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Empathic neural responses are modulated by the perceived fairness of others

Abstract

The neural processes underlying empathy are a subject of intense interest within the social neurosciences1,2,3. However, very little is known about how brain empathic responses are modulated by the affective link between individuals. We show here that empathic responses are modulated by learned preferences, a result consistent with economic models of social preferences4,5,6,7. We engaged male and female volunteers in an economic game, in which two confederates played fairly or unfairly, and then measured brain activity with functional magnetic resonance imaging while these same volunteers observed the confederates receiving pain. Both sexes exhibited empathy-related activation in pain-related brain areas (fronto-insular and anterior cingulate cortices) towards fair players. However, these empathy-related responses were significantly reduced in males when observing an unfair person receiving pain. This effect was accompanied by increased activation in reward-related areas, correlated with an expressed desire for revenge. We conclude that in men (at least) empathic responses are shaped by valuation of other people's social behaviour, such that they empathize with fair opponents while favouring the physical punishment of unfair opponents, a finding that echoes recent evidence for altruistic punishment.

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Acknowledgements

We thank P. Aston, S. Kiebel and E. Featherstone for their help. This work was supported by the German Academy of Natural Sciences Leopoldina, Halle, from the Ministry of Education and Science, by the Medical Research Council (UK), and by Wellcome Trust Programme Grants to R.J.D. and C.D.F. Author Contributions T.S. designed, implemented, analysed and wrote the paper. B.S., K.E.S. and J.P.O. helped with scanning. All authors contributed to designing the study, discussing the data and preparing the manuscript.

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Correspondence to Tania Singer.

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Reprints and permissions information is available at npg.nature.com/reprintsandpermissions. The authors declare no competing financial interests.

Supplementary information

Supplementary Methods

This file contains the Supplementary Methods section containing information about sample, experimental procedure, image acquisition and analysis. (PDF 28 kb)

Supplementary Tables

This file contains Supplementary Tables 1–11. Supplementary Table 1 shows relevant descriptive statistics of sample, pain intensity and subjective ratings. Supplementary Tables 2–11 display brain coordinates and z-scores for all relevant brain analyses. The colours indicate whether analyses refer to female (pink) or male (blue) subjects. (PDF 82 kb)

Supplementary Figures

This file contains Supplementary Figures 1–4 depicting the experimental procedure, correlations between empathy scores and brain activation in ACC and AI, mean level differences of the three revenge scales as a function of gender and their inter correlations and correlation between desire for revenge and brain activity in nucleus accumbens. (PDF 38 kb)

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Further reading

Figure 1: Experimental models I and II and behavioural ratings.
Figure 2: Pain-sensitive activation networks to the sight of fair and unfair players in pain.
Figure 3: Gender differences in brain activity in nucleus accumbens specific to the perception of an unfair compared to fair player in pain.

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