Dual midbrain and forebrain origins of thalamic inhibitory interneurons

  1. Polona Jager
  2. Gerald Moore
  3. Padraic Calpin
  4. Xhuljana Durmishi
  5. Irene Salgarella
  6. Lucy Menage
  7. Yoshiaki Kita
  8. Yan Wang
  9. Dong Won Kim
  10. Seth Blackshaw
  11. Simon R Schultz
  12. Stephen Brickley
  13. Tomomi Shimogori
  14. Alessio Delogu  Is a corresponding author
  1. King's College London, United Kingdom
  2. Imperial College London, United Kingdom
  3. University College London, United Kingdom
  4. RIKEN, Japan
  5. Johns Hopkins University School of Medicine, United States
  6. Johns Hopkins University, United States
  7. Centor for Brain Science, Japan

Abstract

The ubiquitous presence of inhibitory interneurons in the thalamus of primates contrasts with the sparsity of interneurons reported in mice. Here, we identify a larger than expected complexity and distribution of interneurons across the mouse thalamus, where all thalamic interneurons can be traced back to two developmental programs: one specified in the midbrain and the other in the forebrain. Interneurons migrate to functionally distinct thalamocrtical nuclei depending on their origin: the abundant, midbrain-generated class populates the first and higher order sensory thalamus while the rarer, forebrain-generated class is restricted to some higher order associative regions. We also observe that markers for the midbrain-born class are abundantly expressed throughout the thalamus of the New World monkey marmoset. These data therefore reveal that, despite the broad variability in interneuron density across mammalian species, the blueprint of the ontogenetic organisation of thalamic interneurons of larger-brained mammals exists and can be studied in mice.

Data availability

All data generated or analysed during this study are included in the manuscript.

Article and author information

Author details

  1. Polona Jager

    Basic and Clinical Neuroscience, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Gerald Moore

    Department of Life Sciences, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Padraic Calpin

    Department of Physics and Astronomy, University College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Xhuljana Durmishi

    Basic and Clinical Neuroscience, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Irene Salgarella

    Basic and Clinical Neuroscience, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Lucy Menage

    Basic and Clinical Neuroscience, King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Yoshiaki Kita

    Center for Brain Science (CBS), RIKEN, Saitama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  8. Yan Wang

    Center for Brain Science (CBS), RIKEN, Saitama, Japan
    Competing interests
    The authors declare that no competing interests exist.
  9. Dong Won Kim

    Neuroscience, Johns Hopkins University School of Medicine, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Seth Blackshaw

    The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  11. Simon R Schultz

    Centre for Neurotechnology and Department of Bioengineering, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6794-5813
  12. Stephen Brickley

    Centre for Neurotechnology and Department of Bioengineering, Imperial College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  13. Tomomi Shimogori

    Laboratory for Molecular Mechanism of Brain Development, Centor for Brain Science, Wako, Japan
    Competing interests
    The authors declare that no competing interests exist.
  14. Alessio Delogu

    Basic and Clinical Neuroscience, King's College London, London, United Kingdom
    For correspondence
    alessio.delogu@kcl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4414-4714

Funding

Biotechnology and Biological Sciences Research Council (BB/L020068/1)

  • Alessio Delogu

Biotechnology and Biological Sciences Research Council (BB/R007020/1)

  • Alessio Delogu

Biotechnology and Biological Sciences Research Council (BB/R007659/1)

  • Stephen Brickley

Engineering and Physical Sciences Research Council (EP/J021199/1)

  • Simon R Schultz

Engineering and Physical Sciences Research Council (EP/L016737/1)

  • Gerald Moore

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

Ethics

Animal experimentation: Mice: Housing and experimental procedures were approved by the King's College London Ethical Committee and conformed to the regulations of the UK Home Office personal and project licences under the UK Animals (Scientific Procedures) 1986 Act.Marmoset: All experiments were conducted in accordance with the guidelines approved by the RIKEN Institutional Animal Care (W2020-2-022).

Reviewing Editor

  1. Sonia Garel, Ecole Normale Superieure, France

Publication history

  1. Received: May 24, 2020
  2. Accepted: January 31, 2021
  3. Accepted Manuscript published: February 1, 2021 (version 1)
  4. Version of Record published: February 25, 2021 (version 2)

Copyright

© 2021, Jager 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. Polona Jager
  2. Gerald Moore
  3. Padraic Calpin
  4. Xhuljana Durmishi
  5. Irene Salgarella
  6. Lucy Menage
  7. Yoshiaki Kita
  8. Yan Wang
  9. Dong Won Kim
  10. Seth Blackshaw
  11. Simon R Schultz
  12. Stephen Brickley
  13. Tomomi Shimogori
  14. Alessio Delogu
(2021)
Dual midbrain and forebrain origins of thalamic inhibitory interneurons
eLife 10:e59272.
https://doi.org/10.7554/eLife.59272

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