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.

Reviewing Editor

  1. Inna Slutsky, Tel Aviv University, Israel

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.

Version 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.

Metrics

  • 6,575
    views
  • 774
    downloads
  • 31
    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. 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

Share this article

https://doi.org/10.7554/eLife.32373

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Kenneth Chiou, Noah Snyder-Mackler
    Insight

    Single-cell RNA sequencing reveals the extent to which marmosets carry genetically distinct cells from their siblings.

    1. Neuroscience
    Flavio J Schmidig, Simon Ruch, Katharina Henke
    Research Article

    We are unresponsive during slow-wave sleep but continue monitoring external events for survival. Our brain wakens us when danger is imminent. If events are non-threatening, our brain might store them for later consideration to improve decision-making. To test this hypothesis, we examined whether novel vocabulary consisting of simultaneously played pseudowords and translation words are encoded/stored during sleep, and which neural-electrical events facilitate encoding/storage. An algorithm for brain-state-dependent stimulation selectively targeted word pairs to slow-wave peaks or troughs. Retrieval tests were given 12 and 36 hr later. These tests required decisions regarding the semantic category of previously sleep-played pseudowords. The sleep-played vocabulary influenced awake decision-making 36 hr later, if targeted to troughs. The words’ linguistic processing raised neural complexity. The words’ semantic-associative encoding was supported by increased theta power during the ensuing peak. Fast-spindle power ramped up during a second peak likely aiding consolidation. Hence, new vocabulary played during slow-wave sleep was stored and influenced decision-making days later.