Motor cortex can directly drive the globus pallidus neurons in a projection neuron type- dependent manner in the rat

  1. Fuyuki Karube  Is a corresponding author
  2. Susumu Takahashi
  3. Kenta Kobayashi
  4. Fumino Fujiyama  Is a corresponding author
  1. Doshisha University, Japan
  2. National Institute for Physiological Sciences, Japan

Abstract

The basal ganglia are critical for the control of motor behaviors and for reinforcement learning. Here, we demonstrate in rats that primary and secondary motor areas (M1 and M2) make functional synaptic connections in the globus pallidus (GP), not usually thought of as an input site of the basal ganglia. Morphological observation revealed that the density of axonal boutons from motor cortices in the GP was 47% and 78% of that in the subthalamic nucleus (STN) from M1 and M2, respectively. Cortical excitation of GP neurons was comparable to that of STN neurons in slice preparations. FoxP2-expressing arkypallidal neurons were preferentially innervated by the motor cortex. The connection probability of cortico-pallidal innervation was higher for M2 than M1. These results suggest that cortico-pallidal innervation is an additional excitatory input to the basal ganglia, and that it can affect behaviors via the cortex-basal ganglia-thalamus motor loop.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files in a Microsoft Exel format are provided for Table 2, for Figures 2C, 2D, 2E, 4A2, 4B2, 4B3, 4B4, 4C, 5B, 5C, 5D, 5F, 6A, 6B, 6C, 6D, and also for Figure 1-Figure supplement 2E, and Figure 2-Figure supplement 1D.

Article and author information

Author details

  1. Fuyuki Karube

    Laboratory of Neural Circuitry, Graduate School of Brain Science, Doshisha University, Kyotanabe, Japan
    For correspondence
    fkarube@mail.doshisha.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5365-3297
  2. Susumu Takahashi

    Laboratory of Neural Circuitry, Graduate School of Brain Science, Doshisha University, Kyotanabe, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Kenta Kobayashi

    Section of Viral Vector Development, National Institute for Physiological Sciences, Okazaki, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Fumino Fujiyama

    Laboratory of Neural Circuitry, Graduate School of Brain Science, Doshisha University, Kyotanabe, Japan
    For correspondence
    ffujiyam@mail.doshisha.ac.jp
    Competing interests
    The authors declare that no competing interests exist.

Funding

Japan Society for the Promotion of Science London (Grant-in-Aid for Scientific Research(S) 26350983)

  • Fuyuki Karube

Japan Society for the Promotion of Science London (Grant-in-Aid for Scientific Research(S) 16H01622)

  • Fuyuki Karube

Japan Society for the Promotion of Science London (Grant-in-Aid for Specially Promoted Research 16H06543)

  • Susumu Takahashi

Japan Society for the Promotion of Science London (Grant-in-Aid for Scientific Research(S) 16H02840)

  • Susumu Takahashi

Japan Society for the Promotion of Science London (Grant-in-Aid for Scientific Research(S) 25282247)

  • Fumino Fujiyama

Japan Society for the Promotion of Science London (Grant-in-Aid for Scientific Research(S) 15K12770)

  • Fumino Fujiyama

Japan Society for the Promotion of Science London (Scientific Researches on Innovative Areas 26112001)

  • Fumino Fujiyama

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: Animal experiments were approved and performed in accordance with the guidelines for the care and use of laboratory animals established by the Committee for Animal Care (Permit Number: A16008, A17001, A18001, A19036) and Use and the Committee for Recombinant DNA Study (Permit Number: D16008, D17001, D18001, D19036) of Doshisha University. All efforts were made to minimize animal suffering and the number of animals used.

Reviewing Editor

  1. Naoshige Uchida, Harvard University, United States

Publication history

  1. Received: June 20, 2019
  2. Accepted: October 29, 2019
  3. Accepted Manuscript published: November 12, 2019 (version 1)
  4. Version of Record published: November 19, 2019 (version 2)

Copyright

© 2019, Karube et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Fuyuki Karube
  2. Susumu Takahashi
  3. Kenta Kobayashi
  4. Fumino Fujiyama
(2019)
Motor cortex can directly drive the globus pallidus neurons in a projection neuron type- dependent manner in the rat
eLife 8:e49511.
https://doi.org/10.7554/eLife.49511
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