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Dopamine responses comply with basic assumptions of formal learning theory

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.

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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.

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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.

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Correspondence to Wolfram Schultz.

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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

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