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The Journal of Neuroscience, November 5, 2003, 23(31):10052-10057

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BRIEF COMMUNICATION
Neural Correlates of Rewarded and Unrewarded Eye Movements in the Primate Caudate Nucleus

Katsumi Watanabe,^1,3 Johan Lauwereyns,^2,3 and Okihide Hikosaka³

¹Institute for Human Science and Biomedical Engineering, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki 305-8566, Japan, ²School of Psychology, Victoria University of Wellington, Wellington 6006, New Zealand, and ³National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892-4435

The prospect of immediate reward elicits goal-oriented behavior. However, animals often have to perform actions that do not immediately lead to reward in the pursuit of a long-term goal. Here we identify neural activity in monkey caudate nucleus that specifically correlates with rewarded and unrewarded eye movements. The monkey performed a visually guided saccade task in which only one position was associated with positive reinforcement. To advance in the experimental session, however, the monkey had no choice but to complete a saccade to an unrewarded position as well as to a rewarded position. Some caudate saccadic neurons showed enhanced activity around the time of the saccade in rewarded trials (rewarded-saccade neurons). Another subset of neurons discharged selectively around the execution of the saccade in unrewarded trials (unrewarded-saccade neurons). In both rewarded and unrewarded trials, stronger activity of these neurons was associated with reduced saccade latency. These results suggest that both rewarded and unrewarded saccades are facilitated by caudate saccadic activity. The neuronal activity of unrewarded-saccade neurons might reflect the required execution of unrewarded eye movements on the way to future reward.

Key words: caudate; motivation; reinforcement; saccade; monkey; latency

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Received May 28, 2003; revised September 15, 2003; accepted September 16, 2003.

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