Flexible combination of reward information across primates

Abstract

A fundamental but rarely contested assumption in economics and neuroeconomics is that decision-makers compute subjective values of risky options by multiplying functions of reward probability and magnitude. By contrast, an additive strategy for valuation allows flexible combination of reward information required in uncertain or changing environments. We hypothesized that the level of uncertainty in the reward environment should determine the strategy used for valuation and choice. To test this hypothesis, we examined choice between risky options in humans and rhesus macaques across three tasks with different levels of uncertainty. We found that whereas humans and monkeys adopted a multiplicative strategy under risk when probabilities are known, both species spontaneously adopted an additive strategy under uncertainty when probabilities must be learned. Additionally, the level of volatility influenced relative weighting of certain and uncertain reward information, and this was reflected in the encoding of reward magnitude by neurons in the dorsolateral prefrontal cortex.

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Fig. 1: Experimental paradigms.
Fig. 2: Different strategies for combination of reward information under risk and uncertainty.
Fig. 3: Additive models explain choice under uncertainty.
Fig. 4: Adjustment of choice behaviour to volatility of the environment.
Fig. 5: Behavioural adjustments in response to changes in volatility of the environment in the ML task.
Fig. 6: Neural signature of behavioural adjustments to volatility in the dlPFC.

Data availability

The data that support the findings of this study are available from the corresponding author upon request.

Code availability

Custom computer codes that support the findings of this study are available from the corresponding author upon request.

References

  1. 1.

    Bernoulli, D. Expositions of a new theory of the measurement of risk. Econometrica 22, 23–36 (1954).

    Article  Google Scholar 

  2. 2.

    Edwards, W. The theory of decision making. Psychol. Bull. 51, 380 (1954).

    CAS  Article  Google Scholar 

  3. 3.

    Kahneman, D. & Tversky, A. On the psychology of prediction. Psych. Rev. 80, 237–251 (1973).

    Article  Google Scholar 

  4. 4.

    Stewart, N. Information integration in risky choice: identification and stability. Front. Psychol. 2, 301 (2011).

    Article  Google Scholar 

  5. 5.

    Ernst, M. O. & Banks, M. S. Humans integrate visual and haptic information in a statistically optimal fashion. Nature 415, 429 (2002).

    CAS  Article  Google Scholar 

  6. 6.

    Hunt, L. T., Dolan, R. J. & Behrens, T. E. Hierarchical competitions subserving multi-attribute choice. Nat. Neurosci. 17, 1613–1622 (2014).

    CAS  Article  Google Scholar 

  7. 7.

    Farashahi, S., Rowe, K., Aslami, Z., Lee, D. & Soltani, A. Feature-based learning improves adaptability without compromising precision. Nat. Commun. 8, 1768 (2017).

    Article  Google Scholar 

  8. 8.

    Farashahi, S. et al. Metaplasticity as a neural substrate for adaptive learning and choice under uncertainty. Neuron 94, 401–414 (2017).

    CAS  Article  Google Scholar 

  9. 9.

    Spitmaan, M., Chu, E. & Soltani, A. Salience-driven value construction for adaptive choice under risk. J. Neurosci. 39, 5195–5209 (2019).

    CAS  Article  Google Scholar 

  10. 10.

    Strait, C. E., Blanchard, T. C. & Hayden, B. Y. Reward value comparison via mutual inhibition in ventromedial prefrontal cortex. Neuron 82, 1357–1366 (2014).

    CAS  Article  Google Scholar 

  11. 11.

    Farashahi, S., Azab, H., Hayden, B. & Soltani, A. On the flexibility of basic risk attitudes in monkeys. J. Neurosci. 38, 4383–4398 (2018).

    CAS  Article  Google Scholar 

  12. 12.

    Hayden, B., Heilbronner, S. & Platt, M. Ambiguity aversion in rhesus macaques. Front. Neurosci. 4, 166 (2010).

    Article  Google Scholar 

  13. 13.

    Donahue, C. H. & Lee, D. Dynamic routing of task-relevant signals for decision making in dorsolateral prefrontal cortex. Nat. Neurosci. 18, 295–301 (2015).

    CAS  Article  Google Scholar 

  14. 14.

    Massi, B., Donahue, C. H. & Lee, D. Volatility facilitates value updating in the prefrontal cortex. Neuron 99, 598–608 (2018).

    CAS  Article  Google Scholar 

  15. 15.

    Stephan, K. E., Penny, W. D., Daunizeau, J., Moran, R. J. & Friston, K. J. Bayesian model selection for group studies. NeuroImage 46, 1005–1017 (2009); erratum 48, 311–311 (2009).

  16. 16.

    Behrens, T. E. J., Woolrich, M. W., Walton, M. E. & Rushworth, M. F. S. Learning the value of information in an uncertain world. Nat. Neurosci. 10, 1214–1221 (2007).

    CAS  Article  Google Scholar 

  17. 17.

    Tversky, A. Intransitivity of preferences. Psychol. Rev. 76, 31 (1969).

    Article  Google Scholar 

  18. 18.

    Lichtenstein, S. & Slovic, P. The Construction of Preference (Cambridge Univ. Press, 2006).

  19. 19.

    Ariely, D., Loewenstein, G. & Prelec, D. “Coherent arbitrariness”: stable demand curves without stable preferences. Q. J. Econ. 118, 73–106 (2003).

    Article  Google Scholar 

  20. 20.

    Frederick, S., Loewenstein, G. & O’Donoghue, T. Time discounting and time preference: a critical review. J. Econ. Lit. 40, 351–401 (2002).

    Article  Google Scholar 

  21. 21.

    Kolling, N., Wittmann, M. & Rushworth, M. F. Multiple neural mechanisms of decision making and their competition under changing risk pressure. Neuron 81, 1190–1202 (2014).

    CAS  Article  Google Scholar 

  22. 22.

    Ferrari-Toniolo, S., Bujold, P. M. & Schultz, W. Probability distortion depends on choice sequence in rhesus monkeys. J. Neurosci. 39, 2915–2929 (2019).

    CAS  Article  Google Scholar 

  23. 23.

    Hayden, B. Y. Time discounting and time preference in animals: a critical review. Psychon. Bull. Rev. 23, 39–53 (2016).

    Article  Google Scholar 

  24. 24.

    Kennerley, S. W., Walton, M. E., Behrens, T. E. J., Buckley, M. J. & Rushworth, M. F. S. Optimal decision making and the anterior cingulate cortex. Nat. Neurosci. 9, 940–947 (2006).

    CAS  Article  Google Scholar 

  25. 25.

    Soltani, A. & Izquierdo, A. Adaptive learning under expected and unexpected uncertainty. Nat. Rev. Neurosci. https://doi.org/10.1038/341583-019-0180-y (2019).

  26. 26.

    Brainard, D. H. The psychophysics toolbox. Spat. Vis. 10, 433–436 (1997).

    CAS  Article  Google Scholar 

  27. 27.

    Cornelissen, F. W., Peters, E. M. & Palmer, J. The Eyelink Toolbox: eye tracking with MATLAB and the Psychophysics Toolbox. Behav. Res. Methods Instrum. Comput. 34, 613–617 (2002).

    Article  Google Scholar 

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Acknowledgements

We thank E. Chu, S. Nichols-Worley and L. Tran for collecting human data, and C. Strait and M. Mancarella for collecting monkey data in the gambling task. This work is supported by the National Science Foundation (CAREER Award no. BCS1253576 to B.Y.H. and EPSCoR Award no. 1632738 to A.S.), and the National Institutes of Health (grant no. R01 DA038615 to B.Y.H., grant nos. R01 DA029330 and R01 MH108629 to D.L., and grant no. R01 DA047870 to A.S.). The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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A.S. conceived the project. C.H.D., B.Y.H. and D.L. designed the experiments in monkeys. S.F. and A.S. designed the human experiments. S.F. and A.S. performed model simulations and analysed the data. C.H.D. and S.F. conducted the experiments. C.H.D., S.F., D.L., B.Y.H. and A.S. analysed and interpreted the experimental data. D.L., B.Y.H. and A.S wrote the manuscript and all authors contributed to revising the manuscript.

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Correspondence to Alireza Soltani.

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The authors declare no competing interests.

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Peer review information: Primary Handling Editor: Marike Schiffer.

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Supplementary Information

Supplementary Notes 1 and 2 and Figs. 1–7.

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Farashahi, S., Donahue, C.H., Hayden, B.Y. et al. Flexible combination of reward information across primates. Nat Hum Behav 3, 1215–1224 (2019). https://doi.org/10.1038/s41562-019-0714-3

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