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:

Abstract reward and punishment representations in the human orbitofrontal cortex

Abstract

The orbitofrontal cortex (OFC) is implicated in emotion and emotion-related learning. Using event-related functional magnetic resonance imaging (fMRI), we measured brain activation in human subjects doing an emotion-related visual reversal-learning task in which choice of the correct stimulus led to a probabilistically determined 'monetary' reward and choice of the incorrect stimulus led to a monetary loss. Distinct areas of the OFC were activated by monetary rewards and punishments. Moreover, in these areas, we found a correlation between the magnitude of the brain activation and the magnitude of the rewards and punishments received. These findings indicate that one emotional involvement of the human orbitofrontal cortex is its representation of the magnitudes of abstract rewards and punishments, such as receiving or losing money.

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 design.
Figure 2: The results from the group random effects analysis across the nine subjects with a threshold at p < 0.005 (uncorrected) superimposed on the structural MRI scan of a single subject.
Figure 3
Figure 4: Results from the correlation analysis.
Figure 5: The mean percent change in BOLD signal from baseline across subjects for six different category ranges of reward and punishment, shown for the peak voxels from the subtraction analysis.
Figure 6: Comparison of rewards and punishments with control condition.

Similar content being viewed by others

References

  1. Damasio, A. R. Descartes' Error (Putnam, New York, 1994).

    Google Scholar 

  2. Anderson, S. W., Bechara, A., Damasio, H., Tranel, D. & Damasio, A. R. Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat. Neurosci. 2, 1032–1037 (1999).

    Article  CAS  Google Scholar 

  3. Rolls, E. T. The Brain and Emotion (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  4. Rolls, E. T., Hornak, J., Wade, D. & McGrath, J. Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. J. Neurol. Neurosurg. Psychiatry 57, 1518–1524 (1994).

    Article  CAS  Google Scholar 

  5. Bechara, A., Damasio, A. R., Damasio, H. & Anderson, S. W. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15 (1994).

    Article  CAS  Google Scholar 

  6. Bechara, A., Damasio, H., Tranel, D. & Damasio, A. R. Deciding advantageously before knowing the advantageous strategy. Science 275, 1293–1295 (1997).

    Article  CAS  Google Scholar 

  7. Iversen, S. D. & Mishkin, M. Perseverative interference in monkeys following selective lesions of the inferior prefrontal convexity. Exp. Brain Res. 11, 376–386 (1970).

    Article  CAS  Google Scholar 

  8. Jones, B. & Mishkin, M. Limbic lesions and the problem of stimuluS−reinforcement associations. Exp. Neurol. 36, 362–377 (1972).

    Article  CAS  Google Scholar 

  9. Meunier, M., Bachevalier, J. & Mishkin, M. Effects of orbital frontal and anterior cingulate lesions on object and spatial memory in rhesus monkeys. Neuropsychologia 35, 999–1015 (1997).

    Article  CAS  Google Scholar 

  10. Freedman, M., Black, S., Ebert, P. & Binns, M. Orbitofrontal function, object alternation and perseveration. Cereb. Cortex 8, 18–27 (1998).

    Article  CAS  Google Scholar 

  11. Rolls, E. T., Critchley, H. D., Mason, R. & Wakeman, E. A. Orbitofrontal cortex neurons: role in olfactory and visual association learning. J. Neurophysiol. 75, 1970–1981 (1996).

    Article  CAS  Google Scholar 

  12. Thut, G. et al. Activation of the human brain by monetary reward. Neuroreport 8, 1225–1228 (1997).

    Article  CAS  Google Scholar 

  13. Elliott, R., Frith, C. D. & Dolan, R. J. Differential neural response to positive and negative feedback in planning and guessing tasks. Neuropsychologia 35, 1395–1404 (1997).

    Article  CAS  Google Scholar 

  14. Buckner, R. L. Event-related fMRI and the hemodynamic response. Hum. Brain Mapp. 6, 373–377 (1998).

    Article  CAS  Google Scholar 

  15. Cavada, C., Company, T., Tejedor, J., Cruz Rizzolo, R. J. & Reinoso Suarez, F. The anatomical connections of the macaque monkey orbitofrontal cortex. A review. Cereb. Cortex 10, 220–242 (2000).

    Article  CAS  Google Scholar 

  16. Carmichael, S. T. & Price, J. L. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J. Comp. Neurol. 363, 615–641 (1995).

    Article  CAS  Google Scholar 

  17. Morecraft, R. J., Geula, C. & Mesulam, M. -M. Cytoarchitecture and neural afferents of orbitofrontal cortex in the brain of the monkey. J. Comp. Neurol. 232, 341–358 (1992).

    Article  Google Scholar 

  18. Carmichael, S. T. & Price, J. L. Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. J. Comp. Neurol. 371, 179–207 (1996).

    Article  CAS  Google Scholar 

  19. Konishi, S. et al. Transient activation of inferior prefrontal cortex during cognitive set shifting. Nat. Neurosci. 1, 80–84 (1998).

    Article  CAS  Google Scholar 

  20. Konishi, S., Nakajima, K., Uchida, I., Sekihara, K. & Miyashita, Y. No-go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging. Eur. J. Neurosci. 10, 1209–1213 (1998).

    Article  CAS  Google Scholar 

  21. Elliott, R., Dolan, R. J. & Frith, C. D. Dissociable functions in the medial and lateral orbitofrontal cortex: evidence from human neuroimaging studies. Cereb. Cortex 10, 308–317 (2000).

    Article  CAS  Google Scholar 

  22. Rolls, E. T. in The Frontal Lobes (eds. Stuss, D. T. & Knight, R. T.) (Oxford Univ. Press, Oxford, in press).

  23. Miezin, F. M., Maccotta, L., Ollinger, J. M., Petersen, S. E. & Buckner, R. L. Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage 11, 735–759 (2000).

    Article  CAS  Google Scholar 

  24. Francis, S. et al. The representation of the pleasantness of touch in the human brain, and its relation to taste and olfactory areas. Neuroreport 10, 453–459 (1999).

    Article  CAS  Google Scholar 

  25. Buckner, R. L. et al. Functional-anatomic study of episodic retrieval: II. Selective averaging of event-related fMRI trials to test the retrieval success hypothesis. Neuroimage 7, 163–175 (1998).

    Article  CAS  Google Scholar 

  26. Rolls, E. T. & Baylis, L. L. Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J. Neurosci. 14, 5437–5452 (1994).

    Article  CAS  Google Scholar 

  27. Rolls, E. T., Yaxley, S. & Sienkiewicz, Z. J. Gustatory responses of single neurons in the caudolateral orbitofrontal cortex of the macaque monkey. J. Neurophysiol. 64, 1055–1066 (1990).

    Article  CAS  Google Scholar 

  28. Rolls, E. T. & Tovee, M. J. Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. J. Neurophysiol. 73, 713–726 (1995).

    Article  CAS  Google Scholar 

  29. Rolls, E. T. The orbitofrontal cortex and reward. Cereb. Cortex 10, 284–294 (2000).

    Article  CAS  Google Scholar 

  30. Rees, G., Friston, K. & Koch, C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci. 3, 716–723 (2000).

    Article  CAS  Google Scholar 

  31. Davidson, R. J. Anterior cerebral asymmetry and the nature of emotion. Brain Cogn. 6, 245–268 (1992).

    Google Scholar 

  32. Dias, R., Robbins, T. & Roberts, A. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380, 69–72 (1996).

    Article  CAS  Google Scholar 

  33. Tremblay, L. & Schultz, W. Relative reward preference in primate orbitofrontal cortex. Nature 398, 704–708 (1999).

    Article  CAS  Google Scholar 

  34. O'Doherty, J. et al. Sensory-specific satiety-related olfactory activation of the human orbitofrontal cortex. Neuroreport 11, 893–897 (2000).

    Article  CAS  Google Scholar 

  35. Birn, R. M., Bandettini, P. A., Cox, R. W. & Shaker, R. Event-related fMRI of tasks involving brief motion. Hum. Brain Mapp. 7, 106–114 (1999).

    Article  CAS  Google Scholar 

  36. Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, Stuttgart, 1988).

    Google Scholar 

Download references

Acknowledgements

This research is funded by the MRC (to FMRIB), the MRC (to E.T.R.), the MRC IRC for Cognitive Neuroscience, the MRC, Oxford McDonnell- Pew Centre for Cognitive Neuroscience and Firmenich (to J.O.D.) and the Danish Research Agency, Aarhus, Denmark (to M.L.K.). We thank P. Matthews, S. Smith, P. Jezzard, S. Clare and I. Tracey for their help.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. T. Rolls.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Cite this article

O'Doherty, J., Kringelbach, M., Rolls, E. et al. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 4, 95–102 (2001). https://doi.org/10.1038/82959

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/82959

This article is cited by

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