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

Carlotta Pribbenow; Yi-chun Chen; M-Marcel Heim; Desiree Laber; Silas Reubold; Eric Reynolds; Isabella Balles; Tania Fernández-d V Alquicira; Raquel Suárez-Grimalt; Lisa Scheunemann; Carolin Rauch; Tanja Matkovic; Jörg Rösner; Gregor Lichtner; Sridhar R Jagannathan; David Owald

doi:10.7554/eLife.80445

eLife (Oct 2022)

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

Carlotta Pribbenow,
Yi-chun Chen,
M-Marcel Heim,
Desiree Laber,
Silas Reubold,
Eric Reynolds,
Isabella Balles,
Tania Fernández-d V Alquicira,
Raquel Suárez-Grimalt,
Lisa Scheunemann,
Carolin Rauch,
Tanja Matkovic,
Jörg Rösner,
Gregor Lichtner,
Sridhar R Jagannathan,
David Owald

Affiliations

Carlotta Pribbenow: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Yi-chun Chen: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
M-Marcel Heim: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Desiree Laber: Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Silas Reubold: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Eric Reynolds: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Isabella Balles: Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Tania Fernández-d V Alquicira: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Raquel Suárez-Grimalt: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Einstein Center for Neurosciences Berlin, Berlin, Germany
Lisa Scheunemann: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; NeuroCure, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Institut für Biologie, Freie Universität Berlin, Berlin, Germany
Carolin Rauch: Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
Tanja Matkovic: Institut für Biologie, Freie Universität Berlin, Berlin, Germany
Jörg Rösner: NWFZ, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Greifswald, Germany
Gregor Lichtner: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Universitätsmedizin Greifswald, Department of Anesthesia, Critical Care, Emergency and Pain Medicine, Greifswald, Germany
Sridhar R Jagannathan: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany
David Owald: ORCiD; Institute of Neurophysiology, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany; Einstein Center for Neurosciences Berlin, Berlin, Germany; NeuroCure, Charité – Universitätsmedizin Berlin, corporate member of Freie Universität Berlin and Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany

DOI: https://doi.org/10.7554/eLife.80445
Journal volume & issue: Vol. 11

Abstract

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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 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 discs large (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.

Published in eLife

ISSN: 2050-084X (Online)
Publisher: eLife Sciences Publications Ltd
Country of publisher: United Kingdom
LCC subjects: Medicine; Science: Biology (General)
Website: https://elifesciences.org

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