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Functional differences between macaque prefrontal cortex and caudate nucleus during eye movements with and without reward

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Abstract

The prefrontal cortex and the basal ganglia form mutually connected networks and are thought to play essential roles together in guiding goal-directed behaviors. Yet, these structures seem to have independent pathways to motor outputs as well, suggesting differential contributions to goal-directed behaviors. We hypothesized that the prefrontal cortex guides actions to a direction required by external demands and the basal ganglia guide actions to an internally motivated direction. To test this hypothesis, we used a task in which monkeys were required to make a memory-guided saccade to a direction indicated by a visual cue while only one direction was associated with reward. We observed a functional dissociation between the lateral prefrontal cortex (LPFC), which commonly represented the cue direction, and the caudate nucleus (CD), which commonly represented the reward-associated direction. Furthermore, cue-directed and reward-directed signals were integrated differently in the two areas; when the cue direction and the reward direction were opposite, LPFC neurons maintained tuning to the cue direction, whereas CD neurons lost the tuning. Different types of spatial tuning in the two brain areas may contribute to different types of goal-directed behavior.

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Acknowledgments

We thank Makoto Kato and Brian Coe for designing the computer programs and Hideaki Itoh for helpful discussions. SK is supported by Japan Society for the Promotion of Science (JSPS) Research Fellowships for Young Scientists. MS is supported by Precursory Research for Embryonic Science and Technology (PREST), Japan Science and Technology Corporation (JST).

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Authors and Affiliations

  1. Brain Science Research Center, Tamagawa University Research Institute, 6-1-1, Tamagawa gakuen, Machida, Tokyo, 194-8610, Japan

    Shunsuke Kobayashi, Masashi Koizumi & Masamichi Sakagami

  2. Department of Physiology, Juntendo University School of Medicine, 2-1-1, Hongo, Bunkyo-ku, Tokyo, 113-8421, Japan

    Reiko Kawagoe, Yoriko Takikawa & Masamichi Sakagami

  3. Laboratory of Sensorimotor Research, National Eye Institute, NIH, Bldg. 49, Room 2A50, Bethesda, MD, 20892, USA

    Okihide Hikosaka

  4. Department of Neurology, Division of Neuroscience, University of Tokyo Graduate School of Medicine, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8654, Japan

    Shunsuke Kobayashi

  5. Department of Physiology, Development and Neuroscience, University of Cambridge, Downing Street, Cambridge, CB2 3DY, UK

    Shunsuke Kobayashi

Authors
  1. Shunsuke Kobayashi
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  2. Reiko Kawagoe
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  3. Yoriko Takikawa
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  4. Masashi Koizumi
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  5. Masamichi Sakagami
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  6. Okihide Hikosaka
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Correspondence to Shunsuke Kobayashi.

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Kobayashi, S., Kawagoe, R., Takikawa, Y. et al. Functional differences between macaque prefrontal cortex and caudate nucleus during eye movements with and without reward. Exp Brain Res 176, 341–355 (2007). https://doi.org/10.1007/s00221-006-0622-4

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  • DOI: https://doi.org/10.1007/s00221-006-0622-4

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