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The Journal of Neuroscience, April 15, 2009, 29(15):4858-4870; doi:10.1523/JNEUROSCI.4415-08.2009

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Behavioral/Systems/Cognitive
Different Pedunculopontine Tegmental Neurons Signal Predicted and Actual Task Rewards

Ken-ichi Okada,¹ Keisuke Toyama,² Yuka Inoue,³ Tadashi Isa,³ and Yasushi Kobayashi^1,2

¹Graduate School of Frontier Biosciences, Osaka University, Toyonaka 560-8531, Japan, ²ATR Computational Neuroscience Laboratories, Seika-cho, Kyoto 619-0288, Japan and ³Department of Developmental Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan

Correspondence should be addressed to Dr. Yasushi Kobayashi, Graduate School of Frontier Biosciences, Osaka University, 1-3 Machikaneyama, Toyonaka 560-8531, Japan. Email: yasushi{at}fbs.osaka-u.ac.jp

The dopamine system has been implicated in guiding behavior based on rewards. The pedunculopontine tegmental nucleus (PPTN) of the brainstem receives afferent inputs from reward-related structures, including the cerebral cortices and the basal ganglia, and in turn provides strong excitatory projections to dopamine neurons. This anatomical evidence predicts that PPTN neurons may carry reward information. To elucidate the functional role of the PPTN in reward-seeking behavior, we recorded single PPTN neurons while monkeys performed a visually guided saccade task in which the predicted reward value was informed by the shape of the fixation target. Two distinct groups of neurons, fixation target (FT) and reward delivery (RD) neurons, carried reward information. The activity of FT neurons persisted between FT onset and reward delivery, with the level of activity associated with the magnitude of the expected reward. RD neurons discharged phasically after reward delivery, with the levels of activity associated with the actual reward. These results suggest that separate populations of PPTN neurons signal predicted and actual reward values, both of which are necessary for the computation of reward prediction error as represented by dopamine neurons.

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Received Sept. 2, 2008; revised Feb. 28, 2009; accepted March 12, 2009.

Correspondence should be addressed to Dr. Yasushi Kobayashi, Graduate School of Frontier Biosciences, Osaka University, 1-3 Machikaneyama, Toyonaka 560-8531, Japan. Email: yasushi{at}fbs.osaka-u.ac.jp

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