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.

Interactions between decision making and performance monitoring within prefrontal cortex

Nature Neuroscience volume 7, pages 1259–1265 (2004)Cite this article

Abstract

Our ability to judge the consequences of our actions is central to rational decision making. A large body of evidence implicates primate prefrontal regions in the regulation of this ability. It has proven extremely difficult, however, to separate functional areas in the frontal lobes. Using functional magnetic resonance imaging, we demonstrate complementary and reciprocal roles for the human orbitofrontal (OFC) and dorsal anterior cingulate cortices (ACd) in monitoring the outcome of behavior. Activation levels in these regions were negatively correlated, with activation increasing in the ACd and decreasing in the OFC when the selected response was the result of the participant's own decision. The pattern was reversed when the selected response was guided by the experimenter rather than the participant. These results indicate that the neural mechanisms underlying the way we assess the consequences of choices differ depending on whether we are told what to do or are able to exercise our volition.

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

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

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

Figure 1: Experimental design.
Figure 2: Mean switch costs across subjects (and their standard errors) for trials 1 and 2 (T1 and T2) after the cues in Experiment 1.
Figure 3: Monitoring the outcome of freely chosen actions.
Figure 4: Monitoring the outcome of externally guided actions.
Figure 5
Figure 6: Representation of the activation common to both of the feedback monitoring conditions: GUESSSw–St − INSTRUCTEDSw–St and FIXEDSw–St − INSTRUCTEDSw–St comparisons.
Figure 7: Mean switch costs across subjects (and their standard errors) for trials 1 and 2 (T1 and T2) after the cues in Experiment 2.
Figure 8: Activations and effect sizes in Experiment 2, investigating the contributions of decision making and performance monitoring to ACd activation.

References

  1. Ito, S., Stuphorn, V., Brown, J.W. & Schall, J.D. Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302, 120–122 (2003).

    Article  CAS  Google Scholar 

  2. Paus, T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat. Rev. Neurosci. 2, 417–424 (2001).

    Article  CAS  Google Scholar 

  3. 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 

  4. Elliott, R., Friston, K.J. & Dolan, R.J. Dissociable neural responses in human reward systems. J. Neurosci. 20, 6159–6165 (2000).

    Article  CAS  Google Scholar 

  5. Berns, G.S., McClure, S.M., Pagnoni, G. & Montague, P.R. Predictability modulates human brain response to reward. J. Neurosci. 21, 2793–2798 (2001).

    Article  CAS  Google Scholar 

  6. O'Doherty, J., Critchley, H., Deichmann, R. & Dolan, R.J. Dissociating valence of outcome from behavioral control in human orbital and ventral prefrontal cortices. J. Neurosci. 23, 7931–7939 (2003).

    Article  CAS  Google Scholar 

  7. Botvinick, M.M., Braver, T.S., Barch, D.M., Carter, C.S. & Cohen, J.D. Conflict monitoring and cognitive control. Psychol. Rev. 108, 624–652 (2001).

    Article  CAS  Google Scholar 

  8. Holroyd, C.B. & Coles, M.G. The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol. Rev. 109, 679–709 (2002).

    Article  Google Scholar 

  9. O'Doherty, J., Kringelbach, M.L., Rolls, E.T., Hornak, J. & Andrews, C. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat. Neurosci. 4, 95–102 (2001).

    Article  CAS  Google Scholar 

  10. Kringelbach, M.L. & Rolls, E.T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog. Neurobiol. 72, 341–372 (2004).

    Article  Google Scholar 

  11. Shidara, M. & Richmond, B.J. Anterior cingulate: single neuronal signals related to degree of reward expectancy. Science 296, 1709–1711 (2002).

    Article  Google Scholar 

  12. 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 

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

    Article  CAS  Google Scholar 

  14. Shima, K. & Tanji, J. Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282, 1335–1338 (1998).

    Article  CAS  Google Scholar 

  15. Procyk, E., Tanaka, Y.L. & Joseph, J.P. Anterior cingulate activity during routine and non-routine sequential behaviors in macaques. Nat. Neurosci. 3, 502–508 (2000).

    Article  CAS  Google Scholar 

  16. Hadland, K.A., Rushworth, M.F., Gaffan, D. & Passingham, R.E. The anterior cingulate and reward-guided selection of actions. J. Neurophysiol. 89, 1161–1164 (2003).

    Article  CAS  Google Scholar 

  17. Saxena, S., Brody, A.L., Schwartz, J.M. & Baxter, L.R. Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. Br. J. Psychiatry suppl. 35, 26–37 (1998).

    Article  Google Scholar 

  18. Frith, C.D., Blakemore, S. & Wolpert, D.M. Explaining the symptoms of schizophrenia: abnormalities in the awareness of action. Brain Res. Brain Res. Rev. 31, 357–363 (2000).

    Article  CAS  Google Scholar 

  19. Duncan, J. & Owen, A.M. Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci. 23, 475–483 (2000).

    Article  CAS  Google Scholar 

  20. Koski, L. & Paus, T. Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis. Exp. Brain Res. 133, 55–65 (2000).

    Article  CAS  Google Scholar 

  21. Frith, C.D., Friston, K., Liddle, P.F. & Frackowiak, R.S. Willed action and the prefrontal cortex in man: a study with PET. Proc. R. Soc. Lond. B 244, 241–246 (1991).

    Article  CAS  Google Scholar 

  22. Rushworth, M.F., Hadland, K.A., Paus, T. & Sipila, P.K. Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study. J. Neurophysiol. 87, 2577–2592 (2002).

    Article  CAS  Google Scholar 

  23. Jueptner, M., Frith, C.D., Brooks, D.J., Frackowiak, R.S. & Passingham, R.E. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J. Neurophysiol. 77, 1325–1337 (1997).

    Article  CAS  Google Scholar 

  24. 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 

  25. Picard, N. & Strick, P.L. Motor areas of the medial wall: a review of their location and functional activation. Cereb. Cortex 6, 342–353 (1996).

    Article  CAS  Google Scholar 

  26. Morecraft, R.J. & Van Hoesen, G.W. Convergence of limbic input to the cingulate motor cortex in the rhesus monkey. Brain Res. Bull. 45, 209–232 (1998).

    Article  CAS  Google Scholar 

  27. Bates, J.F. & Goldman-Rakic, P.S. Prefrontal connections of medial motor areas in the rhesus monkey. J. Comp. Neurol. 336, 211–228 (1993).

    Article  CAS  Google Scholar 

  28. Dum, R.P. & Strick, P.L. The origin of corticospinal projections from the premotor areas in the frontal lobe. J. Neurosci. 11, 667–689 (1991).

    Article  CAS  Google Scholar 

  29. Bush, G. et al. Dorsal anterior cingulate cortex: A role in reward-based decision making. Proc. Natl Acad. Sci. USA 99, 523–528 (2002).

    Article  CAS  Google Scholar 

  30. Ullsperger, M. & Von Cramon, D.Y. Error monitoring using external feedback: specific roles of the habenular complex, the reward system, and the cingulate motor area revealed by functional magnetic resonance imaging. J. Neurosci. 23, 4308–4314 (2003).

    Article  CAS  Google Scholar 

  31. Knutson, B., Adams, C.M., Fong, G.W. & Hommer, D. Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J. Neurosci. 21, RC159 (2001).

    Article  CAS  Google Scholar 

  32. Tricomi, E.M., Delgado, M.R. & Fiez, J.A. Modulation of caudate activity by action contingency. Neuron 41, 281–292 (2004).

    Article  CAS  Google Scholar 

  33. Matsumoto, K., Suzuki, W. & Tanaka, K. Neuronal correlates of goal-based motor selection in the prefrontal cortex. Science 301, 229–232 (2003).

    Article  CAS  Google Scholar 

  34. Ongur, D., Ferry, A.T. & Price, J.L. Architectonic subdivision of the human orbital and medial prefrontal cortex. J. Comp. Neurol. 460, 425–449 (2003).

    Article  Google Scholar 

  35. Chiavaras, M.M. & Petrides, M. Orbitofrontal sulci of the human and macaque monkey brain. J. Comp. Neurol. 422, 35–54 (2000).

    Article  CAS  Google Scholar 

  36. Carmichael, S.T. & Price, J.L. Sensory and premotor connections of the orbital and medial prefrontal cortex of macaque monkeys. J. Comp. Neurol. 363, 642–664 (1995).

    Article  CAS  Google Scholar 

  37. O'Doherty, J.P., Dayan, P., Friston, K., Critchley, H. & Dolan, R.J. Temporal difference models and reward-related learning in the human brain. Neuron 38, 329–337 (2003).

    Article  CAS  Google Scholar 

  38. Nobre, A.C., Coull, J.T., Frith, C.D. & Mesulam, M.M. Orbitofrontal cortex is activated during breaches of expectation in tasks of visual attention. Nat. Neurosci. 2, 11–12 (1999).

    Article  CAS  Google Scholar 

  39. Petrides, M., Alivisatos, B. & Frey, S. Differential activation of the human orbital, mid-ventrolateral, and mid-dorsolateral prefrontal cortex during the processing of visual stimuli. Proc. Natl Acad. Sci. USA 99, 5649–5654 (2002).

    Article  CAS  Google Scholar 

  40. Thaler, D., Chen, Y.C., Nixon, P.D., Stern, C.E. & Passingham, R.E. The functions of the medial premotor cortex. I. Simple learned movements. Exp. Brain Res. 102, 445–460 (1995).

    Article  CAS  Google Scholar 

  41. Kremer, S., Chassagnon, S., Hoffmann, D., Benabid, A.L. & Kahane, P. The cingulate hidden hand. J. Neurol. Neurosurg. Psychiatry 70, 264–265 (2001).

    Article  CAS  Google Scholar 

  42. Toni, I., Rushworth, M.F. & Passingham, R.E. Neural correlates of visuomotor associations. Spatial rules compared with arbitrary rules. Exp. Brain Res. 141, 359–369 (2001).

    Article  CAS  Google Scholar 

  43. Paus, T., Petrides, M., Evans, A.C. & Meyer, E. Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J. Neurophysiol. 70, 453–469 (1993).

    Article  CAS  Google Scholar 

  44. Ferry, A.T., Ongur, D., An, X. & Price, J.L. Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J. Comp. Neurol. 425, 447–470 (2000).

    Article  CAS  Google Scholar 

  45. Wilson, J.L. et al. Fast, fully automated global and local magnetic field optimization for fMRI of the human brain. Neuroimage 17, 967–976 (2002).

    Article  Google Scholar 

  46. Jenkinson, M., Bannister, P., Brady, M. & Smith, S. Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17, 825–841 (2002).

    Article  Google Scholar 

  47. Jenkinson, M. & Smith, S. A global optimisation method for robust affine registration of brain images. Med. Image Anal. 5, 143–156 (2001).

    Article  CAS  Google Scholar 

  48. Woolrich, M.W., Ripley, B.D., Brady, M. & Smith, S.M. Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage 14, 1370–1386 (2001).

    Article  CAS  Google Scholar 

  49. Friston, K.J., Worsley, K.J., Frackowiak, R.S., Mazziotta, J.C. & Evans, A.C. Assessing the significance of focal activations using their spatial extent. Hum. Brain Mapp. 1, 214–220 (1994).

    Google Scholar 

  50. Forman, S.D. et al. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33, 636–647 (1995).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the UK Medical Research Council and a Wellcome Trust Prize Studentship to M.E.W. We would like to thank P. Hobden, S. Hudsen and H. Johansen-Berg for radiography, and S. Smith, M. Jenkinson, C. Beckmann and T. Behrens for advice about analysis and registration.

Author information

Authors and Affiliations

  1. Department of Experimental Psychology, South Parks Road, Oxford, OX1 3UD, England, UK

    Mark E Walton, Joseph T Devlin & Matthew F S Rushworth

  2. Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), John Radcliffe Hospital, Headington, Oxford, OX3 9DU, England, UK

    Mark E Walton, Joseph T Devlin & Matthew F S Rushworth

Authors
  1. Mark E Walton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joseph T Devlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Matthew F S Rushworth
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mark E Walton.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Walton, M., Devlin, J. & Rushworth, M. Interactions between decision making and performance monitoring within prefrontal cortex. Nat Neurosci 7, 1259–1265 (2004). https://doi.org/10.1038/nn1339

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1339

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