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Positive and Negative Modulation of Motor Response in Primate Superior Colliculus by Reward Expectation

¹Department of Developmental Physiology, National Institute for Physiological Sciences, Okazaki, Aichi; ²Core Research for Evolutional Science and Technology, Japan Science and Technology Agency, Kawaguchi; ³Brain Science Research Center, Tamagawa University Research Institute, Tokyo, Japan; ⁴Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland; and ⁵Department of Physiology, Juntendo University, School of Medicine, Tokyo, Japan

Submitted 29 August 2007; accepted in final form 4 October 2007

Expectation of reward is crucial for goal-directed behavior of animals. However, little is known about how reward information is used in the brain at the time of action. We investigated this question by recording from single neurons in the macaque superior colliculus (SC) while the animal was performing a memory-guided saccade task with an asymmetrical reward schedule. The SC is an ideal structure to ask this question because it receives inputs from many brain areas including the prefrontal cortex and the basal ganglia where reward information is thought to be encoded and sends motor commands to the brain stem saccade generators. We found two groups of SC neurons that encoded reward information in the presaccadic period: positive reward-coding neurons that showed higher activity when reward was expected and negative reward-coding neurons that showed higher activity when reward was not expected. The positive reward-coding usually started even before a cue for target position was presented, whereas the negative reward-coding was largely restricted to the presaccadic period. The two kinds of reward-coding may be useful for the animal to select an appropriate behavior in a complex environment.

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