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.

Dopamine responses comply with basic assumptions of formal learning theory

Nature volume 412, pages 43–48 (2001)Cite this article

Abstract

According to contemporary learning theories, the discrepancy, or error, between the actual and predicted reward determines whether learning occurs when a stimulus is paired with a reward. The role of prediction errors is directly demonstrated by the observation that learning is blocked when the stimulus is paired with a fully predicted reward. By using this blocking procedure, we show that the responses of dopamine neurons to conditioned stimuli was governed differentially by the occurrence of reward prediction errors rather than stimulus–reward associations alone, as was the learning of behavioural reactions. Both behavioural and neuronal learning occurred predominantly when dopamine neurons registered a reward prediction error at the time of the reward. Our data indicate that the use of analytical tests derived from formal behavioural learning theory provides a powerful approach for studying the role of single neurons in learning.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Behavioural performance in the blocking paradigm and neuronal localizations.
Figure 2: Acquisition of dopamine responses to conditioned stimuli depends on prediction errors in the blocking paradigm.
Figure 3: Dopamine prediction error response at the time of the reward in the blocking paradigm.
Figure 4: Dopamine responses to unrewarded stimuli may reflect stimulus generalization rather than reward prediction.

References

  1. Thorndike, E. L. Animal Intelligence: Experimental Studies (MacMillan, New York, 1911).

    Book  Google Scholar 

  2. Pavlov, I. P. Conditional Reflexes (Oxford Univ. Press, London, 1927).

    Google Scholar 

  3. Rescorla, R. A. & Wagner, A. R. in Classical Conditioning II: Current Research and Theory (eds Black, A. H. & Prokasy, W. F.) 64–99 (Appleton Century Crofts, New York, 1972).

    Google Scholar 

  4. Mackintosh, N. J. A theory of attention: Variations in the associability of stimulus with reinforcement. Psychol. Rev. 82, 276–298 (1975).

    Article  Google Scholar 

  5. Pearce, J. M. & Hall, G. A. A model for Pavlovian conditioning: variations in the effectiveness of conditioned but not of unconditioned stimuli. Psychol. Rev. 87, 532–552 (1980).

    Article  CAS  Google Scholar 

  6. Dickinson, A. Contemporary Animal Learning Theory (Cambridge Univ. Press, Cambridge, 1980).

    Google Scholar 

  7. Schultz, W. & Dickinson, A. Neuronal coding of prediction errors. Annu. Rev. Neurosci. 23, 473–500 (2000).

    Article  CAS  Google Scholar 

  8. Widrow, G. & Hoff, M. E. Adaptive switching circuits. IRE Western Electron. Show Convention, Convention Record Part 4, 96–104 (1960).

  9. Kalman, R. E. A new approach to linear filtering and prediction problems. J. Basic Eng. Trans. ASME 82, 35–45 (1960).

    Article  Google Scholar 

  10. Widrow, G. & Sterns, S. D. Adaptive Signal Processing (Prentice-Hall, Englewood Cliffs, 1985).

    Google Scholar 

  11. Marr, D. A theory of cerebellar cortex. J. Physiol. 202, 437–470 (1969).

    Article  CAS  Google Scholar 

  12. Ito, M. Long-term depression. Ann. Rev. Neurosci. 12, 85–102 (1989).

    Article  CAS  Google Scholar 

  13. Thompson, R. F. & Gluck, M. A. in Perspectives on Cognitive Neuroscience (eds Lister, R. G. & Weingartner, H.) 25–45 (Oxford Univ. Press, New York, 1991).

    Google Scholar 

  14. Kawato, M. & Gomi, H. The cerebellum and VOR/OKR learning models. Trends Neurosci. 15, 445–453 (1992).

    Article  CAS  Google Scholar 

  15. Kim, J. J., Krupa, D. J. & Thompson, R. F. Inhibitory cerebello-olivary projections and blocking effect in classical conditioning. Science 279, 570–573 (1998).

    Article  ADS  CAS  Google Scholar 

  16. 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 

  17. Sutton, R. S. & Barto, A. G. Reinforcement Learning (MIT Press, Cambridge, Massachusetts, 1998).

    Google Scholar 

  18. Fibiger, H. C. & Phillips, A. G. in Handbook of Physiology—The Nervous System IV (ed. Bloom, F. E.) 647–675 (Williams and Wilkins, Baltimore, 1986).

    Google Scholar 

  19. Wise, R. A. & Hoffman, C. D. Localization of drug reward mechanisms by intracranial injections. Synapse 10, 247–263 (1992).

    Article  CAS  Google Scholar 

  20. Robinson, T. E. & Berridge, K. C. The neural basis for drug craving: an incentive-sensitization theory of addiction. Brain Res. Rev. 18, 247–291 (1993).

    Article  CAS  Google Scholar 

  21. Robbins, T. W. & Everitt, B. J. Neurobehavioural mechanisms of reward and motivation. Curr. Opin. Neurobiol. 6, 228–236 (1996).

    Article  CAS  Google Scholar 

  22. Romo, R. & Schultz, W. Dopamine neurons of the monkey midbrain: Contingencies of responses to active touch during self-initiated arm movements. J. Neurophysiol. 63, 592–606 (1990).

    Article  CAS  Google Scholar 

  23. Schultz, W. & Romo, R. Dopamine neurons of the monkey midbrain: Contingencies of responses to stimuli eliciting immediate behavioural reactions. J. Neurophysiol. 63, 607–624 (1990).

    Article  CAS  Google Scholar 

  24. Ljungberg, T., Apicella, P. & Schultz, W. Responses of monkey dopamine neurons during learning of behavioural reactions. J. Neurophysiol. 67, 145–163 (1992).

    Article  CAS  Google Scholar 

  25. Schultz, W., Apicella, P. & Ljungberg, T. Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J. Neurosci. 13, 900–913 (1993).

    Article  CAS  Google Scholar 

  26. Schultz, W., Dayan, P. & Montague, R. R. A neural substrate of prediction and reward. Science 275, 1593–1599 (1997).

    Article  CAS  Google Scholar 

  27. Hollerman, J. R. & Schultz, W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nature Neurosci. 1, 304–309 (1998).

    Article  CAS  Google Scholar 

  28. Schultz, W. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80, 1–27 (1998).

    Article  CAS  Google Scholar 

  29. Salamone, J. D. The involvement of nucleus accumbens dopamine in appetitive and aversive motivation. Behav. Brain Res. 61, 117–133 (1994).

    Article  CAS  Google Scholar 

  30. Horvitz, J. C. Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96, 651–656 (2000).

    Article  CAS  Google Scholar 

  31. Sutton, R. S. & Barto, A. G. in Learning and Computational Neuroscience: Foundations of Adaptive Networks (eds Gabriel, M. & Moore, J.) 497–537 (MIT Press, Cambridge, Massachusetts, 1990).

    Google Scholar 

  32. Mackintosh, N. J. Conditioning and Associative Learning (Oxford Univ. Press, New York, 1983).

    Google Scholar 

  33. Friston, K. J., Tononi, G., Reeke, G. N. Jr, Sporns, O. & Edelman, G. M. Value-dependent selection in the brain: simulation in a synthetic neural model. Neuroscience 59, 229–243 (1994).

    Article  CAS  Google Scholar 

  34. Montague, P. R., Dayan, P. & Sejnowski, T. J. A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J. Neurosci. 16, 1936–1947 (1996).

    Article  CAS  Google Scholar 

  35. Houk, J. C., Adams, J. L. & Barto, A. G. in Models of Information Processing in the Basal Ganglia (eds Houk, J. C., Davis, J. L. & Beiser, D. G.) 249–270 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  36. Suri, R. & Schultz, W. A neural network with dopamine-like reinforcement signal that learns a spatial delayed response task. Neuroscience 91, 871–890 (1999).

    Article  CAS  Google Scholar 

  37. Kamin, L. J. in Fundamental Issues in Instrumental Learning (eds Mackintosh, N. J. & Honig, W. K.) 42–64 (Dalhousie Univ. Press, Dalhousie, 1969).

    Google Scholar 

  38. Martin, I. & Levey, A. B. Blocking observed in human eyelid conditioning. Q. J. Exp. Psychol. B 43, 233–255 (1991).

    CAS  PubMed  Google Scholar 

  39. Dickinson, A. Causal learning: An associative analysis. Q. J. Exp. Psychol. B 54, 3–25 (2001).

    Article  CAS  Google Scholar 

  40. Holland, P. C. Brain mechanisms for changes in processing of conditioned stimuli in Pavlovian conditioning: Implications for behavioural theory. Anim. Learn. Behav. 25, 373–399 (1997).

    Article  Google Scholar 

  41. Calabresi, P., Maj, R., Pisani, A., Mercuri, N. B. & Bernardi, G. Long-term synaptic depression in the striatum: Physiological and pharmacological characterization. J. Neurosci. 12, 4224–4233 (1992).

    Article  CAS  Google Scholar 

  42. Garcia-Munoz, M., Young, S. J. & Groves, P. Presynaptic long-term changes in excitability of the corticostriatal pathway. NeuroReport 3, 357–360 (1992).

    Article  CAS  Google Scholar 

  43. Wickens, J. R., Begg, A. J. & Arbuthnott, G. W. Dopamine reverses the depression of rat corticostriatal synapses which normally follows high-frequency stimulation of cortex in vitro. Neuroscience 70, 1–5 (1996).

    Article  CAS  Google Scholar 

  44. Calabresi, P. et al. Abnormal synaptic plasticity in the striatum of mice lacking dopamine D2 receptors. J. Neurosci. 17, 4536–4544 (1997).

    Article  CAS  Google Scholar 

  45. Otani, S., Blond, O., Desce, J. M. & Crepel, F. Dopamine facilitates long-term depression of glutamatergic transmission in rat prefrontal cortex. Neuroscience 85, 669–676 (1998).

    Article  CAS  Google Scholar 

  46. Otani, S., Auclair, N., Desce, J., Roisin, M. P. & Crepel, F. J. Neurosci. 19, 9788–9802 (1999).

    Article  CAS  Google Scholar 

  47. Centonze, D. et al. Unilateral dopamine denervation blocks corticostriatal LTP. J. Neurophysiol. 82, 3575–3579 (1999).

    Article  CAS  Google Scholar 

  48. Minsky, M. L. Steps toward artificial intelligence. Proc. Inst. Radio Engineers 49, 8–30 (1961).

    MathSciNet  Google Scholar 

  49. Rauhut, A. S., McPhee, J. E. & Ayres, J. J. B. Blocked and overshadowed stimuli are weakened in their ability to serve as blockers and second-order reinforcers in Pavlovian fear conditioning. J. Exp. Psychol: Anim. Behav. Process 25, 45–67 (1999).

    CAS  Google Scholar 

  50. Schultz, W. & Romo, R. Responses of nigrostriatal dopamine neurons to high intensity somatosensory stimulation in the anesthetized monkey. J. Neurophysiol. 57, 201–217 (1987).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank B. Aebischer, J. Corpataux, A. Gaillard, B. Morandi, A. Pisani and F. Tinguely for expert technical assistance. The study was supported by the Swiss NSF, the European Union (Human Capital and Mobility, and Biomed 2 programmes), the James S. McDonnell Foundation and the British Council.

Author information

Authors and Affiliations

  1. Institute of Physiology and Programme in Neuroscience, University of Fribourg, Fribourg, CH-1700, Switzerland

    Pascale Waelti & Wolfram Schultz

  2. Department of Experimental Psychology, University of Cambridge, Cambridge, CB2 3EB, UK

    Anthony Dickinson

Authors
  1. Pascale Waelti
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anthony Dickinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wolfram Schultz
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wolfram Schultz.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Waelti, P., Dickinson, A. & Schultz, W. Dopamine responses comply with basic assumptions of formal learning theory. Nature 412, 43–48 (2001). https://doi.org/10.1038/35083500

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/35083500

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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