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Moral transgressions corrupt neural representations of value

Nature Neuroscience volume 20, pages 879–885 (2017)Cite this article

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Abstract

Moral systems universally prohibit harming others for personal gain. However, we know little about how such principles guide moral behavior. Using a task that assesses the financial cost participants ascribe to harming others versus themselves, we probed the relationship between moral behavior and neural representations of profit and pain. Most participants displayed moral preferences, placing a higher cost on harming others than themselves. Moral preferences correlated with neural responses to profit, where participants with stronger moral preferences had lower dorsal striatal responses to profit gained from harming others. Lateral prefrontal cortex encoded profit gained from harming others, but not self, and tracked the blameworthiness of harmful choices. Moral decisions also modulated functional connectivity between lateral prefrontal cortex and the profit-sensitive region of dorsal striatum. The findings suggest moral behavior in our task is linked to a neural devaluation of reward realized by a prefrontal modulation of striatal value representations.

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Figure 1: Moral decision task and behavioral results.
Figure 2: Moral transgressions modulate corticostriatal responses to profit.
Figure 3: Blame computation in LPFC.
Figure 4: Corticostriatal connectivity during the exercise of moral choices.

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Acknowledgements

We thank E. Boorman, A. de Berker, L. Hunt, M. Klein-Flugge, C. Mathys, R. Rutledge, B. Seymour, P. Smittenaar, G. Story, I. Vlaev and J. Winston for feedback. M.J.C. was supported by a Sir Henry Wellcome Postdoctoral Fellowship (092217/Z/10/Z) and a Wellcome Trust Institutional Strategic Support Fund grant. J.Z.S. was supported by a Wellcome Trust Society and Ethics studentship (104980/Z/14/Z). Z.K.-N. was supported by a Joint Initiative on Computational Psychiatry and Ageing Research between the Max Planck Society and University College London. P.D. is funded by the Gatsby Charitable Foundation. R.J.D. holds a Wellcome Trust Senior Investigator Award (098362/Z/12/Z). The Max Planck UCL Centre is a joint initiative supported by UCL and the Max Planck Society. The Wellcome Trust Centre for Neuroimaging, where scanning was carried out, is supported by core funding from the Wellcome Trust (091593/Z/10/Z).

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Authors and Affiliations

  1. Department of Experimental Psychology, University of Oxford, Oxford, UK

    Molly J Crockett & Jenifer Z Siegel

  2. Department of Psychology, Yale University, New Haven, Connecticut, USA

    Molly J Crockett

  3. Max Planck–University College London Centre for Computational Psychiatry and Ageing, London, UK

    Zeb Kurth-Nelson & Raymond J Dolan

  4. Wellcome Trust Centre for Neuroimaging, University College London, London, UK

    Zeb Kurth-Nelson & Raymond J Dolan

  5. Gatsby Computational Neuroscience Unit, University College London, London, UK

    Peter Dayan

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Contributions

M.J.C. conceived the study. M.J.C., J.Z.S., Z.K.-N., P.D. and R.J.D. designed the study. M.J.C. and J.Z.S. collected behavioral and fMRI data. M.J.C., J.Z.S., Z.K.-N. and P.D. analyzed the data. M.J.C. wrote the manuscript with edits from J.Z.S., Z.K.-N., P.D. and R.J.D.

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Correspondence to Molly J Crockett.

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Integrated supplementary information

Supplementary Figure 1 Blame judgment task.

Participants viewed others’ decisions and were asked to rate them on a scale from blameworthy to praiseworthy. Across trials we independently manipulated the amounts of profit and pain resulting from choices.

Supplementary Figure 2 Moral transgressions modulate relative chosen value signal in vmPFC.

(a) The model-derived subjective value of the chosen option, relative to the unchosen option, was correlated positively with BOLD responses in a widespread network including vmPFC (k=1157, p<0.0001), mid-posterior cingulate (PFWE <0.0001), precuneus (PFWE <0.0001), bilateral clusters encompassing amygdala, striatum and insula (PFWE <0.0001). Chosen relative to unchosen subjective value was correlated negatively with BOLD responses in mid-cingulate cortex and anterior insula (PFWE =0.0002). All results whole brain familywise error corrected at the cluster level after voxel-wise thresholding at p<0.001. Image displayed at p < 0.005, uncorrected to show extent of activation. (b) The value-sensitive region of vmPFC (circled in a) showed reduced sensitivity to the value of the harmful option in the other condition relative to the self condition (t(27)=2.51, p=0.019). *P < 0.05; n.s., nonsignificant. Error bars depict s.e.m.

Supplementary Figure 3 Neural representation of pain is uncorrelated with moral behavior.

(a) At choice onset, left TPJ activity positively correlated with the relative amount of pain a harmful choice could inflict on others, but not self (Δsother > Δsself, mean signal extracted from independently defined ROI in TPJ, t(27) = 2.61, p = 0.015). Image displayed at p<0.005, uncorrected to show extent of activation. (b) Parameter estimates for Δsother and Δsself extracted from ROI in TPJ. At choice onset, left TPJ activity positively correlated with Δsother (t(27) = 2.27, p = 0.031), but not Δsself (t(27) = -0.30, p = 0.77); difference Δsother > Δsself, t(27) = 2.61, p = 0.015). (c) Differential response to self vs. others’ pain in TPJ was uncorrelated with individual differences in moral preferences (r=-0.14, 95% CI=[-0.46 0.26]). (d) At choice onset, ACC activity positively correlated with the relative amount of pain a harmful choice could inflict on both self and others (Δsother ∩ Δsself, mean signal extracted from independently defined ROI in ACC, t(27) = 2.56, p = 0.016). Image displayed at p<0.005, uncorrected to show extent of activation. (e) Parameter estimates for Δsother and Δsself extracted from ROI in ACC. At choice onset, ACC activity positively correlated with Δsself (t(27) = 3.35, p = 0.002) but not Δsother (t(27) = 0.77, p = 0.45). ACC tended to respond more strongly to pain for self than other (t(27) = -1.91, p = 0.067). (f) Differential response to pain for self vs others in ACC was uncorrelated with individual differences in moral preferences (robust correlation, r=0.09, 95% CI=[-0.32 0.47]). Error bars depict s.e.m. *P < 0.05; **P < 0.01; n.s., nonsignificant; n.s.t., nonsignificant trend.

Supplementary Figure 4 Corticostriatal connectivity during moral decisions and value sensitivity in DS.

(a) For illustrative purposes we display parameter estimates for LPFC-DS connectivity during choices to help others, harm others, and help self, extracted from the DS cluster depicted in Fig. 4a. We note that this figure is purely illustrative, and we confine our inferences solely to those arising out of a comparison between conditions (which were significant in a whole brain analysis). (b) The extent to which DS activity was sensitive to relative chosen value predicted the degree of negative connectivity between DS and LPFC during moral choices (robust correlation, r =-0.51, 95% CI [-0.73 -0.14]). Error bars depict s.e.m.

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Crockett, M., Siegel, J., Kurth-Nelson, Z. et al. Moral transgressions corrupt neural representations of value. Nat Neurosci 20, 879–885 (2017). https://doi.org/10.1038/nn.4557

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