Non-canonical role for Lpar1-EGFP subplate neurons in early postnatal mouse somatosensory cortex

  1. Filippo Ghezzi
  2. Andre Marques-Smith
  3. Paul G Anastasiades
  4. Daniel Lyngholm
  5. Cristiana Vagnoni
  6. Alexandra Rowett
  7. Gokul Parameswaran
  8. Anna Hoerder-Suabedissen
  9. Yasushi Nakagawa
  10. Zoltan Molnar
  11. Simon J B Butt  Is a corresponding author
  1. University of Oxford, United Kingdom
  2. University of Bristol, United Kingdom
  3. Sensae, Germany
  4. University of Minnesota Medical School, United States

Abstract

Subplate neurons (SPNs) are thought to play a role in nascent sensory processing in neocortex. To better understand how heterogeneity within this population relates to emergent function, we investigated the synaptic connectivity of Lpar1-EGFP SPNs through the first postnatal week in whisker somatosensory cortex (S1BF). These SPNs comprise of two morphological subtypes: fusiform SPNs with local axons, and pyramidal SPNs with axons that extend through the marginal zone. The former receive translaminar synaptic input up until the emergence of the whisker barrels; a timepoint coincident with significant cell death. In contrast, pyramidal SPNs receive local input from the subplate at early ages but then – during the later time window, acquire input from overlying cortex. Combined electrical and optogenetic activation of thalamic afferents identified that Lpar1-EGFP SPNs receive sparse thalamic innervation. These data reveal components of the postnatal network that interpret sparse thalamic input to direct the emergent columnar structure of S1BF.

Data availability

All data generated and analysed during this study are available via the University of Oxford open access data repository (https://ora.ox.ac.uk)

Article and author information

Author details

  1. Filippo Ghezzi

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  2. Andre Marques-Smith

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6879-2858
  3. Paul G Anastasiades

    Neuroscience, University of Bristol, Bristol, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Daniel Lyngholm

    Sensae, 2100 Copenhagen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3708-0249
  5. Cristiana Vagnoni

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Alexandra Rowett

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  7. Gokul Parameswaran

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Anna Hoerder-Suabedissen

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Yasushi Nakagawa

    Department of Neuroscience, University of Minnesota Medical School, Minneapolis, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4876-5718
  10. Zoltan Molnar

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6852-6004
  11. Simon J B Butt

    Physiology, Anatomy & Genetics, University of Oxford, Oxford, United Kingdom
    For correspondence
    simon.butt@dpag.ox.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2399-0102

Funding

Wellcome Trust (215199/Z/19/Z)

  • Filippo Ghezzi

Wellcome Trust (086362/Z/08/Z)

  • Andre Marques-Smith

Medical Research Council (MR/K004387/1)

  • Simon J B Butt

Human Frontiers Science Program Organisation (CDA0023/2008-C)

  • Simon J B Butt

Brain and Behavior Research Foundation (19079)

  • Simon J B Butt

Wellcome Trust (089286/Z/09/Z)

  • Simon J B Butt

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 care and experimental procedures were approved by the University of Oxford local ethical review committee and conducted in accordance with UK Home Office personal and project (70/6767; 30/3052; P861F9BB75) licenses under the Animals (Scientific Procedures) 1986 Act.

Reviewing Editor

  1. Sonia Garel, Ecole Normale Superieure, France

Publication history

  1. Preprint posted: May 13, 2020 (view preprint)
  2. Received: July 7, 2020
  3. Accepted: July 9, 2021
  4. Accepted Manuscript published: July 12, 2021 (version 1)
  5. Accepted Manuscript updated: July 15, 2021 (version 2)
  6. Version of Record published: July 21, 2021 (version 3)

Copyright

© 2021, Ghezzi 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. Filippo Ghezzi
  2. Andre Marques-Smith
  3. Paul G Anastasiades
  4. Daniel Lyngholm
  5. Cristiana Vagnoni
  6. Alexandra Rowett
  7. Gokul Parameswaran
  8. Anna Hoerder-Suabedissen
  9. Yasushi Nakagawa
  10. Zoltan Molnar
  11. Simon J B Butt
(2021)
Non-canonical role for Lpar1-EGFP subplate neurons in early postnatal mouse somatosensory cortex
eLife 10:e60810.
https://doi.org/10.7554/eLife.60810

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