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.

Evaluating self-generated decisions in frontal pole cortex of monkeys

Abstract

The frontal pole cortex (FPC) expanded markedly during human evolution, but its function remains uncertain in both monkeys and humans. Accordingly, we examined single-cell activity in this area. On every trial, monkeys decided between two response targets on the basis of a 'stay' or 'shift' cue. Feedback followed at a fixed delay. FPC cells did not encode the monkeys' decisions when they were made, but did so later on, as feedback approached. This finding indicates that the FPC is involved in monitoring or evaluating decisions. Using a control task and delayed feedback, we found that decision coding lasted until feedback only when the monkeys combined working memory with sensory cues to 'self-generate' decisions, as opposed to when they simply followed trial-by-trial instructions. A role in monitoring or evaluating self-generated decisions could account for FPC's expansion during human evolution.

Your institute does not have access to this article

Relevant articles

Open Access articles citing this article.

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Task and cues.
Figure 2: Decision-selective activity in the visually cued strategy task.
Figure 3: Decision-selective activity by task period.
Figure 4: Population activity on error trials.
Figure 5: Effect of delayed feedback.
Figure 6: Decision-selective activity in the fluid-cued strategy task.
Figure 7: Activity in the delayed-response task.
Figure 8: Recording locations.

References

  1. Walker, A.E. A cytoarchitectual study of the prefrontal areas of the macaque monkey. J. Comp. Neurol. 73, 59–86 (1940).

    Article  Google Scholar 

  2. Ramnani, N. & Owen, A.M. Anterior prefrontal cortex: insights into function from anatomy and neuroimaging. Nat. Rev. Neurosci. 5, 184–194 (2004).

    CAS  Article  Google Scholar 

  3. Burgess, P.W., Simons, J.S., Dumontheil, I. & Gilbert, S.J. The gateway hypothesis of rostral prefrontal cortex (area 10) function, in Measuring the Mind: Speed, Control, and Age (eds Duncan, J., McLeod, P. & Phillips, L.) 215–246 (Oxford University Press, Oxford, 2009).

  4. Ongür, 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 

  5. Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K. & Van Hoesen, G.W. Prefrontal cortex in humans and apes: a comparative study of area 10. Am. J. Phys. Anthropol. 114, 224–241 (2001).

    CAS  Article  Google Scholar 

  6. Jones, E.G. & Powell, T.P.S. An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93, 793–820 (1970).

    CAS  Article  Google Scholar 

  7. 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).

    CAS  Article  Google Scholar 

  8. Petrides, M. & Pandya, D.N. Efferent association pathways from the rostral prefrontal cortex in the macaque monkey. J. Neurosci. 27, 11573–11586 (2007).

    CAS  Article  Google Scholar 

  9. Hagmann, P. et al. Mapping the structural core of human cerebral cortex. PLoS Biol. 6, e159 (2008).

    Article  Google Scholar 

  10. Jacobs, B. et al. Regional dendritic and spine variation in human cerebral cortex: a quantitative Golgi study. Cereb. Cortex 11, 558–571 (2001).

    CAS  Article  Google Scholar 

  11. Sakai, K. Task set and prefrontal cortex. Annu. Rev. Neurosci. 31, 219–245 (2008).

    CAS  Article  Google Scholar 

  12. Okuda, J. et al. Differential involvement of regions of rostral prefrontal cortex (Brodmann area 10) in time- and event-based prospective memory. Int. J. Psychophysiol. 64, 233–246 (2007).

    Article  Google Scholar 

  13. McClure, S.M., Ericson, K.M., Laibson, D.I., Loewenstein, G. & Cohen, J.D. Time discounting for primary rewards. J. Neurosci. 27, 5796–5804 (2007).

    CAS  Article  Google Scholar 

  14. Koechlin, E., Basso, G., Pietrini, P., Panzer, S. & Grafman, J. The role of the anterior prefrontal cortex in human cognition. Nature 399, 148–151 (1999).

    CAS  Article  Google Scholar 

  15. Daw, N.D., O'Doherty, J.P., Dayan, P., Seymour, B. & Dolan, R.J. Cortical substrates for exploratory decisions in humans. Nature 441, 876–879 (2006).

    CAS  Article  Google Scholar 

  16. Soon, C.S., Brass, M., Heinze, H.J. & Haynes, J.D. Unconscious determinants of free decisions in the human brain. Nat. Neurosci. 11, 543–545 (2008).

    CAS  Article  Google Scholar 

  17. Ramnani, N., Elliott, R., Athwal, B.S. & Passingham, R.E. Prediction error for free monetary reward in the human prefrontal cortex. Neuroimage 23, 777–786 (2004).

    CAS  Article  Google Scholar 

  18. Boorman, E.D., Behrens, T.E.J., Woolrich, M.W. & Rushworth, M.F.S. 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).

    CAS  Article  Google Scholar 

  19. Burgess, P.W., Dumontheil, I. & Gilbert, S.J. The gateway hypothesis of rostral prefrontal cortex (area 10) function. Trends Cogn. Sci. 11, 290–298 (2007).

    Article  Google Scholar 

  20. Kroger, J.K. et al. Recruitment of anterior dorsolateral prefrontal cortex in human reasoning: a parametric study of relational complexity. Cereb. Cortex 12, 477–485 (2002).

    Article  Google Scholar 

  21. Bunge, S.A., Helskog, E.H. & Wendelken, C. Left, but not right, rostrolateral prefrontal cortex meets a stringent test of the relational integration hypothesis. Neuroimage 46, 338–342 (2009).

    Article  Google Scholar 

  22. Christoff, K., Ream, J.M., Geddes, L.P. & Gabrieli, J.D. Evaluating self-generated information: anterior prefrontal contributions to human cognition. Behav. Neurosci. 117, 1161–1168 (2003).

    Article  Google Scholar 

  23. Zysset, S., Huber, O., Ferstl, E. & von Cramon, D.Y. The anterior frontomedian cortex and evaluative judgment: an fMRI study. Neuroimage 15, 983–991 (2002).

    Article  Google Scholar 

  24. Ganis, G., Kosslyn, S.M., Stose, S., Thompson, W.L. & Yurgelun-Todd, D.A. Neural correlates of different types of deception: An fMRI investigation. Cereb. Cortex 13, 830–836 (2003).

    CAS  Article  Google Scholar 

  25. Karim, A.A. et al. The truth about lying: Inhibition of the anterior prefrontal cortex improves deceptive behavior. Cereb. Cortex published online, doi:10.1093/cercor/bhp090 (14 May 2009).

  26. Mitz, A.R., Tsujimoto, S., Maclarty, A.J. & Wise, S.P. A method for recording single-cell activity in the frontal-pole cortex of macaque monkeys. J. Neurosci. Methods 177, 60–66 (2009).

    Article  Google Scholar 

  27. Genovesio, A., Brasted, P.J., Mitz, A.R. & Wise, S.P. Prefrontal cortex activity related to abstract response strategies. Neuron 47, 307–320 (2005).

    CAS  Article  Google Scholar 

  28. Genovesio, A., Brasted, P.J. & Wise, S.P . Representation of future and previous spatial goals by separate neural populations in prefrontal cortex. J. Neurosci. 26, 7305–7316 (2006).

    CAS  Article  Google Scholar 

  29. Tsujimoto, S., Genovesio, A. & Wise, S.P. Transient neuronal correlations underlying goal selection and maintenance in prefrontal cortex. Cereb. Cortex 18, 2748–2761 (2008).

    Article  Google Scholar 

  30. Wise, S.P. Forward frontal fields: phylogeny and fundamental function. Trends Neurosci. 31, 599–608 (2008).

    CAS  Article  Google Scholar 

  31. Pochon, J.B. et al. The neural system that bridges reward and cognition in humans: an fMRI study. Proc. Natl. Acad. Sci. USA 99, 5669–5674 (2002).

    CAS  Article  Google Scholar 

  32. Schall, J.D., Stuphorn, V. & Brown, J.W. Monitoring and control of action by the frontal lobes. Neuron 36, 309–322 (2002).

    CAS  Article  Google Scholar 

  33. Kiani, R. & Shadlen, M.N. Representation of confidence associated with a decision by neurons in the parietal cortex. Science 324, 759–764 (2009).

    CAS  Article  Google Scholar 

  34. Kepecs, A., Uchida, N., Zariwala, H.A. & Mainen, Z.F. Neural correlates, computation and behavioural impact of decision confidence. Nature 455, 227–231 (2008).

    CAS  PubMed  Google Scholar 

  35. Genovesio, A., Tsujimoto, S. & Wise, S.P. Encoding problem-solving strategies in prefrontal cortex: activity during strategic errors. Eur. J. Neurosci. 27, 984–990 (2008).

    Article  Google Scholar 

  36. van Duijvenvoorde, A.C.K., Zanolie, K., Rombouts, S.A., Raijmakers, M.E. & Crone, E.A. Evaluating the negative or valuing the positive? Neural mechanisms supporting feedback-based learning across development. J. Neurosci. 28, 9495–9503 (2008).

    CAS  Article  Google Scholar 

  37. Walsh, N.D. & Phillips, M.L. Interacting outcome retrieval, anticipation, and feedback processes in the human brain. Cereb. Cortex published online, doi:10.1093/cercor/bhp098 (8 May 2009).

  38. Lawrence, N.S., Jollant, F., O'Daly, O., Zelaya, F. & Phillips, M.L. Distinct roles of prefrontal cortical subregions in the Iowa gambling task. Cereb. Cortex 19, 1134–1143 (2009).

    Article  Google Scholar 

  39. Burgess, P.W. Function and localization within rostral prefrontal cortex (area 10). Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 887–899 (2007).

    Article  Google Scholar 

  40. Gilbert, S.J. et al. Functional specialization within rostral prefrontal cortex (area 10): a meta-analysis. J. Cogn. Neurosci. 18, 932–948 (2006).

    Article  Google Scholar 

  41. Mason, M.F. et al. Wandering minds: the default network and stimulus-independent thought. Science 315, 393–395 (2007).

    CAS  Article  Google Scholar 

  42. Gusnard, D.A., Akbudak, E., Shulman, G.L. & Raichle, M.E. Medial prefrontal cortex and self-referential mental activity: relation to a default mode of brain function. Proc. Natl. Acad. Sci. USA 98, 4259–4264 (2001).

    CAS  Article  Google Scholar 

  43. Christoff, K., Ream, J.M. & Gabrieli, J.D. Neural basis of spontaneous thought processes. Cortex 40, 623–630 (2004).

    Article  Google Scholar 

  44. Forstmann, B.U., Brass, M., Koch, I. & von Cramon, D.Y. Internally generated and directly cued task sets: an investigation with fMRI. Neuropsychologia 43, 943–952 (2005).

    Article  Google Scholar 

  45. Raichle, M.E. et al. A default mode of brain function. Proc. Natl. Acad. Sci. USA 98, 676–682 (2001).

    CAS  Article  Google Scholar 

  46. Bengtsson, S.L., Haynes, J.D., Sakai, K., Buckley, M.J. & Passingham, R.E. The representation of abstract task rules in the human prefrontal cortex. Cereb. Cortex 19, 1929–1936 (2009).

    Article  Google Scholar 

  47. Sakai, K. & Passingham, R.E. Prefrontal set activity predicts rule-specific neural processing during subsequent cognitive performance. J. Neurosci. 26, 1211–1218 (2006).

    CAS  Article  Google Scholar 

  48. Bunge, S.A. How we use rules to select actions: a review of evidence from cognitive neuroscience. Cogn. Affect. Behav. Neurosci. 4, 564–579 (2004).

    Article  Google Scholar 

  49. Mithen, S. The Prehistory of the Mind (Thames and Hudson, London, 1996).

  50. Mitz, A.R. A liquid-delivery device that provides precise reward control for neurophysiological and behavioral experiments. J. Neurosci. Methods 148, 19–25 (2005).

    Article  Google Scholar 

Download references

Acknowledgements

We thank S. Bunge, G. di Pellegrino, E. Murray, R. Passingham, N. Ramnani and P. Rudebeck for comments on drafts of this manuscript. A. Mitz, J. Fellows and P.-Y. Chen provided technical support. This work was supported by the Division of Intramural Research of the National Institute of Mental Health (Z01MH-01092) and by a Grant-in-Aid for Scientific Research on Innovative Areas (21119513) from the Ministry of Education, Culture, Sports, Science and Technology, Japan. S.T. was supported by a research fellowship from the Japan Society for the Promotion of Science.

Author information

Authors and Affiliations

Authors

Contributions

S.T. and S.P.W. conceived and designed the experiment. S.T. and A.G. performed the experiment and analyzed the data. S.T., A.G. and S.P.W. wrote the paper.

Corresponding author

Correspondence to Satoshi Tsujimoto.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–5 and Supplementary Tables 1–3 (PDF 1993 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Tsujimoto, S., Genovesio, A. & Wise, S. Evaluating self-generated decisions in frontal pole cortex of monkeys. Nat Neurosci 13, 120–126 (2010). https://doi.org/10.1038/nn.2453

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2453

Further reading

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