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:

Dynamic routing of task-relevant signals for decision making in dorsolateral prefrontal cortex

Nature Neuroscience volume 18, pages 295–301 (2015)Cite this article

Subjects

Abstract

Neurons in the dorsolateral prefrontal cortex (DLPFC) encode a diverse array of sensory and mnemonic signals, but little is known about how this information is dynamically routed during decision making. We analyzed the neuronal activity in the DLPFC of monkeys performing a probabilistic reversal task where information about the probability and magnitude of reward was provided by the target color and numerical cues, respectively. The location of the target of a given color was randomized across trials and therefore was not relevant for subsequent choices. DLPFC neurons encoded signals related to both task-relevant and irrelevant features, but only task-relevant mnemonic signals were encoded congruently with choice signals. Furthermore, only the task-relevant signals related to previous events were more robustly encoded following rewarded outcomes. Thus, multiple types of neural signals are flexibly routed in the DLPFC so as to favor actions that maximize reward.

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: Behavioral task and performance.
Figure 2: Population summary and single-neuron examples for activity related to events in the previous trial.
Figure 3: Population summary and single-neuron examples for activity related to events in the current trial.
Figure 4: Population summary and single-neuron examples related to interaction effects.
Figure 5: Congruent coding of HVL and choice.
Figure 6: Effects of reward on task-relevant and task-irrelevant signals in the DLPFC.

Similar content being viewed by others

References

  1. Funahashi, S., Bruce, C.J. & Goldman-Rakic, P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J. Neurophysiol. 61, 331–349 (1989).

    Article  CAS  PubMed  Google Scholar 

  2. Lara, A.H. & Wallis, J.D. Executive control processes underlying multi-item working memory. Nat. Neurosci. 17, 876–883 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Romo, R., Brody, C.D., Hernández, A. & Lemus, L. Neuronal correlates of parametric working memory in the prefrontal cortex. Nature 399, 470–473 (1999).

    Article  CAS  PubMed  Google Scholar 

  4. Constantinidis, C., Franowicz, M.N. & Goldman-Rakic, P.S. The sensory nature of mnemonic representation in the primate prefrontal cortex. Nat. Neurosci. 4, 311–316 (2001).

    Article  CAS  PubMed  Google Scholar 

  5. Ó Scalaidhe, S.P., Wilson, F.A. & Goldman-Rakic, P.S. Areal segregation of face-processing neurons in prefrontal cortex. Science 278, 1135–1138 (1997).

    Article  PubMed  Google Scholar 

  6. Rao, S.C., Rainer, G. & Miller, E.K. Integration of what and where in the primate prefrontal cortex. Science 276, 821–824 (1997).

    Article  CAS  PubMed  Google Scholar 

  7. Miller, E.K. & Cohen, J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24, 167–202 (2001).

    Article  CAS  PubMed  Google Scholar 

  8. Tanji, J. & Hoshi, E. Role of the lateral prefrontal cortex in executive behavioral control. Physiol. Rev. 88, 37–57 (2008).

    Article  PubMed  Google Scholar 

  9. Lebedev, M.A., Messinger, A., Kralik, J.D. & Wise, S.P. Representation of attended versus remembered locations in prefrontal cortex. PLoS Biol. 2, e365 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Messinger, A., Lebedev, M.A., Kralik, J.D. & Wise, S.P. Multitasking of attention and memory functions in the primate prefrontal cortex. J. Neurosci. 29, 5640–5653 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Watanabe, M. Reward expectancy in primate prefrontal neurons. Nature 382, 629–632 (1996).

    Article  CAS  PubMed  Google Scholar 

  12. Leon, M.I. & Shadlen, M.N. Effect of expected reward magnitude on the response of neurons in the dorsolateral prefrontal cortex of the macaque. Neuron 24, 415–425 (1999).

    Article  CAS  PubMed  Google Scholar 

  13. Barraclough, D.J., Conroy, M.L. & Lee, D. Prefrontal cortex and decision making in a mixed-strategy game. Nat. Neurosci. 7, 404–410 (2004).

    Article  CAS  PubMed  Google Scholar 

  14. Kim, S., Hwang, J. & Lee, D. Prefrontal coding of temporally discounted values during intertemporal choice. Neuron 59, 161–172 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kim, S., Cai, X., Hwang, J. & Lee, D. Prefrontal and striatal activity related to values of objects and locations. Front. Neurosci. 6, 108 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Kennerley, S.W., Dahmubed, A.F., Lara, A.H. & Wallis, J.D. Neurons in the frontal lobe encode the value of multiple decision variables. J. Cogn. Neurosci. 21, 1162–1178 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Lauwereyns, J. et al. Responses to task-irrelevant visual features by primate prefrontal neurons. J. Neurophysiol. 86, 2001–2010 (2001).

    Article  CAS  PubMed  Google Scholar 

  18. Genovesio, A., Tsujimoto, S., Navarra, G., Falcone, R. & Wise, S.P. Autonomous encoding of irrelevant goals and outcomes by prefrontal cortex neurons. J. Neurosci. 34, 1970–1978 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Sutton, R.S. & Barto, A.G. Reinforcement Learning: An Introduction (MIT Press, 1998).

  20. Tobler, P.N., Fiorillo, C.D. & Schultz, W. Adaptive coding of reward value by dopamine neurons. Science 307, 1642–1645 (2005).

    Article  CAS  PubMed  Google Scholar 

  21. Knutson, B., Taylor, J., Kaufman, M., Peterson, R. & Glover, G. Distributed neural representation of expected value. J. Neurosci. 25, 4806–4812 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Yacubian, J. et al. Dissociable systems for gain- and loss-related value predictions and errors of prediction in the human brain. J. Neurosci. 26, 9530–9537 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tobler, P.N., Christopoulos, G.I., O'Doherty, J.P., Dolan, R.J. & Schultz, W. Neuronal distortions of reward probability without choice. J. Neurosci. 28, 11703–11711 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Christopoulos, G.I., Tobler, P.N., Bossaerts, P., Dolan, R.J. & Schultz, W. Neural correlates of value, risk, and risk aversion contributing to decision making under risk. J. Neurosci. 29, 12574–12583 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Venkatraman, V., Payne, J.W., Bettman, J.R., Luce, M.F. & Huettel, S.A. Separate neural mechanisms underlie choices and strategic preferences in risky decision making. Neuron 62, 593–602 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Berns, G.S. & Bell, E. Striatal topography of probability and magnitude information for decisions under uncertainty. Neuroimage 59, 3166–3172 (2012).

    Article  PubMed  Google Scholar 

  27. Donahue, C.H., Seo, H. & Lee, D. Cortical signals for rewarded actions and strategic exploration. Neuron 80, 223–234 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Histed, M.H., Pasupathy, A. & Miller, E.K. Learning substrates in the primate prefrontal cortex and striatum: sustained activity related to successful actions. Neuron 63, 244–253 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ito, M. & Doya, K. Validation of decision-making models and analysis of decision variables in the rat basal ganglia. J. Neurosci. 29, 9861–9874 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Daw, N.D., Niv, Y. & Dayan, P. Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat. Neurosci. 8, 1704–1711 (2005).

    Article  CAS  PubMed  Google Scholar 

  31. Hampton, A.N., Bossaerts, P. & O'Doherty, J.P. The role of the ventromedial prefrontal cortex in abstract state-based inference during decision making in humans. J. Neurosci. 26, 8360–8367 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lee, D., Seo, H. & Jung, M.W. Neural basis of reinforcement learning and decision making. Annu. Rev. Neurosci. 35, 287–308 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Gläscher, J., Daw, N., Dayan, P. & O'Doherty, J.P. States versus rewards: dissociable neural prediction error signals underlying model-based and model- free reinforcement learning. Neuron 66, 585–595 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Daw, N.D., Gershman, S.J., Seymour, B., Dayan, P. & Dolan, R.J. Model-based influences on humans' choices and striatal prediction errors. Neuron 69, 1204–1215 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Abe, H. & Lee, D. Distributed coding of actual and hypothetical outcomes in the orbital and dorsolateral prefrontal cortex. Neuron 70, 731–741 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Lee, S.W., Shimojo, S. & O'Doherty, J.P. Neural computations underlying arbitration between model-based and model-free learning. Neuron 81, 687–699 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Seo, H., Cai, X., Donahue, C.H. & Lee, D. Neural correlates of strategic reasoning during competitive games. Science 346, 340–343 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Asaad, W.F., Rainer, G. & Miller, E.K. Neural activity in the primate prefrontal cortex during associative learning. Neuron 21, 1399–1407 (1998).

    Article  CAS  PubMed  Google Scholar 

  39. Curtis, C.E. & Lee, D. Beyond working memory: the role of persistent activity in decision making. Trends Cogn. Sci. 14, 216–222 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Bernacchia, A., Seo, H., Lee, D. & Wang, X.-J. A reservoir of time constants for memory traces in cortical neurons. Nat. Neurosci. 14, 366–372 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Fuster, J.M., Bodner, M. & Kroger, J.K. Cross-modal and cross-temporal association in neurons of frontal cortex. Nature 405, 347–351 (2000).

    Article  CAS  PubMed  Google Scholar 

  44. Mante, V., Sussillo, D., Shenoy, K.V. & Newsome, W.T. Context-dependent computation by recurrent dynamics in prefrontal cortex. Nature 503, 78–84 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Chen, L.L. & Wise, S.P. Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. J. Neurophysiol. 73, 1101–1121 (1995).

    Article  CAS  PubMed  Google Scholar 

  46. Chen, L.L. & Wise, S.P. Evolution of directional preferences in the supplementary eye field during acquisition of conditional oculomotor associations. J. Neurosci. 16, 3067–3081 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Chen, L.L. & Wise, S.P. Conditional oculomotor learning: population vectors in the supplementary eye field. J. Neurophysiol. 78, 1166–1169 (1997).

    Article  CAS  PubMed  Google Scholar 

  48. Singer, A.C. & Frank, L.M. Rewarded outcomes enhance reactivation of experience in the hippocampus. Neuron 64, 910–921 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Rigotti, M. et al. The importance of mixed selectivity in complex cognitive tasks. Nature 497, 585–590 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Duncan, J. An adaptive coding model of neural function in prefrontal cortex. Nat. Rev. Neurosci. 2, 820–829 (2001).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank M. Hammond and P. Kurnath for technical support, and Z. Zhang for his help with the experiment. This study was supported by the National Institutes of Health (T32 NS007224 to C.H.D. and R01 DA029330 to D.L.).

Author information

Author notes

  1. Christopher H Donahue

    Present address: Present address: Gladstone Institute of Neurological Disease, San Francisco, California, USA.,

Authors and Affiliations

  1. Department of Neurobiology, Yale University School of Medicine, New Haven, Connecticut, USA

    Christopher H Donahue & Daeyeol Lee

  2. Kavli Institute for Neuroscience, Yale University School of Medicine, New Haven, Connecticut, USA

    Daeyeol Lee

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

    Daeyeol Lee

Authors
  1. Christopher H Donahue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daeyeol Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

C.H.D. and D.L. designed the experiments and wrote the manuscript. C.H.D. did the experiment and analyzed the data.

Corresponding author

Correspondence to Daeyeol Lee.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Anatomical distributions for neurons encoding HVL, PRL and choice.

Color symbols correspond to the neurons that showed significant modulations for each variable (n=226 neurons, both monkeys combined).

Supplementary information

Supplementary Text and Figures

Supplementary Figure 1 and Supplementary Table 1 (PDF 471 kb)

Supplementary Methods Checklist (PDF 397 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Donahue, C., Lee, D. Dynamic routing of task-relevant signals for decision making in dorsolateral prefrontal cortex. Nat Neurosci 18, 295–301 (2015). https://doi.org/10.1038/nn.3918

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3918

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