1. Neuroscience
Download icon

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
Research Article
  • Cited 0
  • Views 485
  • Annotations
Cite this article as: eLife 2021;10:e60810 doi: 10.7554/eLife.60810

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.

Metrics

  • 485
    Page views
  • 54
    Downloads
  • 0
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

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)

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

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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Unsupervised changes in core object recognition behavior are predicted by neural plasticity in inferior temporal cortex

    Xiaoxuan Jia et al.
    Research Article Updated

    Temporal continuity of object identity is a feature of natural visual input and is potentially exploited – in an unsupervised manner – by the ventral visual stream to build the neural representation in inferior temporal (IT) cortex. Here, we investigated whether plasticity of individual IT neurons underlies human core object recognition behavioral changes induced with unsupervised visual experience. We built a single-neuron plasticity model combined with a previously established IT population-to-recognition-behavior-linking model to predict human learning effects. We found that our model, after constrained by neurophysiological data, largely predicted the mean direction, magnitude, and time course of human performance changes. We also found a previously unreported dependency of the observed human performance change on the initial task difficulty. This result adds support to the hypothesis that tolerant core object recognition in human and non-human primates is instructed – at least in part – by naturally occurring unsupervised temporal contiguity experience.

    1. Genetics and Genomics
    2. Neuroscience

    Neuropeptide ACP facilitates lipid oxidation and utilization during long-term flight in locusts

    Li Hou et al.
    Research Article Updated

    Long-term flight depends heavily on intensive energy metabolism in animals; however, the neuroendocrine mechanisms underlying efficient substrate utilization remain elusive. Here, we report that the adipokinetic hormone/corazonin-related peptide (ACP) can facilitate muscle lipid utilization in a famous long-term migratory flighting species, Locusta migratoria. By peptidomic analysis and RNAi screening, we identified brain-derived ACP as a key flight-related neuropeptide. ACP gene expression increased notably upon sustained flight. CRISPR/Cas9-mediated knockout of ACP gene and ACP receptor gene (ACPR) significantly abated prolonged flight of locusts. Transcriptomic and metabolomic analyses further revealed that genes and metabolites involved in fatty acid transport and oxidation were notably downregulated in the flight muscle of ACP mutants. Finally, we demonstrated that a fatty-acid-binding protein (FABP) mediated the effects of ACP in regulating muscle lipid metabolism during long-term flight in locusts. Our results elucidated a previously undescribed neuroendocrine mechanism underlying efficient energy utilization associated with long-term flight.

    1. Neuroscience

    Multiple neuronal networks coordinate Hydra mechanosensory behavior

    Krishna N Badhiwala et al.
    Research Article

    Hydra vulgaris is an emerging model organism for neuroscience due to its small size, transparency, genetic tractability, and regenerative nervous system; however, fundamental properties of its sensorimotor behaviors remain unknown. Here, we use microfluidic devices combined with fluorescent calcium imaging and surgical resectioning to study how the diffuse nervous system coordinates Hydra's mechanosensory response. Mechanical stimuli cause animals to contract, and we find this response relies on at least two distinct networks of neurons in the oral and aboral regions of the animal. Different activity patterns arise in these networks depending on whether the animal is contracting spontaneously or contracting in response to mechanical stimulation. Together, these findings improve our understanding of how Hydra’s diffuse nervous system coordinates sensorimotor behaviors. These insights help reveal how sensory information is processed in an animal with a diffuse, radially symmetric neural architecture unlike the dense, bilaterally symmetric nervous systems found in most model organisms.