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The Journal of Neuroscience, April 22, 2009, 29(16):5287-5294; doi:10.1523/JNEUROSCI.5298-08.2009

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Behavioral/Systems/Cognitive
The Hippocampus Codes the Uncertainty of Cue–Outcome Associations: An Intracranial Electrophysiological Study in Humans

Giovanna Vanni-Mercier,¹ François Mauguière,² Jean Isnard,² and Jean-Claude Dreher¹

¹Center for Cognitive Neuroscience, Reward and Decision Making Group, CNRS, UMR 5229, Université Lyon 1, and ²Neurological Hospital, 69675 Bron Cedex, France

Correspondence should be addressed to either Dr. Giovanna Vanni-Mercier or Dr. Jean-Claude Dreher, Reward and Decision Making Group, Cognitive Neuroscience Center, CNRS, UMR 5229, 67 boulevard Pinel, 69675 Bron, France. Email: g.vanni-mercier{at}isc.cnrs.fr. or Email: dreher{at}isc.cnrs.fr

Learning to predict upcoming outcomes based on environmental cues is essential for adaptative behavior. In monkeys, midbrain dopaminergic neurons code two statistical properties of reward: a prediction error at the outcome and uncertainty during the delay period between cues and outcomes. Although the hippocampus is sensitive to reward processing, and hippocampal–midbrain functional interactions are well documented, it is unknown whether it also codes the statistical properties of reward information. To address this question, we recorded local field potentials from intracranial electrodes in human hippocampus while subjects learned to associate cues of slot machines with various monetary reward probabilities (P). We found that the amplitudes of negative event-related potentials covaried with uncertainty at the outcome, being maximal for P = 0.5 and minimal for P = 0 and P = 1, regardless of winning or not. These results show that the hippocampus computes an uncertainty signal that may constitute a fundamental mechanism underlying the role of this brain region in a number of functions, including attention-based learning, associative learning, probabilistic classification, and binding of stimulus elements.

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Received Oct. 30, 2008; revised Dec. 11, 2008; accepted March 3, 2009.

Correspondence should be addressed to either Dr. Giovanna Vanni-Mercier or Dr. Jean-Claude Dreher, Reward and Decision Making Group, Cognitive Neuroscience Center, CNRS, UMR 5229, 67 boulevard Pinel, 69675 Bron, France. Email: g.vanni-mercier{at}isc.cnrs.fr. or Email: dreher{at}isc.cnrs.fr

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