Cited by 1,726Action Observation and SynchronizationExperimental Behavioral Economics StudiesNeural and Behavioral Psychology Studies

The DOI matches its Crossref record; 30 of the 30 references it cites were found in a registry or an index; none of the 27 sources its claims cite is checked for support yet.

Empathic neural responses are modulated by the perceived fairness of others

Open access

Abstract

The neural processes underlying empathy are a subject of intense interest within the social neurosciences. 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 preferences. 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.

Overview

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TL;DR

Empathic brain responses to another person’s pain are shaped by perceived fairness: participants showed pain-related empathy in fronto-insular and anterior cingulate cortices toward fair players, but men showed reduced empathic responses and increased reward-related activity when an unfair player received pain. The authors conclude that, at least in men, empathy is modulated by social valuation, with unfair opponents’ pain potentially linked to reward and revenge.

Key findings

  • After a sequential Prisoner’s Dilemma game, both male and female subjects rated the fair player as significantly more fair, agreeable, likeable, and attractive than the unfair player (scale range 2 to 22; P < 0.001).
  • Both sexes showed empathy-related activation in pain-related brain areas, including bilateral anterior insula/fronto-insular cortex and anterior cingulate cortex, when observing a fair player in pain; ACC activation was significant in women ([9, 18, 27]; P < 0.001 uncorrected, P < 0.05 whole-brain corrected) but borderline in men ([29, 39, 27]; P = 0.001 uncorrected).
  • Men showed significantly enhanced bilateral fronto-insular activation when observing fair compared with unfair players in pain, whereas women showed no significant difference in empathy-related pain regions for fair versus unfair players.
  • In men, but not women, observing an unfair player receiving pain increased activation in left ventral striatum/nucleus accumbens and left orbito-frontal cortex; men also expressed a stronger desire for revenge than women (t(30) = 2.40, P < 0.05), and men with stronger revenge desire showed greater nucleus accumbens activation for unfair versus fair player pain.

Methods

  • Subjects were 16 men and 16 women; four professional actors (two female, two male) served as confederates. Subjects played a sequential iterated Prisoner’s Dilemma game in which confederates reciprocated fairly or unfairly, inducing liking or disliking.
  • In an empathy-for-pain fMRI task, subjects observed cues indicating that they, the fair player, or the unfair player would receive low or high electrical stimulation; each 12-s trial included a cue followed after 6 s by a circle indicating stimulation onset.
  • fMRI data were acquired on a 1.5-T Siemens Sonata scanner and analyzed in SPM2 using an event-related model with a 2 × 3 × 2 factorial design (pain vs no pain; self, fair, unfair; male vs female subject), random-effects group analyses, conjunction/masking, and regression analyses; results are reported at P < 0.005 uncorrected in a priori regions of interest.

Limitations

  • The paper states that further experiments are needed to confirm the gender specificity of the effect.
  • The paper notes that the experimental design may have favoured men because the punishment modality involved physical threat rather than psychological or financial threat; alternatively, the findings could indicate a predominant role for males in maintaining justice and punishing norm violation.
  • Evident from the text: the sample was small (32 subjects), several key results are reported at uncorrected thresholds within a priori regions of interest, and the gender analysis is binary and based on male/female subject groups.

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Crossref · 10.1038/nature04271

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  • It may state two separate claims as one. 8
  • Probably not a substantial claim. 11
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  • The paper relies on this without support.

    The modulation of empathic neural responses by the social relations between individuals is unknown.

    “However, it is unclear whether or how these responses are modulated by the social relations between individuals.”
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Metadata

Authors
Singer, T., Seymour, B., O'Doherty, J. P., Stephan, K. E., Dolan, R. J., & Frith, C. D.
Affiliations
  • University College London (GB)
  • Wellcome Trust (GB)
Corresponding author
Singer, Tania
Venue
Nature
Published
2006-01
Volume
439
Issue
7075
Pages
466-469
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2098425678
Cited by
1,726
References
30
Citations by year
2026: 28 · 2025: 33 · 2024: 51 · 2023: 67 · 2022: 57 · 2021: 65 · 2020: 139 · 2019: 88 · 2018: 91 · 2017: 74 · 2016: 93 · 2015: 105 · 2014: 98 · 2013: 111 · 2012: 100
FWCI
139.81
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
  • PubMed Central (acceptedVersion)
  • CaltechAUTHORS (California Institute of Technology) (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • UCL Discovery (University College London) (submittedVersion)
  • Max Planck Digital Library (submittedVersion, other-oa)
  • Max Planck Digital Library (submittedVersion)
  • Cambridge University Engineering Department Publications Database (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • Wellcome Trust (078865)
  • Medical Research Council
Topics
  • Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
  • Social Sciences › Economics, Econometrics and Finance › Economics and Econometrics › Experimental Behavioral Economics Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Keywords
empathy, perceived fairness, social preferences, schadenfreude, altruistic punishment, revenge, sex differences, anterior cingulate cortex, reward processing, economic games, corporal punishment
MeSH terms
Brain, Empathy, Female, Game Theory, Humans, Learning, Magnetic Resonance Imaging, Male, Nucleus Accumbens, Pain, Photic Stimulation, Punishment, Reward, Sex Characteristics, Social Justice

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