Article | Published:

Double dissociation of value computations in orbitofrontal and anterior cingulate neurons

Nature Neuroscience 14, 1581–1589 (2011) | Download Citation

Subjects

Abstract

Damage to prefrontal cortex (PFC) impairs decision-making, but the underlying value computations that might cause such impairments remain unclear. Here we report that value computations are doubly dissociable among PFC neurons. Although many PFC neurons encoded chosen value, they used opponent encoding schemes such that averaging the neuronal population extinguished value coding. However, a special population of neurons in anterior cingulate cortex (ACC), but not in orbitofrontal cortex (OFC), multiplexed chosen value across decision parameters using a unified encoding scheme and encoded reward prediction errors. In contrast, neurons in OFC, but not ACC, encoded chosen value relative to the recent history of choice values. Together, these results suggest complementary valuation processes across PFC areas: OFC neurons dynamically evaluate current choices relative to recent choice values, whereas ACC neurons encode choice predictions and prediction errors using a common valuation currency reflecting the integration of multiple decision parameters.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

Rent or Buy

All prices are NET prices.

References

  1. 1.

    , , , & Optimal decision making and the anterior cingulate cortex. Nat. Neurosci. 9, 940–947 (2006).

  2. 2.

    et al. Frontal cortex subregions play distinct roles in choices between actions and stimuli. J. Neurosci. 28, 13775–13785 (2008).

  3. 3.

    , , , & Separable learning systems in the macaque brain and the role of orbitofrontal cortex in contingent learning. Neuron 65, 927–939 (2010).

  4. 4.

    et al. Dissociable components of rule-guided behavior depend on distinct medial and prefrontal regions. Science 325, 52–58 (2009).

  5. 5.

    et al. Separate value comparison and learning mechanisms in macaque medial and lateral orbitofrontal cortex. Proc. Natl. Acad. Sci. USA 107, 20547–20552 (2010).

  6. 6.

    Deciding how to decide: ventromedial frontal lobe damage affects information acquisition in multi-attribute decision making. Brain 129, 944–952 (2006).

  7. 7.

    , , , & Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nat. Neurosci. 7, 1370–1375 (2004).

  8. 8.

    , , & Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50, 7–15 (1994).

  9. 9.

    , & Interactions between decision making and performance monitoring within prefrontal cortex. Nat. Neurosci. 7, 1259–1265 (2004).

  10. 10.

    , , , & Cortical substrates for exploratory decisions in humans. Nature 441, 876–879 (2006).

  11. 11.

    , , , & Separate valuation subsystems for delay and effort decision costs. J. Neurosci. 30, 14080–14090 (2010).

  12. 12.

    & Choice, uncertainty and value in prefrontal and cingulate cortex. Nat. Neurosci. 11, 389–397 (2008).

  13. 13.

    & Neurons in the orbitofrontal cortex encode economic value. Nature 441, 223–226 (2006).

  14. 14.

    & Relative reward preference in primate orbitofrontal cortex. Nature 398, 704–708 (1999).

  15. 15.

    , , & Neurons in the frontal lobe encode the value of multiple decision variables. J. Cogn. Neurosci. 21, 1162–1178 (2009).

  16. 16.

    & Impact of expected reward on neuronal activity in prefrontal cortex, frontal and supplementary eye fields and premotor cortex. J. Neurophysiol. 90, 1766–1789 (2003).

  17. 17.

    & Coding of reward risk by orbitofrontal neurons is mostly distinct from coding of reward value. Neuron 68, 789–800 (2010).

  18. 18.

    & Behavioral and neural changes after gains and losses of conditioned reinforcers. J. Neurosci. 29, 3627–3641 (2009).

  19. 19.

    & Temporal filtering of reward signals in the dorsal anterior cingulate cortex during a mixed-strategy game. J. Neurosci. 27, 8366–8377 (2007).

  20. 20.

    & Neuronal activity in primate dorsolateral and orbital prefrontal cortex during performance of a reward preference task. Eur. J. Neurosci. 18, 2069–2081 (2003).

  21. 21.

    & Encoding of reward and space during a working memory task in the orbitofrontal cortex and anterior cingulate sulcus. J. Neurophysiol. 102, 3352–3364 (2009).

  22. 22.

    , & Prefrontal coding of temporally discounted values during intertemporal choice. Neuron 59, 161–172 (2008).

  23. 23.

    & The convergence of information about rewarding and aversive stimuli in single neurons. J. Neurosci. 29, 11471–11483 (2009).

  24. 24.

    et al. Expectations, gains, and losses in the anterior cingulate cortex. Cogn. Affect. Behav. Neurosci. 7, 327–336 (2007).

  25. 25.

    & Evaluating choices by single neurons in the frontal lobe: outcome value encoded across multiple decision variables. Eur. J. Neurosci. 29, 2061–2073 (2009).

  26. 26.

    et al. The orbitofrontal cortex and ventral tegmental area are necessary for learning from unexpected outcomes. Neuron 62, 269–280 (2009).

  27. 27.

    & Heterogeneous reward signals in prefrontal cortex. Curr. Opin. Neurobiol. 20, 191–198 (2010).

  28. 28.

    , & A framework for studying the neurobiology of value-based decision making. Nat. Rev. Neurosci. 9, 545–556 (2008).

  29. 29.

    Range-adapting representation of economic value in the orbitofrontal cortex. J. Neurosci. 29, 14004–14014 (2009).

  30. 30.

    , & Adaptation of reward sensitivity in orbitofrontal neurons. J. Neurosci. 30, 534–544 (2010).

  31. 31.

    , & Flexible control of mutual inhibition: a neural model of two-interval discrimination. Science 307, 1121–1124 (2005).

  32. 32.

    , & Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299, 1898–1902 (2003).

  33. 33.

    & Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459, 837–841 (2009).

  34. 34.

    , & Adaptive coding of reward value by dopamine neurons. Science 307, 1642–1645 (2005).

  35. 35.

    , & Heterogeneous coding of temporally discounted values in the dorsal and ventral striatum during intertemporal choice. Neuron 69, 170–182 (2011).

  36. 36.

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

  37. 37.

    et al. Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J. Neurosci. 25, 11730–11737 (2005).

  38. 38.

    & Neural correlates of decision variables in parietal cortex. Nature 400, 233–238 (1999).

  39. 39.

    & Reward timing in the primary visual cortex. Science 311, 1606–1609 (2006).

  40. 40.

    , , & Medial prefrontal cell activity signaling prediction errors of action values. Nat. Neurosci. 10, 647–656 (2007).

  41. 41.

    , & Anterior cingulate error-related activity is modulated by predicted reward. Eur. J. Neurosci. 21, 3447–3452 (2005).

  42. 42.

    , , , & Distinct roles of rodent orbitofrontal and medial prefrontal cortex in decision making. Neuron 66, 449–460 (2010).

  43. 43.

    & Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47, 129–141 (2005).

  44. 44.

    , & Performance monitoring in the anterior cingulate is not all error related: expectancy deviation and the representation of action-outcome associations. J. Cogn. Neurosci. 19, 1994–2004 (2007).

  45. 45.

    , & Error effects in anterior cingulate cortex reverse when error likelihood is high. J. Neurosci. 30, 3467–3472 (2010).

  46. 46.

    , , , & Adaptive coding of action values in the human rostral cingulate zone. J. Neurosci. 29, 7489–7496 (2009).

  47. 47.

    , , & Learning the value of information in an uncertain world. Nat. Neurosci. 10, 1214–1221 (2007).

  48. 48.

    & Neural economics and the biological substrates of valuation. Neuron 36, 265–284 (2002).

  49. 49.

    , , & A reservoir of time constants for memory traces in cortical neurons. Nat. Neurosci. 14, 366–372 (2011).

  50. 50.

    & The representation of economic value in the orbitofrontal cortex is invariant for changes of menu. Nat. Neurosci. 11, 95–102 (2008).

Download references

Acknowledgements

The project was funded by US National Institute on Drug Abuse grant R01DA19028, US National Institute of Neurological Disorders and Stroke grant P01NS040813 to J.W. and US National Institute on Mental Health training grant F32MH081521 to S.W.K. T.E.J.B. and S.W.K. are supported by the Wellcome Trust.

Author information

Affiliations

  1. Institute of Neurology, University College London, London, UK.

    • Steven W Kennerley
    •  & Timothy E J Behrens

  2. Helen Wills Neuroscience Institute, University of California, Berkeley, Berkeley, California, USA.

    • Steven W Kennerley
    •  & Jonathan D Wallis

  3. Oxford Centre for Functional Magnetic Resonance Imaging of the Brain (FMRIB), University of Oxford, John Radcliffe Hospital, Oxford, UK.

    • Timothy E J Behrens

  4. Department of Psychology, University of California, Berkeley, Berkeley, California, USA.

    • Jonathan D Wallis

Authors

  1. Search for Steven W Kennerley in:

  2. Search for Timothy E J Behrens in:

  3. Search for Jonathan D Wallis in:

Contributions

S.W.K. designed the experiment, collected and analyzed the data and wrote the manuscript. T.E.J.B. analyzed the data and edited the manuscript. J.D.W. designed the experiment, supervised the project and edited the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Steven W Kennerley.

Supplementary information

PDF files

  1. 1.

    Supplementary Text and Figures

    Supplementary Figures 1–4 and Supplementary Results

To obtain permission to re-use content from this article visit RightsLink.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nn.2961

Further reading