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. 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

    MRC Centre for Developmental Neurobiology, 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:" 0000-0002-3708-0249
  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

    MRC Centre for Developmental Neurobiology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Anna Hoerder-Suabedissen

    MRC Centre for Developmental Neurobiology, 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

    MRC Centre for Developmental Neurobiology, 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.

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.

Metrics

  • 1,630
    views
  • 182
    downloads
  • 11
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  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

Share this article

https://doi.org/10.7554/eLife.60810

Further reading

    1. Neuroscience
    François Osiurak, Giovanni Federico ... Mathieu Lesourd
    Research Article

    Our propensity to materiality, which consists in using, making, creating, and passing on technologies, has enabled us to shape the physical world according to our ends. To explain this proclivity, scientists have calibrated their lens to either low-level skills such as motor cognition or high-level skills such as language or social cognition. Yet, little has been said about the intermediate-level cognitive processes that are directly involved in mastering this materiality, that is, technical cognition. We aim to focus on this intermediate level for providing new insights into the neurocognitive bases of human materiality. Here, we show that a technical-reasoning process might be specifically at work in physical problem-solving situations. We found via two distinct neuroimaging studies that the area PF (parietal F) within the left parietal lobe is central for this reasoning process in both tool-use and non-tool-use physical problem-solving and can work along with social-cognitive skills to resolve day-to-day interactions that combine social and physical constraints. Our results demonstrate the existence of a specific cognitive module in the human brain dedicated to materiality, which might be the supporting pillar allowing the accumulation of technical knowledge over generations. Intensifying research on technical cognition could nurture a comprehensive framework that has been missing in fields interested in how early and modern humans have been interacting with the physical world through technology, and how this interaction has shaped our history and culture.

    1. Neuroscience
    Roshani Nhuchhen Pradhan, Craig Montell, Youngseok Lee
    Research Article

    The question as to whether animals taste cholesterol taste is not resolved. This study investigates whether the fruit fly, Drosophila melanogaster, is capable of detecting cholesterol through their gustatory system. We found that flies are indifferent to low levels of cholesterol and avoid higher levels. The avoidance is mediated by gustatory receptor neurons (GRNs), demonstrating that flies can taste cholesterol. The cholesterol-responsive GRNs comprise a subset that also responds to bitter substances. Cholesterol detection depends on five ionotropic receptor (IR) family members, and disrupting any of these genes impairs the flies' ability to avoid cholesterol. Ectopic expressions of these IRs in GRNs reveals two classes of cholesterol receptors, each with three shared IRs and one unique subunit. Additionally, expressing cholesterol receptors in sugar-responsive GRNs confers attraction to cholesterol. This study reveals that flies can taste cholesterol, and that the detection depends on IRs in GRNs.