Thalamocortical axons control the cytoarchitecture of neocortical layers by area-specific supply of VGF

  1. Haruka Sato  Is a corresponding author
  2. Jun Hatakeyama
  3. Takuji Iwasato
  4. Kimi Araki
  5. Nobuhiko Yamamoto
  6. Kenji Shimamura  Is a corresponding author
  1. Kumamoto University, Japan
  2. National Institute of Genetics, Japan
  3. Osaka University, Japan

Abstract

Neuronal abundance and thickness of each cortical layer is specific to each area, but how this fundamental feature arises during development remains poorly understood. While some of area-specific features are controlled by intrinsic cues such as morphogens and transcription factors, the exact influence and mechanisms of action by cues extrinsic to the cortex, in particular the thalamic axons, have not been fully established. Here we identify a thalamus-derived factor, VGF, which is indispensable for thalamocortical axons to maintain the proper amount of layer 4 neurons in the mouse sensory cortices. This process is prerequisite for further maturation of the primary somatosensory area, such as barrel field formation instructed by a neuronal activity-dependent mechanism. Our results provide an actual case in which highly site-specific axon projection confers further regional complexity upon the target field through locally secreting signaling molecules from axon terminals.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files; Source data files have been provided for Figures 1-7 and Figure 1-figure supplement 1, Figure 2-figure supplement 1, 2, Figure 5-figure supplment 2, Figure 7-figure supplement 1, 2.

Article and author information

Author details

  1. Haruka Sato

    Department of Brain Morphogenesis, Kumamoto University, Kumamoto, Japan
    For correspondence
    stharuka@kumamoto-u.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6839-0146
  2. Jun Hatakeyama

    Department of Brain Morphogenesis, Kumamoto University, Kumamoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  3. Takuji Iwasato

    Laboratory of Mammalian Neural Circuits, National Institute of Genetics, Mishima, Japan
    Competing interests
    The authors declare that no competing interests exist.
  4. Kimi Araki

    Department of Brain Morphogenesis, Kumamoto University, Kumamoto, Japan
    Competing interests
    The authors declare that no competing interests exist.
  5. Nobuhiko Yamamoto

    Laboratory of Cellular and Molecular Neurobiology, Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan
    Competing interests
    The authors declare that no competing interests exist.
  6. Kenji Shimamura

    Department of Brain Morphogenesis, Kumamoto University, Kumamoto, Japan
    For correspondence
    simamura@kumamoto-u.ac.jp
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7102-6513

Funding

Japan Society for the Promotion of Science (KM101-2587054400)

  • Haruka Sato

Ministry of Education, Culture, Sports, Science and Technology (JP16H06276)

  • Kimi Araki

Ministry of Education, Culture, Sports, Science and Technology (18GS0329-01)

  • Kenji Shimamura

Ministry of Education, Culture, Sports, Science and Technology (JP16K07375)

  • Kenji Shimamura

Japan Society for the Promotion of Science (KM100-2633200)

  • Haruka Sato

Japan Society for the Promotion of Science (KM101-18K1483900)

  • Haruka Sato

Ministry of Education, Culture, Sports, Science and Technology (JP06J08049)

  • Jun Hatakeyama

Ministry of Education, Culture, Sports, Science and Technology (JP21870030)

  • Jun Hatakeyama

Ministry of Education, Culture, Sports, Science and Technology (JP24790288)

  • Jun Hatakeyama

Ministry of Education, Culture, Sports, Science and Technology (JP15K19011)

  • Jun Hatakeyama

Ministry of Education, Culture, Sports, Science and Technology (JP16H01449)

  • Jun Hatakeyama

Ministry of Education, Culture, Sports, Science and Technology (JP17H05771)

  • Jun Hatakeyama

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

Ethics

Animal experimentation: This study was performed in strict accordance with the guidelines for laboratory animals of Kumamoto University and the Japan Neuroscience Society. All of the animals were handled according to approved institutional animal care and protocols by the Committee on the Ethics of Animal Experiments of Kumamoto University (Permit Number: 27-124, A29-080, 2019-110, 2020-055). All surgery was performed under sodium pentobarbital anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. Carol A Mason, Columbia University, United States

Version history

  1. Preprint posted: February 14, 2021 (view preprint)
  2. Received: February 15, 2021
  3. Accepted: March 12, 2022
  4. Accepted Manuscript published: March 15, 2022 (version 1)
  5. Version of Record published: March 28, 2022 (version 2)

Copyright

© 2022, Sato 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. Haruka Sato
  2. Jun Hatakeyama
  3. Takuji Iwasato
  4. Kimi Araki
  5. Nobuhiko Yamamoto
  6. Kenji Shimamura
(2022)
Thalamocortical axons control the cytoarchitecture of neocortical layers by area-specific supply of VGF
eLife 11:e67549.
https://doi.org/10.7554/eLife.67549

Share this article

https://doi.org/10.7554/eLife.67549

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