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Science 14 March 1997:
Vol. 275. no. 5306, pp. 1593 - 1599
DOI: 10.1126/science.275.5306.1593

Articles

A Neural Substrate of Prediction and Reward

Wolfram Schultz, Peter Dayan, P. Read Montague *

The capacity to predict future events permits a creature to detect, model, and manipulate the causal structure of its interactions with its environment. Behavioral experiments suggest that learning is driven by changes in the expectations about future salient events such as rewards and punishments. Physiological work has recently complemented these studies by identifying dopaminergic neurons in the primate whose fluctuating output apparently signals changes or errors in the predictions of future salient and rewarding events. Taken together, these findings can be understood through quantitative theories of adaptive optimizing control.

W. Schultz is at the Institute of Physiology, University of Fribourg, CH-1700 Fribourg, Switzerland. E-mail: Wolfram.Schultz{at}unifr.ch  P. Dayan is in the Department of Brain and Cognitive Sciences, Center for Biological and Computational Learning, E-25 MIT, Cambridge, MA 02139, USA. E-mail: dayan{at}ai.mit.edu  P. R. Montague is in the Division of Neuroscience, Center for Theoretical Neuroscience, Baylor College of Medicine, 1 Baylor Plaza, Houston, TX 77030, USA. E-mail: read{at}bcm.tmc.edu
*   To whom correspondence should be addressed.


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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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   Abstract »    Full Text »    PDF »
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