other. Soc. Cogn. Affect. Neurosci. 2010, 6(2):218-225.
3. Albrecht K., Volz K.G., Sutter M., von Cramon D.Y. What do I want and when do I want it: Brain correlates of decisions made for self and other. PLoS ONE 2013, 8(8):e73531.
4. Baron-Cohen S., Ring H.A., Bullmore E.T., Wheelwright S., Ashwin C., Williams S. The amygdala theory of autism. Neurosci. Biobehav. Rev. 2000, 24(3):355-364.
5. Bartra O., McGuire J.T., Kable J.W. The valuation system: a coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. NeuroImage 2013, 76:412-427. 10.1016/j.neuroimage.2013.02.063.
6. Batson C.D., Batson J.G., Slingsby J.K., Harrell K.L., Peekna H.M., Todd R.M. Empathic joy and the empathy-altruism hypothesis. J. Pers. Soc. Psychol. 1991, 61(3):413-426.
7. Bellebaum C., Jokisch D., Gizewski E., Forsting M., Daum I. The neural coding of expected and unexpected monetary performance outcomes. Dissociations between active and observational learning. Behavioural Brain Research 2012, 227(1):241-251.
8. Blair R. Fine cuts of empathy and the amygdala: Dissociable deficits in psychopathy and autism. Q. J. Exp. Psychol. 2008, 61(1):157-170.
9. Braams B.R., Güroğlu B., de Water E., Meuwese R., Koolschijn P.C., Peper J.S., Crone E.A. Reward-related neural responses are dependent on the beneficiary. Soc. Cogn. Affect. Neurosci. 2014, 9(7):1030-1037.
10. Buckner R.L., Carroll D.C. Self-projection and the brain. Trends Cogn. Sci. 2007, 11(2):49-57. (S1364-6613(06)00327-5 [pii]). 10.1016/j.tics.2006.11.004.
11. Burke C.J., Tobler P.N., Baddeley M., Schultz W. Neural mechanisms of observational learning. Proceedings of the National Academy of Sciences 2010, 107(32):14431-14436.
12. Canessa N., Motterlini M., Di Dio C., Perani D., Scifo P., Cappa S.F., Rizzolatti G. Understanding others' regret: A FMRI study. PLoS ONE 2009, 4(10):e7402.
13. Canessa N., Motterlini M., Alemanno F., Perani D., Cappa S.F. Learning from other people's experience: A neuroimaging study of decisional interactive-learning. NeuroImage 2011, 55(1):353-362.
14. Caspers S., Zilles K., Laird A.R., Eickhoff S.B. ALE meta-analysis of action observation and imitation in the human brain. NeuroImage 2010, 50(3):1148-1167.
15. Chester D.S., Powell C.A., Smith R.H., Joseph J.E., Kedia G., Combs D.J., DeWall C.N. Justice for the average Joe: The role of envy and the mentalizing network in the deservingness of others' misfortunes. Social Neuroscience 2013, 8(6):640-649.
16. Chib V.S., Rangel A., Shimojo S., O'Doherty J.P. Evidence for a common representation of decision values for dissimilar goods in human ventromedial prefrontal cortex. J. Neurosci. 2009, 29(39):12315-12320.
17. Cikara M., Fiske S.T. Bounded empathy: Neural responses to outgroup targets' (mis) fortunes. J. Cogn. Neurosci. 2011, 23(12):3791-3803.
18. Cooper J.C., Dunne S., Furey T., O'Doherty J.P. Human dorsal striatum encodes prediction errors during observational learning of instrumental actions. J. Cogn. Neurosci. 2012, 24(1):106-118.
19. Davis M.H. Empathy: A social psychological approach 1994, Brown and Benchmark, Madison, WI.
20. Dawes C.T., Loewen P.J., Schreiber D., Simmons A.N., Flagan T., McElreath R., Paulus M.P. Neural basis of egalitarian behavior. Proc. Natl. Acad. Sci. 2012, 109(17):6479-6483.
21. de Quervain D.J., Fischbacher U., Treyer V., Schellhammer M., Schnyder U., Buck A., Fehr E. The neural basis of altruistic punishment. Science 2004, 305(5688):1254-1258.
22. Dohmen T., Falk A., Fliessbach K., Sunde U., Weber B. Relative versus absolute income, joy of winning, and gender: Brain imaging evidence. J. Public Econ. 2011, 95(3):279-285.
23. Dunn E., Aknin L., Norton M. Prosocial spending and happiness: Using money to benefit others pays off. Curr. Dir. Psychol. Sci. 2014, 23(2):41-47.
24. Dvash J., Gilam G., Ben-Ze'ev A., Hendler T., Shamay-Tsoory S.G. The envious brain: the neural basis of social comparison. Hum. Brain Mapp. 2010, 31(11):1741-1750.
25. Eickhoff S.B., Laird A.R., Grefkes C., Wang L.E., Zilles K., Fox P.T. Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: A random-effects approach based on empirical estimates of spatial uncertainty. Hum. Brain Mapp. 2009, 30(9):2907-2926.
26. Eickhoff S.B., Bzdok D., Laird A.R., Roski C., Caspers S., Zilles K., Fox P.T. Co-activation patterns distinguish cortical modules, their connectivity and functional differentiation. NeuroImage 2011, 57(3):938-949.
27. Eickhoff S.B., Bzdok D., Laird A.R., Kurth F., Fox P.T. Activation likelihood estimation meta-analysis revisited. NeuroImage 2012, 59(3):2349-2361.
28. Elliott R., Newman J.L., Longe O.A., William Deakin J. Instrumental responding for rewards is associated with enhanced neuronal response in subcortical reward systems. NeuroImage 2004, 21(3):984-990.
29. Ewbank M.P., Barnard P.J., Croucher C.J., Ramponi C., Calder A.J. The amygdala response to images with impact. Soc. Cogn. Affect. Neurosci. 2009, 4(2):127-133.
30. Fareri D.S., Delgado M.R. Differential reward responses during competition against in-and out-of-network others. Soc. Cogn. Affect. Neurosci. 2014, 9(4):412-420.
31. Fareri D.S., Niznikiewicz M.A., Lee V.K., Delgado M.R. Social network modulation of reward-related signals. J. Neurosci. 2012, 32(26):9045-9052.
32. Fehr E., Camerer C.F. Social neuroeconomics: the neural circuitry of social preferences. Trends Cogn. Sci. 2007, 11(10):419-427. (S1364-6613(07)00215-X [pii]). 10.1016/j.tics.2007.09.002.
33. Fujita K., Henderson M.D., Eng J., Trope Y., Liberman N. Spatial distance and mental construal of social events. Psychol. Sci. 2006, 17(4):278-282.
34. Gable S.L. Approach and avoidance social motives and goals. J. Pers. 2006, 74(1):175-222.
35. Gable S.L., Reis H.T. Good news! Capitalizing on positive events in an interpersonal context. Adv. Exp. Soc. Psychol. 2010, 42:195-257.
36. Gläscher J., Hampton A.N., O'Doherty J.P. Determining a role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making. Cereb. Cortex 2009, 19(2):483-495.
37. Gottfried J.A., O'Doherty J., Dolan R.J. Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 2003, 301(5636):1104-1107.
38. Grabenhorst F., Rolls E.T. Value, pleasure and choice in the ventral prefrontal cortex. Trends Cogn. Sci. 2011, 15(2):56-67. 10.1016/j.tics.2010.12.004.
39. Hamilton J.P., Chen M.C., Waugh C.E., Joormann J., Gotlib I.H. Distinctive and common neural underpinnings of major depression, social anxiety, and their comorbidity. Social Cognitive and Affective Neuroscience 2014, nsu084.
40. Harbaugh W.T., Mayr U., Burghart D.R. Neural responses to taxation and voluntary giving reveal motives for charitable donations. Science 2007, 316(5831):1622-1625. (316/5831/1622 [pii]). 10.1126/science.1140738.
41. Hare T.A., O'Doherty J., Camerer C.F., Schultz W., Rangel A. Dissociating the role of the orbitofrontal cortex and the striatum in the computation of goal values and prediction errors. J. Neurosci. 2008, 28(22):5623-5630. (28/22/5623 [pii]). 10.1523/JNEUROSCI.1309-08.2008.
42. Hare T.A., Camerer C.F., Knoepfle D.T., Rangel A. Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J. Neurosci. 2010, 30(2):583-590. (30/2/583 [pii]). 10.1523/JNEUROSCI.4089-09.2010.
43. Hare T.A., Camerer C.F., Knoepfle D.T., Rangel A. Value computations in ventral medial prefrontal cortex during charitable decision making incorporate input from regions involved in social cognition. J. Neurosci. 2010, 30(2):583-590. (30/2/583 [pii]). 10.1523/JNEUROSCI.4089-09.2010.
44. Hooker C.I., Verosky S.C., Miyakawa A., Knight R.T., D'Esposito M. The influence of personality on neural mechanisms of observational fear and reward learning. Neuropsychologia 2008, 46(11):2709-2724.
45. Izquierdo A., Suda R.K., Murray E.A. Bilateral orbital prefrontal cortex lesions in rhesus monkeys disrupt choices guided by both reward value and reward contingency. J. Neurosci. 2004, 24(34):7540-7548.
46. Izuma K., Saito D.N., Sadato N. Processing of social and monetary rewards in the human striatum. Neuron 2008, 58(2):284-294. (S0896-6273(08)00266-3 [pii]). 10.1016/j.neuron.2008.03.020.
47. Izuma K., Saito D.N., Sadato N. The roles of the medial prefrontal cortex and striatum in reputation processing. Soc. Neurosci. 2010, 5(2):133-147.
48. Jabbi M., Swart M., Keysers C. Empathy for positive and negative emotions in the gustatory cortex. NeuroImage 2007, 34(4):1744-1753.
49. Janowski V., Camerer C., Rangel A. Empathic choice involves vmPFC value signals that are modulated by social processing implemented in IPL. Soc. Cogn. Affect. Neurosci. 2012, 8(2):201-209.
50. Jung D., Sul S., Kim H. Dissociable neural processes underlying risky decisions for self versus other. Front. Neurosci. 2013, 7:15.
51. Kätsyri J., Hari R., Ravaja N., Nummenmaa L. Just watching the game ain't enough: striatal fMRI reward responses to successes and failures in a video game during active and vicarious playing. Front. Hum. Neurosci. 2013, 7:278.
52. Kawamichi H., Sasaki A.T., Matsunaga M., Yoshihara K., Takahashi H.K., Tanabe H.C., Sadato N. Medial prefrontal cortex activation is commonly invoked by reputation of self and romantic partners. PLoS ONE 2013, 8(9):e74958.
53. Klucharev V., Hytonen K., Rijpkema M., Smidts A., Fernandez G. Reinforcement learning signal predicts social conformity. Neuron 2009, 61(1):140-151. (S0896-6273(08)01020-9 [pii]). 10.1016/j.neuron.2008.11.027.
54. Knutson B., Fong G.W., Adams C.M., Varner J.L., Hommer D. Dissociation of reward anticipation and outcome with event-related fMRI. Neuroreport 2001, 12(17):3683-3687.
55. Knutson B., Taylor J., Kaufman M., Peterson R., Glover G. Distributed neural representation of expected value. J. Neurosci. 2005, 25(19):4806-4812. (25/19/4806 [pii]). 10.1523/JNEUROSCI. 0642-05.2005.
56. Knutson B., Katovich K., Suri G. Inferring affect from fMRI data. Trends Cogn. Sci. 2014, 8:422-428.
57. Korn C.W., Prehn K., Park S.Q., Walter H., Heekeren H.R. Positively biased processing of self-relevant social feedback. The Journal of Neuroscience 2012, 32(47):16832-16844.
58. Kurth F., Zilles K., Fox P.T., Laird A.R., Eickhoff S.B. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 2010, 214(5-6):519-534.
59. Laird A.R., Fox P.M., Price C.J., Glahn D.C., Uecker A.M., Lancaster J.L., Fox P.T. ALE meta-analysis: Controlling the false discovery rate and performing statistical contrasts. Hum. Brain Mapp. 2005, 25(1):155-164.
60. Lamm C., Decety J., Singer T. Meta-analytic evidence for common and distinct neural networks associated with directly experienced pain and empathy for pain. NeuroImage 2011, 54(3):2492-2502. (S1053-8119(10)01306-6 [pii]). 10.1016/j.neuroimage.2010.10.014.
61. Levy D.J., Glimcher P.W. Comparing apples and oranges: using reward-specific and reward-general subjective value representation in the brain. J. Neurosci. 2011, 31(41):14693-14707. 10.1523/JNEUROSCI. 2218-11.2011.
62. Levy I., Lazzaro S.C., Rutledge R.B., Glimcher P.W. Choice from non-choice: predicting consumer preferences from blood oxygenation level-dependent signals obtained during passive viewing. J. Neurosci. 2011, 31(1):118-125. (31/1/118 [pii]). 10.1523/JNEUROSCI.3214-10.2011.
63. Lieberman M.D. Social cognitive neuroscience. Handbook of social psychology 2010, 143-193. McGraw-Hill, New York, NY. 5th ed. S.T. Fiske, D.T. Gilbert, G. Lindzey (Eds.).
64. Lindquist K.A., Wager T.D., Kober H., Bliss-Moreau E., Barrett L.F. The brain basis of emotion: A meta-analytic review. Behav. Brain Sci. 2012, 35(03):121-143. 10.1017/S0140525X11000446.
65. Liu X., Hairston J., Schrier M., Fan J. Common and distinct networks underlying reward valence and processing stages: a meta-analysis of functional neuroimaging studies. Neurosci. Biobehav. Rev. 2011, 35(5):1219-1236. (S0149-7634(10)00213-7 [pii]). 10.1016/j.neubiorev.2010.12.012.
66. Marcus D.S., Harwell J., Olsen T., Hodge M., Glasser M.F., Prior F., Van Essen D.C. Informatics and data mining tools and strategies for the human connectome project. Frontiers in Neuroinformatics 2011, 5:4.
67. Meffert H., Gazzola V., den Boer J.A., Bartels A.A., Keysers C. Reduced spontaneous but relatively normal deliberate vicarious representations in psychopathy. Brain 2013, 136(8):2550-2562.
68. Meshi D., Morawetz C., Heekeren H.R. Nucleus accumbens response to gains in reputation for the self relative to gains for others predicts social media use. Frontiers in Human Neuroscience 2013, 7.
69. Mitchell J.P. Inferences about mental states. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009, 364(1521):1309-1316. (364/1521/1309 [pii]). 10.1098/rstb.2008.0318.
70. Mitchell J.P., Schirmer J., Ames D.L., Gilbert D.T. Medial prefrontal cortex predicts intertemporal choice. J. Cogn. Neurosci. 2011, 23(4):857-866.
71. Mobbs D., Yu R., Meyer M., Passamonti L., Seymour B., Calder A.J., Dalgleish T. A key role for similarity in vicarious reward. Science 2009, 324(5929):900. (324/5929/900 [pii]). 10.1126/science.1170539.
72. Molenberghs P., Bosworth R., Nott Z., Louis W.R., Smith J.R., Amiot C.E., Decety J. The influence of group membership and individual differences in psychopathy and perspective taking on neural responses when punishing and rewarding others. Hum. Brain Mapp. 2014, 35(10):4989-4999.
73. Moll J., Krueger F., Zahn R., Pardini M., de Oliveira-Souza R., Grafman J. Human fronto-mesolimbic networks guide decisions about charitable donation. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(42):15623-15628. (0604475103 [pii]). 10.1073/pnas.0604475103.
74. Morelli S.A., Rameson L.T., Lieberman M.D. The neural components of empathy: Predicting daily prosocial behavior. Soc. Cogn. Affect. Neurosci. 2014, 9(1):39-47. 10.1093/scan/nss088.
75. Morelli S.A., Lieberman M.D., Zaki J. The emerging study of positive empathy. Soc. Personal. Psychol. Compass 2014.
76. Morelli S.A., Lieberman M.D., Telzer E.H., Zaki J. Positive empathy: Its structure and relation to prosociality, social connection, and well-being 2014, under review.
77. Morrison I., Björnsdotter M., Olausson H. Vicarious responses to social touch in posterior insular cortex are tuned to pleasant caressing speeds. The Journal of Neuroscience 2011, 31(26):9554-9562.
78. Murray E.A. The amygdala, reward and emotion. Trends Cogn. Sci. 2007, 11(11):489-497.
79. Perry D., Hendler T., Shamay-Tsoory S.G. Can we share the joy of others? Empathic neural responses to distress vs joy. Soc. Cogn. Affect. Neurosci. 2012, 7(8):909-916.
80. Puce A., Perrett D. Electrophysiology and brain imaging of biological motion. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2003, 358(1431):435-445.
81. Rangel A., Hare T. Neural computations associated with goal-directed choice. Curr. Opin. Neurobiol. 2010, 20(2):262-270.
82. Rilling J., Gutman D., Zeh T., Pagnoni G., Berns G., Kilts C. A neural basis for social cooperation. Neuron 2002, 35(2):395-405. (S0896627302007559 [pii]).
83. Rushworth M.F.S., Noonan M.A.P., Boorman E.D., Walton M.E., Behrens T.E. Frontal cortex and reward-guided learning and decision-making. Neuron 2011, 70(6):1054-1069.
84. Rutledge R.B., Skandali N., Dayan P., Dolan R.J. A computational and neural model of momentary subjective well-being. Proc. Natl. Acad. Sci. 2014, 111(33):12252-12257.
85. Sanfey A.G. Social decision-making: insights from game theory and neuroscience. Science 2007, 318(5850):598-602.
86. Saxe R., Powell L.J. It's the thought that counts: Specific brain regions for one component of theory of mind. Psychol. Sci. 2006, 17(8):692-699. (PSCI1768 [pii]). 10.1111/j.1467-9280.2006.01768.x.
87. Sescousse G., Caldú X., Segura B., Dreher J.-C. Processing of primary and secondary rewards: a quantitative meta-analysis and review of human functional neuroimaging studies. Neurosci. Biobehav. Rev. 2013, 37(4):681-696.
88. Silani G., Lamm C., Ruff C.C., Singer T. Right supramarginal gyrus is crucial to overcome emotional egocentricity bias in social judgments. J. Neurosci. 2013, 33(39):15466-15476.
89. Singer T., Klimecki O.M. Empathy and compassion. Curr. Biol. 2014, 24(18):R875-R878.
90. Smith A. The theory of moral sentiments 1790/2002, Cambridge University Press, Cambridge, UK.
91. Smith K.D., Keating J.P., Stotland E. Altruism reconsidered: The effect of denying feedback on a victim's status to empathic witnesses. J. Pers. Soc. Psychol. 1989, 57(4):641-650.
92. Spreng R.N., Mar R.A., Kim A.S. The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: a quantitative meta-analysis. J. Cogn. Neurosci. 2009, 21(3):489-510. 10.1162/jocn.2008.21029.
93. Spunt R.P., Lieberman M.D. An integrative model of the neural systems supporting the comprehension of observed emotional behavior. Neuroimage 2012, 59(3):3050-3059. doi:S1053-8119(11)01166-9 [pii]. http://dx.doi.org/10.1016/j.neuroimage.2011.10.005.
94. Strait C.E., Blanchard T.C., Hayden B.Y. Reward value comparison via mutual inhibition in ventromedial prefrontal cortex. Neuron 2014, 82(6):1357-1366.
95. Suzuki S., Harasawa N., Ueno K., Gardner J.L., Ichinohe N., Haruno M., Nakahara H. Learning to simulate others' decisions. Neuron 2012, 74(6):1125-1137.
96. Tamir D.I., Mitchell J.P. The default network distinguishes construals of proximal versus distal events. J. Cogn. Neurosci. 2011, 23(10):2945-2955.
97. Telzer E.H., Masten C.L., Berkman E.T., Lieberman M.D., Fuligni A.J. Gaining while giving: An fMRI study of the rewards of family assistance among White and Latino youth. Soc. Neurosci. 2010, 5(5-6):508-518.
98. Telzer E.H., Fuligni A.J., Lieberman M.D., Galván A. Ventral striatum activation to prosocial rewards predicts longitudinal declines in adolescent risk taking. Dev. Cogn. Neurosci. 2013, 3:45-52.
99. Tricomi E., Rangel A., Camerer C.F., O'Doherty J.P. Neural evidence for inequality-averse social preferences. Nature 2010, 463(7284):1089-1091. (nature08785 [pii]). 10.1038/nature08785.
100. Turkeltaub P.E., Eickhoff S.B., Laird A.R., Fox M., Wiener M., Fox P. Minimizing within-experiment and within-group effects in activation likelihood estimation meta-analyses. Hum. Brain Mapp. 2012, 33(1):1-13.
101. Varnum M.E., Shi Z., Chen A., Qiu J., Han S. When "Your" reward is the same as "My" reward: Self-construal priming shifts neural responses to own vs. friends' rewards. NeuroImage 2014, 87:164-169.
102. Wellman H.M., Cross D., Watson J. Meta-analysis of theory-of-mind development: the truth about false belief. Child Dev. 2001, 72(3):655-684.
103. Wicker B., Keysers C., Plailly J., Royet J., Gallese V., Rizzolatti G. Both of us disgusted in My Insula: The common neural basis of seeing and feeling disgust. Neuron 2003, 40(3):655-664.
104. Wunderlich K., Rangel A., O'Doherty J.P. Economic choices can be made using only stimulus values. Proc. Natl. Acad. Sci. 2010, 107(34):15005-15010.
105. Zaki J. Empathy: A motivated account. Psychol. Bull. 2014, 140(6):1608-1647.
106. Zaki J., Mitchell J. Equitable decision making is associated with neural markers of subjective value. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(49):19761-19766.
107. Zaki J., Mitchell J.P. Intuitive prosociality. Curr. Dir. Psychol. Sci. 2013, 22(6):466-470.
108. Zaki J., Ochsner K. The neuroscience of empathy: Progress, pitfalls, and promise. Nat. Neurosci. 2012, 15(5):675-680.
109. Zaki J., Schirmer J., Mitchell J.P. Social influence modulates the neural computation of value. Psychol. Sci. 2011, 22(7):894-900.
110. Zaki J., Lopez G., Mitchell J. Activity in ventromedial prefrontal cortex covaries with revealed social preferences: Evidence for person-invariant value. Soc. Cogn. Affect. Neurosci. 2014, 9(4):464-469.
111. Zink C.F., Pagnoni G., Martin-Skurski M.E., Chappelow J.C., Berns G.S. Human striatal responses to monetary reward depend on saliency. Neuron 2004, 42(3):509-517.