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The Journal of Neuroscience, November 12, 2003, 23(32):10402-10410

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Behavioral/Systems/Cognitive
Coding of Predicted Reward Omission by Dopamine Neurons in a Conditioned Inhibition Paradigm

Philippe N. Tobler,¹ Anthony Dickinson,² and Wolfram Schultz¹

¹Department of Anatomy, University of Cambridge, Cambridge CB2 3DY, United Kingdom, and Institute of Physiology, University of Fribourg, 1700 Fribourg, Switzerland, and ²Department of Experimental Psychology, University of Cambridge, Cambridge CB2 3EB, United Kingdom

Animals learn not only about stimuli that predict reward but also about those that signal the omission of an expected reward. We used a conditioned inhibition paradigm derived from animal learning theory to train a discrimination between a visual stimulus that predicted reward (conditioned excitor) and a second stimulus that predicted the omission of reward (conditioned inhibitor). Performing the discrimination required attention to both the conditioned excitor and the inhibitor; however, dopamine neurons showed very different responses to the two classes of stimuli. Conditioned inhibitors elicited considerable depressions in 48 of 69 neurons (median of 35% below baseline) and minor activations in 29 of 69 neurons (69% above baseline), whereas reward-predicting excitors induced pure activations in all 69 neurons tested (242% above baseline), thereby demonstrating that the neurons discriminated between conditioned stimuli predicting reward versus nonreward. The discriminative responses to stimuli with differential reward-predicting but common attentional functions indicate differential neural coding of reward prediction and attention. The neuronal responses appear to reflect reward prediction errors, thus suggesting an extension of the correspondence between learning theory and activity of single dopamine neurons to the prediction of nonreward.

Key words: dopamine; reward; attention; prediction error; inhibition; learning theory

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Received June 16, 2003; revised September 17, 2003; accepted September 19, 2003.

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