Embryonic and postnatal neurogenesis produce functionally distinct subclasses of dopaminergic neuron

  1. Elisa Galliano  Is a corresponding author
  2. Eleonora Franzoni
  3. Marine Breton
  4. Annisa N Chand
  5. Darren J Byrne
  6. Venkatesh N Murthy
  7. Matthew Grubb  Is a corresponding author
  1. King's College London, United Kingdom
  2. Harvard University, United States

Abstract

Most neurogenesis in the mammalian brain is completed embryonically, but in certain areas the production of neurons continues throughout postnatal life. The functional properties of mature postnatally-generated neurons often match those of their embryonically-produced counterparts. However, we show here that in the olfactory bulb (OB), embryonic and postnatal neurogenesis produce functionally distinct subpopulations of dopaminergic (DA) neurons. We define two subclasses of OB DA neuron by the presence or absence of a key subcellular specialisation: the axon initial segment (AIS). Large AIS-positive axon-bearing DA neurons are exclusively produced during early embryonic stages, leaving small anaxonic AIS-negative cells as the only DA subtype generated via adult neurogenesis. These populations are functionally distinct: large DA cells are more excitable, yet display weaker and - for certain long-latency or inhibitory events - more broadly-tuned responses to odorant stimuli. Embryonic and postnatal neurogenesis can therefore generate distinct neuronal subclasses, placing important constraints on the functional roles of adult-born neurons in sensory processing.

Data availability

The data is available at Dryad Digital Repository.

The following data sets were generated

Article and author information

Author details

  1. Elisa Galliano

    Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
    For correspondence
    elisa.galliano@kcl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6941-766X
  2. Eleonora Franzoni

    Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Marine Breton

    Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Annisa N Chand

    Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Darren J Byrne

    Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Venkatesh N Murthy

    Center for Brain Science, Harvard University, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2443-4252
  7. Matthew Grubb

    Centre for Developmental Neurobiology, Institute of Psychiatry, Psychology and Neuroscience (IoPPN), King's College London, London, United Kingdom
    For correspondence
    matthew.grubb@kcl.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2673-274X

Funding

Wellcome (103044)

  • Elisa Galliano

National Institutes of Health (DC013329)

  • Venkatesh N Murthy

European Research Council (725729 FUNCOPLAN)

  • Matthew Grubb

Wellcome (88301)

  • Matthew Grubb

Medical Research Council (MR/M501645/1)

  • Darren J Byrne

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

Ethics

Animal experimentation: All experiments were performed under the auspices of UK Home Office personal and project licences held by the authors (Project Licenses: 70/7246 and 70/8906), or were within institutional (Harvard University Institutional Animal Care and Use Committee; Animal Protocol 29/20)) and USA national guidelines.

Reviewing Editor

  1. Inna Slutsky, Tel Aviv University, Israel

Publication history

  1. Received: September 28, 2017
  2. Accepted: April 4, 2018
  3. Accepted Manuscript published: April 20, 2018 (version 1)
  4. Version of Record published: May 4, 2018 (version 2)

Copyright

© 2018, Galliano 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. Elisa Galliano
  2. Eleonora Franzoni
  3. Marine Breton
  4. Annisa N Chand
  5. Darren J Byrne
  6. Venkatesh N Murthy
  7. Matthew Grubb
(2018)
Embryonic and postnatal neurogenesis produce functionally distinct subclasses of dopaminergic neuron
eLife 7:e32373.
https://doi.org/10.7554/eLife.32373

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