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Risk-sensitive neurons in macaque posterior cingulate cortex

Abstract

People and animals often demonstrate strong attraction or aversion to options with uncertain or risky rewards, yet the neural substrate of subjective risk preferences has rarely been investigated. Here we show that monkeys systematically preferred the risky target in a visual gambling task in which they chose between two targets offering the same mean reward but differing in reward uncertainty. Neuronal activity in posterior cingulate cortex (CGp), a brain area linked to visual orienting and reward processing, increased when monkeys made risky choices and scaled with the degree of risk. CGp activation was better predicted by the subjective salience of a chosen target than by its actual value. These data suggest that CGp signals the subjective preferences that guide visual orienting.

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Figure 1: Method for investigating risk sensitivity in macaque posterior cingulate cortex.
Figure 2: Monkeys prefer targets offering uncertain rewards.
Figure 3: Posterior cingulate neurons are risk-sensitive.
Figure 4: Target risk enhances neuronal activity in CGp as well as sensitivity to movement direction.
Figure 5: Average heart rate does not increase with increasing risk.
Figure 6: Population neuronal activity reflects monkeys' preference for risky targets but not prior reward outcomes.
Figure 7: CGp neurons carry information about both target choice and subjective target utility.
Figure 8: Both the frequency of risky target choices and neuronal activity gradually increase after block changes.

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References

  1. Bateson, M. & Kacelnik, A. Starlings' preferences for predictable and unpredictable delays to food. Anim. Behav. 53, 1129–1142 (1997).

    Article  CAS  Google Scholar 

  2. Kahneman, D. & Tversky, A. Prospect theory: an analysis of decision under risk. Econometrica 47, 263–291 (1979).

    Article  Google Scholar 

  3. Weber, E.U., Shafir, S. & Blais, A.R. Predicting risk sensitivity in humans and lower animals: risk as variance or coefficient of variation. Psychol. Rev. 111, 430–445 (2004).

    Article  Google Scholar 

  4. Bernouilli, D. The Works (Birkhauser, Boston, 1758).

    Google Scholar 

  5. Rode, C., Cosmides, L., Hell, W. & Tooby, J. When and why do people avoid unknown probabilities in decisions under uncertainty? Testing some predictions from optimal foraging theory. Cognition 72, 269–304 (1999).

    Article  CAS  Google Scholar 

  6. Bateson, M. Recent advances in our understanding of risk-sensitive foraging preferences. Proc. Nutr. Soc. 61, 509–516 (2002).

    Article  Google Scholar 

  7. Von Neumann, J.V. & Morgenstern, O. Theory of Games and Economic Behavior (Princeton University Press, Princeton, New Jersey, 1944).

    Google Scholar 

  8. McClure, S.M. et al. Neural correlates of behavioral preference for culturally familiar drinks. Neuron 44, 379–387 (2004).

    Article  CAS  Google Scholar 

  9. Arnauld, A. & Nichole, P. The Art of Thinking: Port-Royal Logic (Bobbs-Merrill, Indianapolis, 1662).

    Google Scholar 

  10. Stephens, D.W. & Krebs, J.R. Foraging Theory (Princeton University Press, Princeton, New Jersey, 1986).

    Google Scholar 

  11. Platt, M.L. & Glimcher, P.W. Neural correlates of decision variables in parietal cortex. Nature 400, 233–238 (1999).

    Article  CAS  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  Google Scholar 

  13. Kawagoe, R., Takikawa, Y. & Hikosaka, O. Expectation of reward modulates cognitive signals in the basal ganglia. Nat. Neurosci. 1, 411–416 (1998).

    Article  CAS  Google Scholar 

  14. Sugrue, L.P., Corrado, G.S. & Newsome, W.T. Matching behavior and the representation of value in the parietal cortex. Science 304, 1782–1787 (2004).

    Article  CAS  Google Scholar 

  15. Lauwereyns, J., Watanabe, K., Coe, B. & Hikosaka, O. A neural correlate of response bias in monkey caudate nucleus. Nature 418, 413–417 (2002).

    Article  CAS  Google Scholar 

  16. McCoy, A.N., Crowley, J.C., Haghighian, G., Dean, H.L. & Platt, M.L. Saccade reward signals in posterior cingulate cortex. Neuron 40, 1031–1040 (2003).

    Article  CAS  Google Scholar 

  17. Dorris, M.C. & Glimcher, P.W. Activity in posterior parietal cortex is correlated with the relative subjective desirability of action. Neuron 44, 365–378 (2004).

    Article  CAS  Google Scholar 

  18. Schultz, W. Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology. Curr. Opin. Neurobiol. 14, 139–147 (2004).

    Article  CAS  Google Scholar 

  19. Roesch, M.R. & Olson, C.R. Neuronal activity related to reward value and motivation in primate frontal cortex. Science 304, 307–310 (2004).

    Article  CAS  Google Scholar 

  20. Kacelnik, A. Normative and descriptive models of decision making: time discounting and risk sensitivity. Ciba Found. Symp. 208, 51–67 (1997).

    CAS  PubMed  Google Scholar 

  21. Hopfinger, J.B., Buonocore, M.H. & Mangun, G.R. The neural mechanisms of top-down attentional control. Nat. Neurosci. 3, 284–291 (2000).

    Article  CAS  Google Scholar 

  22. Small, D.M. et al. The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention. Neuroimage 18, 633–641 (2003).

    Article  CAS  Google Scholar 

  23. Berman, R.A. et al. Cortical networks subserving pursuit and saccadic eye movements in humans: an FMRI study. Hum. Brain Mapp. 8, 209–225 (1999).

    Article  CAS  Google Scholar 

  24. Olson, C.R., Musil, S.Y. & Goldberg, M.E. Single neurons in posterior cingulate cortex of behaving macaque: eye movement signals. J. Neurophysiol. 76, 3285–3300 (1996).

    Article  CAS  Google Scholar 

  25. Rescorla, R.A. & Wagner, A.R. A theory of Pavlovian conditioning. Variations in the effectiveness of reinforcement and nonreinforcement. in Classical Conditioning II: Current Research and Theory (eds. Black, A.H. & Prokasy, W.F.) (Appleton-Century-Crofts, New York, 1972).

    Google Scholar 

  26. Sutton, R.S. & Barto, A.G. Toward a modern theory of adaptive networks: expectation and prediction. Psychol. Rev. 88, 135–170 (1981).

    Article  CAS  Google Scholar 

  27. 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  Google Scholar 

  28. Caraco, T. White crowned sparrows (Zonotricha leucophrys): foraging preferences in a risky environment. Behav. Ecol. Sociobiol. 8, 820–830 (1983).

    Google Scholar 

  29. McGlothlin, W.H. Stability of choices among uncertain alternatives. Am. J. Psychol. 69, 604–615 (1956).

    Article  CAS  Google Scholar 

  30. Dean, H.L., Crowley, J.C. & Platt, M.L. Visual and saccade-related activity in macaque posterior cingulate cortex. J. Neurophysiol. 92, 3056–3068 (2004).

    Article  Google Scholar 

  31. Ladouceur, R., Sevigny, S., Blaszczynski, A., O'Connor, K. & Lavoie, M.E. Video lottery: winning expectancies and arousal. Addiction 98, 733–738 (2003).

    Article  Google Scholar 

  32. Sharpe, L. Patterns of autonomic arousal in imaginal situations of winning and losing in problem gambling. J. Gambl. Stud. 20, 95–104 (2004).

    Article  Google Scholar 

  33. Meyer, G. et al. Casino gambling increases heart rate and salivary cortisol in regular gamblers. Biol. Psychiatry 48, 948–953 (2000).

    Article  CAS  Google Scholar 

  34. Bechara, A. & Damasio, H. Decision-making and addiction (part I): impaired activation of somatic states in substance dependent individuals when pondering decisions with negative future consequences. Neuropsychologia 40, 1675–1689 (2002).

    Article  Google Scholar 

  35. Hikosaka, O., Sakamoto, M. & Usui, S. Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J. Neurophysiol. 61, 814–832 (1989).

    Article  CAS  Google Scholar 

  36. Marsh, B. & Kacelnik, A. Framing effects and risky decisions in starlings. Proc. Natl. Acad. Sci. USA 99, 3352–3355 (2002).

    Article  CAS  Google Scholar 

  37. Kelley, A.E., Schochet, T. & Landry, C.F. Risk taking and novelty seeking in adolescence: introduction to part I. Ann. NY Acad. Sci. 1021, 27–32 (2004).

    Article  Google Scholar 

  38. Doremus, T.L., Varlinskaya, E.I. & Spear, L.P. Age-related differences in elevated plus maze behavior between adolescent and adult rats. Ann. NY Acad. Sci. 1021, 427–430 (2004).

    Article  Google Scholar 

  39. Chambers, R.A., Taylor, J.R. & Potenza, M.N. Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am. J. Psychiatry 160, 1041–1052 (2003).

    Article  Google Scholar 

  40. Bickel, W.K., Giordano, L.A. & Badger, G.J. Risk-sensitive foraging theory elucidates risky choices made by heroin addicts. Addiction 99, 855–861 (2004).

    Article  Google Scholar 

  41. McCoy, A.N. & Platt, M.L. Expectations and outcomes: decision-making in the primate brain. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 191, 201–211 (2005).

    Article  Google Scholar 

  42. Gold, J.I. & Shadlen, M.N. Banburismus and the brain: decoding the relationship between sensory stimuli, decisions, and reward. Neuron 36, 299–308 (2002).

    Article  CAS  Google Scholar 

  43. Fiorillo, C.D., Tobler, P.N. & Schultz, W. Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299, 1898–1902 (2003).

    Article  CAS  Google Scholar 

  44. Vogt, B.A. & Pandya, D.N. Cingulate cortex of the rhesus monkey: II. Cortical afferents. J. Comp. Neurol. 262, 271–289 (1987).

    Article  CAS  Google Scholar 

  45. Critchley, H.D., Mathias, C.J. & Dolan, R.J. Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29, 537–545 (2001).

    Article  CAS  Google Scholar 

  46. Dickhaut, J. et al. The impact of the certainty context on the process of choice. Proc. Natl. Acad. Sci. USA 100, 3536–3541 (2003).

    Article  CAS  Google Scholar 

  47. Mesulam, M.M. Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Phil. Trans. R. Soc. Lond. B 354, 1325–1346 (1999).

    Article  CAS  Google Scholar 

  48. Damasio, A. Descartes' Error: Emotion, Reason, and the Human Brain (Avon, New York, 1995).

    Google Scholar 

  49. Judge, S.J., Richmond, B.J. & Chu, F.C. Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res. 20, 535–538 (1980).

    Article  CAS  Google Scholar 

  50. Glimcher, P.W. et al. Application of neurosonography to experimental physiology. J. Neurosci. Methods 108, 131–144 (2001).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank G. Haghighian and J. Crowley for their contribution to the early stages of this work. We also thank S. Roberts for assistance in animal care and S. Huettel, J. Stowe, P. Glimcher, R. Deaner, J. Roitman, M. Bendiksby, S. Shepherd and A. Khera for valuable comments on the manuscript. Supported by the Klingenstein Foundation, the Duke Provost's Common Fund and the National Eye Institute.

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Correspondence to Michael L Platt.

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McCoy, A., Platt, M. Risk-sensitive neurons in macaque posterior cingulate cortex. Nat Neurosci 8, 1220–1227 (2005). https://doi.org/10.1038/nn1523

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