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New Cerebello-Cortical Pathway Involved in Higher-Order Oculomotor Control

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Abstract

The cerebellum and the basal ganglia play an important role in the control of voluntary eye movement associated with complex behavior, but little is known about how cerebellar projections project to cortical eye movement areas. Here we used retrograde transneuronal transport of rabies virus to identify neurons in the cerebellar nuclei that project via the thalamus to supplementary eye field (SEF) of the frontal cortex of macaques. After rabies injections into the SEF, many neurons in the restricted region, the ventral aspects of the dentate nucleus (DN), the caudal pole of the DN, and the posterior interpositus nucleus (PIN) were labeled disynaptically via the thalamus, whereas no neuron labeling was found in the anterior interpositus nucleus (AIN). The distribution of the labeled neurons was dorsoventrally different from that of DN and PIN neurons labeled from the motor cortex. In the basal ganglia, a large number of labeled neurons were confined to the dorsomedial portion of the internal segment of the globus pallidus (GPi) as more neurons were labeled in the inner portion of the GPi (GPii) than in the outer portion of the GPi (GPio). This is the first evidence of a projection between cerebellum/basal ganglia and the SEF that could enable the cerebellum to modulate the cognitive control of voluntary eye movement.

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Funding

This work was supported by Scientific Research (18500247 and 20500293) to X.L. from the Ministry of Education, Culture, Sports, Science, and Technology of Japan.

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Authors and Affiliations

  1. Department of Neuroscience, University of Minnesota, Minneapolis, MN, 55414, USA

    Xiaofeng Lu

  2. Brain Science Center, Veterans Administration Medical Center, One Veterans Drive, Bldg 49, Rm 240, Minneapolis, MN, 55417-2399, USA

    Xiaofeng Lu

  3. Department of Neurophysiology, School of Medicine, Juntendo University, Tokyo, 113-8421, Japan

    Xiaofeng Lu, Shogo Ohmae & Yusuke Uchida

  4. Systems Neuroscience Section, Department of Neuroscience, Primate Research Institute, Kyoto University, Inuyama, Aichi, 484-8506, Japan

    Ken-ichi Inoue

  5. Department of Neuroscience, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA

    Shogo Ohmae

  6. Department of Science and Technology, Meijo University 1-501 Shiogamaguchi, Tempaku, Nagoya, 468-8502, Japan

    Yusuke Uchida

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  1. Xiaofeng Lu
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  2. Ken-ichi Inoue
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Contributions

X.L. designed the study, performed all the physiological and anatomical procedures. KI, SO and YU performed parts of the experiment and data analysis and wrote the manuscript together with XL. We truly thank Dr. Okihide Hikosaka for helpful discussion on story, Dr. Masahiko Takada for providing the experimental environment for viral injection, and Drs. James Ashe and Masahiko Takada made the helpful comments on the manuscript. The authors have declared that no competing interests exist.

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Correspondence to Xiaofeng Lu.

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This article does not contain any studies with human performed by any of the authors. All procedures performed in studies involving animals were in accordance with the ethical standards of the Guiding Principles for the Care and Use of Animals, approved by the Council of the Physiological Society of Japan. All experiments were approved by the Committee for Animal Experimentation of Juntendo University School of Medicine and Tokyo Metropolitan Institute for Neuroscience.

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Lu, X., Inoue, Ki., Ohmae, S. et al. New Cerebello-Cortical Pathway Involved in Higher-Order Oculomotor Control. Cerebellum 19, 401–408 (2020). https://doi.org/10.1007/s12311-020-01108-8

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