Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

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.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

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.

Similar content being viewed by others

References

  1. Preston, S. D. & de-Waal, F. B. M. Empathy: Its ultimate and proximate bases. Behav. Brain Sci. 25, 1–72 (2002)

    PubMed  Google Scholar 

  2. Gallese, V., Keysers, C. & Rizzolatti, G. A unifying view of the basis of social cognition. Trends Cogn. Sci. 8, 396–403 (2004)

    Article  Google Scholar 

  3. Decety, J. & Jackson, P. L. The functional architecture of human empathy. Behav. Cogn. Neurosci. Rev. 3, 71–100 (2004)

    Article  Google Scholar 

  4. Rabin, M. Incorporating fairness into game theory and economics. Am. Econ. Rev. 83, 1281–1302 (1993)

    Google Scholar 

  5. Levine, D. K. Modeling altruism and spitefulness in experiments. Rev. Econ. Dynam. 1, 593–622 (1998)

    Article  Google Scholar 

  6. Camerer, C. F. Behavioral Game Theory: Experiments in Strategic Interaction (Princeton Univ. Press, Princeton, 2003)

    MATH  Google Scholar 

  7. Fehr, E. & Schmidt, K. M. A theory of fairness, competition, and cooperation. Q. J. Econ. 114, 817–868 (1999)

    Article  Google Scholar 

  8. Wicker, B. et al. Both of us disgusted in my insula: The common neural basis of seeing and feeling disgust. Neuron 40, 655–664 (2003)

    Article  CAS  Google Scholar 

  9. Keysers, C. et al. A touching sight: SII/PV activation during the observation and experience of touch. Neuron 42, 335–346 (2004)

    Article  CAS  Google Scholar 

  10. Singer, T. et al. Empathy for pain involves the affective but not sensory components of pain. Science 303, 1157–1162 (2004)

    Article  ADS  CAS  Google Scholar 

  11. Jackson, P. L., Meltzoff, A. N. & Decety, J. How do we perceive the pain of others: A window into the neural processes involved in empathy. Neuroimage 3, 771–779 (2005)

    Article  Google Scholar 

  12. Morrison, I., Lloyd, D., di Pellegrino, G. & Roberts, N. Vicarious responses to pain in anterior cingulate cortex: is empathy a multisensory issue? Cogn. Affect. Behav. Neurosci. 4, 270–278 (2004)

    Article  Google Scholar 

  13. Craig, A. D. Human feelings: why are some more aware than others? Trends Cogn. Sci. 8, 239–241 (2004)

    Article  Google Scholar 

  14. Singer, T., Kiebel, S. J., Winston, J. S., Dolan, R. J. & Frith, C. D. Brain responses to the acquired moral status of faces. Neuron 41, 653–662 (2004)

    Article  CAS  Google Scholar 

  15. Fehr, E. & Gachter, S. Altruistic punishment in humans. Nature 415, 137–140 (2002)

    Article  ADS  CAS  Google Scholar 

  16. Fehr, E. & Fischbacher, U. The nature of human altruism. Nature 425, 785–791 (2003)

    Article  ADS  CAS  Google Scholar 

  17. Boyd, R., Gintis, H., Bowles, S. & Richerson, P. J. The evolution of altruistic punishment. Proc. Natl Acad. Sci. USA 100, 3531–3535 (2003)

    Article  ADS  CAS  Google Scholar 

  18. Cardinal, R. N., Parkinson, J. A., Hall, J. & Everitt, B. J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci. Biobehav. Rev. 26, 321–352 (2002)

    Article  Google Scholar 

  19. O'Doherty, J. et al. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304, 452–454 (2004)

    Article  ADS  CAS  Google Scholar 

  20. Schultz, W. Multiple reward signals in the brain. Nature Rev. Neurosci. 1, 199–207 (2000)

    Article  CAS  Google Scholar 

  21. de Quervain, D. J. et al. The neural basis of altruistic punishment. Science 305, 1254–1258 (2004)

    Article  ADS  CAS  Google Scholar 

  22. Davis, M. A. A multidimensional approach to individual differences in empathy. JSAS Cat. Selected Docs Psychol. 10, 85 (1980)

    Google Scholar 

  23. Dayan, P. & Balleine, B. W. Reward, motivation, and reinforcement learning. Neuron 36, 285–298 (2002)

    Article  CAS  Google Scholar 

  24. Montague, P. R., Hyman, S. E. & Cohen, J. D. Computational roles for dopamine in behavioural control. Nature 431, 760–767 (2004)

    Article  ADS  CAS  Google Scholar 

  25. Berg, J., Dickhaut, J. & McCabe, K. Trust, reciprocity and social history. Games Econ. Behav. 10, 122–142 (1995)

    Article  Google Scholar 

  26. Friston, K. J. et al. Spatial registration and normalization of images. Hum. Brain Mapp. 2, 165–189 (1995)

    Article  Google Scholar 

  27. Josephs, O., Turner, R. & Friston, K. Event-related fMRI. Hum. Brain Mapp. 5, 243–248 (1997)

    Article  CAS  Google Scholar 

  28. Friston, K. J. et al. Statistical parametric maps in functional imaging: A general linear approach. Hum. Brain Mapp. 2, 189–210 (1995)

    Article  Google Scholar 

  29. Penny, W. & Holmes, A. P. in Human Brain Function (eds Frackowiak, R. S. J. et al.) 843–850 (Elsevier, San Diego, 2004)

    Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tania Singer.

Ethics declarations

Competing interests

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)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Singer, T., Seymour, B., O'Doherty, J. et al. Empathic neural responses are modulated by the perceived fairness of others. Nature 439, 466–469 (2006). https://doi.org/10.1038/nature04271

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature04271

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing