1. Neuroscience

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
https://doi.org/10.7554/eLife.32373
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

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

  • 7,092
    views
  • 814
    downloads
  • 38
    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

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Dopamine increases protein synthesis in hippocampal neurons enabling dopamine-dependent LTP

    Tanja Fuchsberger, Imogen Stockwell ... Ole Paulsen
    Research Advance

    The reward and novelty-related neuromodulator dopamine plays an important role in hippocampal long-term memory, which is thought to involve protein-synthesis-dependent synaptic plasticity. However, the direct effects of dopamine on protein synthesis, and the functional implications of newly synthesised proteins for synaptic plasticity, have not yet been investigated. We have previously reported that timing-dependent synaptic depression (t-LTD) can be converted into potentiation by dopamine application during synaptic stimulation (Brzosko et al., 2015) or postsynaptic burst activation (Fuchsberger et al., 2022). Here, we show that dopamine increases protein synthesis in mouse hippocampal CA1 neurons, enabling dopamine-dependent long-term potentiation (DA-LTP), which is mediated via the Ca2+-sensitive adenylate cyclase (AC) subtypes 1/8, cAMP, and cAMP-dependent protein kinase (PKA). We found that neuronal activity is required for the dopamine-induced increase in protein synthesis. Furthermore, dopamine induced a protein-synthesis-dependent increase in the AMPA receptor subunit GluA1, but not GluA2. We found that DA-LTP is absent in GluA1 knock-out mice and that it requires calcium-permeable AMPA receptors. Taken together, our results suggest that dopamine together with neuronal activity controls synthesis of plasticity-related proteins, including GluA1, which enable DA-LTP via a signalling pathway distinct from that of conventional LTP.

    1. Neuroscience

    Aminergic and peptidergic modulation of insulin-producing cells in Drosophila

    Martina Held, Rituja S Bisen ... Jan M Ache
    Research Article

    Insulin plays a critical role in maintaining metabolic homeostasis. Since metabolic demands are highly dynamic, insulin release needs to be constantly adjusted. These adjustments are mediated by different pathways, most prominently the blood glucose level, but also by feedforward signals from motor circuits and different neuromodulatory systems. Here, we analyze how neuromodulatory inputs control the activity of the main source of insulin in Drosophila – a population of insulin-producing cells (IPCs) located in the brain. IPCs are functionally analogous to mammalian pancreatic beta cells, but their location makes them accessible for in vivo recordings in intact animals. We characterized functional inputs to IPCs using single-nucleus RNA sequencing analysis, anatomical receptor expression mapping, connectomics, and an optogenetics-based ‘intrinsic pharmacology’ approach. Our results show that the IPC population expresses a variety of receptors for neuromodulators and classical neurotransmitters. Interestingly, IPCs exhibit heterogeneous receptor profiles, suggesting that the IPC population can be modulated differentially. This is supported by electrophysiological recordings from IPCs, which we performed while activating different populations of modulatory neurons. Our analysis revealed that some modulatory inputs have heterogeneous effects on the IPC activity, such that they inhibit one subset of IPCs, while exciting another. Monitoring calcium activity across the IPC population uncovered that these heterogeneous responses occur simultaneously. Certain neuromodulatory populations shifted the IPC population activity towards an excited state, while others shifted it towards inhibition. Taken together, we provide a comprehensive, multi-level analysis of neuromodulation in the insulinergic system of Drosophila.