Inhibitory muscarinic acetylcholine receptors enhance aversive olfactory learning in adult Drosophila

  1. Noa Bielopolski
  2. Hoger Amin
  3. Anthi A Apostolopoulou
  4. Eyal Rozenfeld
  5. Hadas Lerner
  6. Wolf Huetteroth
  7. Andrew C Lin  Is a corresponding author
  8. Moshe Parnas  Is a corresponding author
  1. Tel Aviv University, Israel
  2. University of Sheffield, United Kingdom
  3. University of Leipzig, Germany

Abstract

Olfactory associative learning in Drosophila is mediated by synaptic plasticity between the Kenyon cells of the mushroom body and their output neurons. Both Kenyon cells and their inputs from projection neurons are cholinergic, yet little is known about the physiological function of muscarinic acetylcholine receptors in learning in adult flies. Here we show that aversive olfactory learning in adult flies requires type A muscarinic acetylcholine receptors (mAChR-A), particularly in the gamma subtype of Kenyon cells. mAChR-A inhibits odor responses and is localized in Kenyon cell dendrites. Moreover, mAChR-A knockdown impairs the learning-associated depression of odor responses in a mushroom body output neuron. Our results suggest that mAChR-A function in Kenyon cell dendrites is required for synaptic plasticity between Kenyon cells and their output neurons.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for Figures 1-8 and Figures S1, S8.

Article and author information

Author details

  1. Noa Bielopolski

    Department of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    The authors declare that no competing interests exist.
  2. Hoger Amin

    Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7884-4815
  3. Anthi A Apostolopoulou

    Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Eyal Rozenfeld

    Department of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Hadas Lerner

    Department of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Wolf Huetteroth

    Institute for Biology, University of Leipzig, Leipzig, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Andrew C Lin

    Department of Biomedical Science, University of Sheffield, Sheffield, United Kingdom
    For correspondence
    andrew.lin@sheffield.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
  8. Moshe Parnas

    Department of Physiology and Pharmacology, Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel
    For correspondence
    mparnas@tauex.tau.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9726-1511

Funding

European Commission (676844)

  • Moshe Parnas

European Commission (639489)

  • Andrew C Lin

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

Reviewing Editor

  1. Mani Ramaswami, Trinity College Dublin, Ireland

Publication history

  1. Received: May 7, 2019
  2. Accepted: June 18, 2019
  3. Accepted Manuscript published: June 19, 2019 (version 1)
  4. Version of Record published: July 19, 2019 (version 2)

Copyright

© 2019, Bielopolski 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. Noa Bielopolski
  2. Hoger Amin
  3. Anthi A Apostolopoulou
  4. Eyal Rozenfeld
  5. Hadas Lerner
  6. Wolf Huetteroth
  7. Andrew C Lin
  8. Moshe Parnas
(2019)
Inhibitory muscarinic acetylcholine receptors enhance aversive olfactory learning in adult Drosophila
eLife 8:e48264.
https://doi.org/10.7554/eLife.48264

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