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Expectation of reward modulates cognitive signals in the basal ganglia

Abstract

Action is controlled by both motivation and cognition. The basal ganglia may be the site where these kinds of information meet. Using a memory-guided saccade task with an asymmetric reward schedule, we show that visual and memory responses of caudate neurons are modulated by expectation of reward so profoundly that a neuron's preferred direction often changed with the change in the rewarded direction. The subsequent saccade to the target was earlier and faster for the rewarded direction. Our results indicate that the caudate contributes to the determination of oculomotor outputs by connecting motivational values (for example, expectation of reward) to visual information.

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Figure 1: Memory-guided saccade task in the 'one direction rewarded' condition (1DR).
Figure 2: Reward-dependent visual response (reward-facilitated type) of a neuron recorded in the right caudate nucleus.
Figure 3: Reward-dependent visual response (reward-suppressed type) of a neuron recorded in the left caudate nucleus.
Figure 4: Reward-dependent memory response (reward-facilitated type) of a neuron recorded in the left caudate nucleus.
Figure 5: Effects of reward expectation on caudate neuron activity (a), saccade latency (b), and saccade velocity (c).
Figure 6: Change in direction selectivity within one block of 1DR trials.
Figure 7: Recording sites of reward-contingent caudate neurons plotted on coronal sections in one monkey.

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Acknowledgements

We thank Masamichi Sakagami, Johan Lauwereyns, Katsuyuki Sakai, Hiroyuki Nakahara, Thomas Trappenberg and Brian Coe for comments, Makoto Kato for designing the computer programs and Masashi Koizumi for technical support. This work was supported by CREST (Core Research for Evolutional Science and Technology) of Japan Science and Technology Corporation (JST) and JSPS (Japan Society for the Promotion of Science) Research for the Future program.

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Correspondence to Okihide Hikosaka.

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Kawagoe, R., Takikawa, Y. & Hikosaka, O. Expectation of reward modulates cognitive signals in the basal ganglia. Nat Neurosci 1, 411–416 (1998). https://doi.org/10.1038/1625

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