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J Neurophysiol 91: 1013-1024, 2004. First published October 1, 2003; doi:10.1152/jn.00721.2003
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Reward-Predicting Activity of Dopamine and Caudate Neurons—A Possible Mechanism of Motivational Control of Saccadic Eye Movement

Reiko Kawagoe1, Yoriko Takikawa1 and Okihide Hikosaka1,2

1Department of Physiology, Juntendo University, School of Medicine, Tokyo 113-8421, Japan; and 2Laboratory of Sensorimotor Research, National Eye Institute, National Institute of Health, Bethesda, Maryland 20892-4435

Submitted 28 July 2003; accepted in final form 28 September 2003

Recent studies have suggested that the basal ganglia are related to motivational control of behavior. To study how motivational signals modulate motor signals in the basal ganglia, we examined activity of midbrain dopamine (DA) neurons and caudate (CD) projection neurons while monkeys were performing a one-direction-rewarded version (1DR) of memory-guided saccade task. The cue stimulus indicated the goal position for an upcoming saccade and the presence or absence of reward after the trial. Among four monkeys we studied, three were sensitive to reward such that saccade velocity was significantly higher in the rewarded trials than in the nonrewarded trials; one monkey was insensitive to reward. In the reward-sensitive monkeys, both DA and CD neurons responded differentially to reward-indicating and no-reward-indicating cues. Thus DA neurons responded with excitation to a reward-indicating cue and with inhibition to a no-reward-indicating cue. A group of CD neurons responded to the cue in their response fields (mostly contralateral) and the cue response was usually enhanced when it indicated reward. In the reward-insensitive monkey, DA neurons showed no response to the cue, while the cue responses of CD neurons were not modulated by reward. Many CD neurons in the reward-sensitive monkeys, but not the reward-insensitive monkey, showed precue activity. These results suggest that DA neurons, with their connection to CD neurons, modulate the spatially selective signals in CD neurons in the reward-predicting manner and CD neurons in turn modulate saccade parameters with their polysynaptic connections to the oculomotor brain stem.


Address for reprint requests and other correspondence: O. Hikosaka, Laboratory of Sensorimotor Research, National Eye Institute, National Institute of Health, 49 Convent Drive, Bldg. 49, Rm. 2A50, Bethesda, MD 20892-4435 (E-mail: oh{at}lsr.nei.nih.gov).




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