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.

  • Article
  • Published:

Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice

Nature Neuroscience volume 14, pages 1468–1474 (2011)Cite this article

Subjects

Abstract

Humans are noted for their capacity to over-ride self-interest in favor of normatively valued goals. We examined the neural circuitry that is causally involved in normative, fairness-related decisions by generating a temporarily diminished capacity for costly normative behavior, a 'deviant' case, through non-invasive brain stimulation (repetitive transcranial magnetic stimulation) and compared normal subjects' functional magnetic resonance imaging signals with those of the deviant subjects. When fairness and economic self-interest were in conflict, normal subjects (who make costly normative decisions at a much higher frequency) displayed significantly higher activity in, and connectivity between, the right dorsolateral prefrontal cortex (DLPFC) and the posterior ventromedial prefrontal cortex (pVMPFC). In contrast, when there was no conflict between fairness and economic self-interest, both types of subjects displayed identical neural patterns and behaved identically. These findings suggest that a parsimonious prefrontal network, the activation of right DLPFC and pVMPFC, and the connectivity between them, facilitates subjects' willingness to incur the cost of normative decisions.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Rejection rates.
Figure 2: Differential group activation in the right DLPFC: left TMS (unfair > fair) > right TMS (unfair > fair).
Figure 3: Differential group activation in pVMPFC: left TMS (unfair > fair) > right TMS (unfair > fair).
Figure 4: Treatment group differences in connectivity between right DLPFC and pVMPFC.

Similar content being viewed by others

References

  1. Boyd, R.T. & Richerson, P. The Origin and Evolution of Cultures (Oxford University Press, Oxford, 2005).

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

    Article  CAS  Google Scholar 

  3. Damasio, A.R. Descartes' Error: Emotion, Reason and the Human Brain (Hayrer Collins, New York, 1995).

  4. Shallice, T. & Burgess, P.W. Deficits in strategy application following frontal lobe damage in man. Brain 114, 727–741 (1991).

    Article  Google Scholar 

  5. Neary, D. et al. Frontotemporal lobar degeneration: a consensus on clinical diagnostic criteria. Neurology 51, 1546–1554 (1998).

    Article  CAS  Google Scholar 

  6. Miller, B.L., Darby, A., Benson, D.F., Cummings, J.L. & Miller, M.H. Aggressive, socially disruptive and antisocial behaviour associated with fronto-temporal dementia. Br. J. Psychiatry 170, 150–154 (1997).

    Article  CAS  Google Scholar 

  7. Moll, J. et al. Human fronto-mesolimbic networks guide decisions about charitable donation. Proc. Natl. Acad. Sci. USA 103, 15623–15628 (2006).

    Article  CAS  Google Scholar 

  8. Sanfey, A.G., Rilling, J.K., Aronson, J.A., Nystrom, L.E. & Cohen, J.D. The neural basis of economic decision-making in the Ultimatum Game. Science 300, 1755–1758 (2003).

    Article  CAS  Google Scholar 

  9. Harbaugh, W.T., Mayr, U. & Burghart, D.R. Neural responses to taxation and voluntary giving reveal motives for charitable donations. Science 316, 1622–1625 (2007).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  11. Baumgartner, T., Fischbacher, U., Feierabend, A., Lutz, K. & Fehr, E. The neural circuitry of a broken promise. Neuron 64, 756–770 (2009).

    Article  CAS  Google Scholar 

  12. Baumgartner, T., Gotte, L., Gugler, R. & Fehr, E. The mentalizing network orchestrates the impact of parochial altruism on social norm enforcement. Hum. Brain Mapp. published online, doi:10.1002/hbm.21298 (13 May 2011).

  13. 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. 30, 583–590 (2010).

    Article  CAS  Google Scholar 

  14. Tricomi, E., Rangel, A., Camerer, C.F. & O'Doherty, J.P. Neural evidence for inequality-averse social preferences. Nature 463, 1089–1091 (2010).

    Article  CAS  Google Scholar 

  15. Knoch, D., Gianotti, L.R., Baumgartner, T. & Fehr, E. A neural marker of costly punishment behavior. Psychol. Sci. 21, 337–342 (2010).

    Article  Google Scholar 

  16. Knoch, D., Pascual-Leone, A., Meyer, K., Treyer, V. & Fehr, E. Diminishing reciprocal fairness by disrupting the right prefrontal cortex. Science 314, 829–832 (2006).

    Article  CAS  Google Scholar 

  17. van 't Wout, M., Kahn, R.S., Sanfey, A.G. & Aleman, A. Repetitive transcranial magnetic stimulation over the right dorsolateral prefrontal cortex affects strategic decision-making. Neuroreport 16, 1849–1852 (2005).

    Article  Google Scholar 

  18. Knoch, D. et al. Studying the neurobiology of social interaction with transcranial direct current stimulation–the example of punishing unfairness. Cereb. Cortex 18, 1987–1990 (2008).

    Article  Google Scholar 

  19. Güth, W., Schmittberger, R. & Schwarze, B. An experimental analyses of ultimatum bargaining. J. Econ. Behav. Organ. 3, 367–388 (1982).

    Article  Google Scholar 

  20. Henrich, J. et al. In search of homo economicus: behavioral experiments in 15 small-scale societies. Am. Econ. Rev. 91, 73–78 (2001).

    Article  Google Scholar 

  21. Tabibnia, G., Satpute, A.B. & Lieberman, M.D. The sunny side of fairness: preference for fairness activates reward circuitry (and disregarding unfairness activates self-control circuitry). Psychol. Sci. 19, 339–347 (2008).

    Article  Google Scholar 

  22. Phillips, M.L. et al. A specific neural substrate for perceiving facial expressions of disgust. Nature 389, 495–498 (1997).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  24. Herwig, U. et al. Modulation of anticipatory emotion and perception processing by cognitive control. Neuroimage 37, 652–662 (2007).

    Article  Google Scholar 

  25. Plassmann, H., O'Doherty, J. & Rangel, A. Orbitofrontal cortex encodes willingness to pay in everyday economic transactions. J. Neurosci. 27, 9984–9988 (2007).

    Article  CAS  Google Scholar 

  26. 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. 28, 5623–5630 (2008).

    Article  CAS  Google Scholar 

  27. 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. 29, 12315–12320 (2009).

    Article  CAS  Google Scholar 

  28. Boorman, E.D., Behrens, T.E., Woolrich, M.W. & Rushworth, M.F. How green is the grass on the other side? Frontopolar cortex and the evidence in favor of alternative courses of action. Neuron 62, 733–743 (2009).

    Article  CAS  Google Scholar 

  29. Hare, T.A., Camerer, C.F. & Rangel, A. Self-control in decision-making involves modulation of the vmPFC valuation system. Science 324, 646–648 (2009).

    Article  CAS  Google Scholar 

  30. Kable, J.W. & Glimcher, P.W. The neural correlates of subjective value during intertemporal choice. Nat. Neurosci. 10, 1625–1633 (2007).

    Article  CAS  Google Scholar 

  31. Kable, J.W. & Glimcher, P.W. The neurobiology of decision: consensus and controversy. Neuron 63, 733–745 (2009).

    Article  CAS  Google Scholar 

  32. Montague, P.R. & Berns, G.S. Neural economics and the biological substrates of valuation. Neuron 36, 265–284 (2002).

    Article  CAS  Google Scholar 

  33. Robertson, E.M., Theoret, H. & Pascual-Leone, A. Studies in cognition: the problems solved and created by transcranial magnetic stimulation. J. Cogn. Neurosci. 15, 948–960 (2003).

    Article  CAS  Google Scholar 

  34. Baumgartner, T., Heinrichs, M., Vonlanthen, A., Fischbacher, U. & Fehr, E. Oxytocin shapes the neural circuitry of trust and trust adaptation in humans. Neuron 58, 639–650 (2008).

    Article  CAS  Google Scholar 

  35. Carter, C.S. et al. Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280, 747–749 (1998).

    Article  CAS  Google Scholar 

  36. Ridderinkhof, K.R., Ullsperger, M., Crone, E.A. & Nieuwenhuis, S. The role of the medial frontal cortex in cognitive control. Science 306, 443–447 (2004).

    Article  CAS  Google Scholar 

  37. Friston, K.J. et al. Psychophysiological and modulatory interactions in neuroimaging. Neuroimage 6, 218–229 (1997).

    Article  CAS  Google Scholar 

  38. Frith, U. & Frith, C.D. Development and neurophysiology of mentalizing. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 459–473 (2003).

    Article  Google Scholar 

  39. Van Overwalle, F. Social cognition and the brain: a meta-analysis. Hum. Brain Mapp. 30, 829–858 (2009).

    Article  Google Scholar 

  40. Blount, S. When social outcomes aren't fair: the effect of causal attributions on preferences. Organ. Behav. Hum. Decis. Process. 63, 131–144 (1995).

    Article  Google Scholar 

  41. Smith, D.V. et al. Distinct value signals in anterior and posterior ventromedial prefrontal cortex. J. Neurosci. 30, 2490–2495 (2010).

    Article  CAS  Google Scholar 

  42. Lieberman, M.D. & Cunningham, W.A. Type I and type II error concerns in fMRI research: re-balancing the scale. Soc. Cogn. Affect. Neurosci. 4, 423–428 (2009).

    Article  Google Scholar 

  43. Knoch, D., Schneider, F., Schunk, D., Hohmann, M. & Fehr, E. Disrupting the prefrontal cortex diminishes the human ability to build a good reputation. Proc. Natl. Acad. Sci. USA 106, 20895–20899 (2009).

    Article  CAS  Google Scholar 

  44. Koch, G. et al. rTMS evidence of different delay and decision processes in a fronto-parietal neuronal network activated during spatial working memory. Neuroimage 24, 34–39 (2005).

    Article  Google Scholar 

  45. Griskova, I., Ruksenas, O., Dapsys, K., Herpertz, S. & Hoppner, J. The effects of 10-Hz repetitive transcranial magnetic stimulation on resting EEG power spectrum in healthy subjects. Neurosci. Lett. 419, 162–167 (2007).

    Article  CAS  Google Scholar 

  46. Rossi, S., Hallett, M., Rossini, P.M. & Pascual-Leone, A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin. Neurophysiol. 120, 2008–2039 (2009).

    Article  Google Scholar 

  47. Eisenegger, C., Treyer, V., Fehr, E. & Knoch, D. Time-course of 'off-line' prefrontal rTMS effects: a PET study. Neuroimage 42, 379–384 (2008).

    Article  CAS  Google Scholar 

  48. Pruessmann, K.P., Weiger, M., Scheidegger, M.B. & Boesiger, P. SENSE: sensitivity encoding for fast MRI. Magn. Reson. Med. 42, 952–962 (1999).

    Article  CAS  Google Scholar 

  49. Maldjian, J.A., Laurienti, P.J., Kraft, R.A. & Burdette, J.H. An automated method for neuroanatomic and cytoarchitectonic atlas–based interrogation of fMRI data sets. Neuroimage 19, 1233–1239 (2003).

    Article  Google Scholar 

  50. Tzourio-Mazoyer, N. et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15, 273–289 (2002).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank C. Ruff, K.E. Stephan and A. Rangel for their helpful comments. This study is a part of the project on the foundations of norm compliance in the National Center of Competence in Affective Sciences. E.F. also acknowledges support from the Neurochoice Project of SystemsX, the Swiss Initiative for Systems Biology. D.K. acknowledges support from the Swiss National Science Foundation (grant no. PP00P1-123381).

Author information

Author notes

  1. Thomas Baumgartner and Daria Knoch: These authors contributed equally to this work.

Authors and Affiliations

  1. Department of Economics, Laboratory for Social and Neural Systems Research, University of Zurich, Zurich, Switzerland

    Thomas Baumgartner, Philine Hotz, Christoph Eisenegger & Ernst Fehr

  2. Department of Psychology, Laboratory for Social and Affective Neuroscience, University of Basel, Basel, Switzerland

    Thomas Baumgartner & Daria Knoch

  3. Department of Experimental Psychology, Behavioral and Clinical Neuroscience Institute, University of Cambridge, Cambridge, UK

    Christoph Eisenegger

Authors
  1. Thomas Baumgartner
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daria Knoch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philine Hotz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christoph Eisenegger
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ernst Fehr
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.B., D.K. and E.F. designed the study. T.B., D.K. and C.E. performed all of the experiments. T.B. and P.H. analyzed the data. T.B., D.K. and E.F. wrote the manuscript.

Corresponding authors

Correspondence to Thomas Baumgartner, Daria Knoch or Ernst Fehr.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7, Supplementary Tables 1–3, Supplementary Analysis 1 and 2, and Supplementary Discussion (PDF 2458 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Baumgartner, T., Knoch, D., Hotz, P. et al. Dorsolateral and ventromedial prefrontal cortex orchestrate normative choice. Nat Neurosci 14, 1468–1474 (2011). https://doi.org/10.1038/nn.2933

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2933

This article is cited by

Search

Advanced 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