Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila

Abstract

In vertebrates, several forms of memory-relevant synaptic plasticity involve postsynaptic rearrangements of glutamate receptors. In contrast, previous work indicates that Drosophila and other invertebrates store memories using presynaptic plasticity of cholinergic synapses. Here, we provide evidence for postsynaptic plasticity at cholinergic output synapses from the Drosophila mushroom bodies (MBs). We find that the nicotinic acetylcholine receptor (nAChR) subunit α5 is required within specific MB output neurons (MBONs) for appetitive memory induction, but is dispensable for aversive memories. In addition, nAChR α2 subunits mediate memory expression and likely function downstream of α5 and the postsynaptic scaffold protein Dlg. We show that postsynaptic plasticity traces can be induced independently of the presynapse, and that in vivo dynamics of α2 nAChR subunits are changed both in the context of associative and non-associative (familiarity) memory formation, underlying different plasticity rules. Therefore, regardless of neurotransmitter identity, key principles of postsynaptic plasticity support memory storage across phyla.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

The following previously published data sets were used

Article and author information

Author details

  1. Carlotta Pribbenow

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  2. Yi-chun Chen

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9187-930X
  3. Michael-Marcel Heim

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Desiree Laber

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Silas Reubold

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Eric Reynolds

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  7. Isabella Balles

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Tania Fernández-d.V. Alquicira

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Raquel Suárez-Grimalt

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5374-7963
  10. Lisa Scheunemann

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Carolin Rauch

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Tanja Matkovic

    Institute for Biology, Freie Universität Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Jörg Rösner

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Gregor Lichtner

    Department of Anesthesia, University of Greifswald, Greifswald, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Sridhar R Jagannathan

    Institute of Neurophysiology, Charité - Universitätsmedizin Berlin, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  16. David Owald

    NeuroCure, Charité - Universitätsmedizin Berlin, Berlin, Germany
    For correspondence
    david.owald@charite.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7747-7884

Funding

Deutsche Forschungsgemeinschaft (390688087)

  • David Owald

Deutsche Forschungsgemeinschaft (184695641)

  • David Owald

Deutsche Forschungsgemeinschaft (327654276)

  • David Owald

Deutsche Forschungsgemeinschaft (365082554)

  • David Owald

Deutsche Forschungsgemeinschaft

  • Sridhar R Jagannathan

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

Reviewing Editor

  1. Patrik Verstreken, KU Leuven, Belgium

Publication history

  1. Received: May 20, 2022
  2. Preprint posted: July 16, 2022 (view preprint)
  3. Accepted: October 17, 2022
  4. Accepted Manuscript published: October 17, 2022 (version 1)

Copyright

© 2022, Pribbenow 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. Carlotta Pribbenow
  2. Yi-chun Chen
  3. Michael-Marcel Heim
  4. Desiree Laber
  5. Silas Reubold
  6. Eric Reynolds
  7. Isabella Balles
  8. Tania Fernández-d.V. Alquicira
  9. Raquel Suárez-Grimalt
  10. Lisa Scheunemann
  11. Carolin Rauch
  12. Tanja Matkovic
  13. Jörg Rösner
  14. Gregor Lichtner
  15. Sridhar R Jagannathan
  16. David Owald
(2022)
Postsynaptic plasticity of cholinergic synapses underlies the induction and expression of appetitive and familiarity memories in Drosophila
eLife 11:e80445.
https://doi.org/10.7554/eLife.80445

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