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Nitric oxide acts as a cotransmitter in a subset of dopaminergic neurons to diversify memory dynamics
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Abstract
Animals employ diverse learning rules and synaptic plasticity dynamics to record temporal and statistical information about the world. However, the molecular mechanisms underlying this diversity are poorly understood. The anatomically defined compartments of the insect mushroom body function as parallel units of associative learning, with different learning rates, memory decay dynamics and flexibility (Aso and Rubin, 2016). Here, we show that nitric oxide (NO) acts as a neurotransmitter in a subset of dopaminergic neurons in Drosophila . NO’s effects develop more slowly than those of dopamine and depend on soluble guanylate cyclase in postsynaptic Kenyon cells. NO acts antagonistically to dopamine; it shortens memory retention and facilitates the rapid updating of memories. The interplay of NO and dopamine enables memories stored in local domains along Kenyon cell axons to be specialized for predicting the value of odors based only on recent events. Our results provide key mechanistic insights into how diverse memory dynamics are established in parallel memory systems.
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“Co-transmission of a fast-acting transmitter and a neuropeptide was more common, e.g., Kenyon cells (at least acetylcholine, sparkly and short neuropeptide F),21,25,55,164 the dorsal paired medial (DPM) neuron (GABA, serotonin, sparkly, nplp1, proctolin, orcokinin, eclosion hormone, CG34136)25,56,60 and most central complex, mushroom body output and mushroom body dopaminergic neurons.25,157”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [25]
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“Nitric oxide is used as a co-transmitter,25 we did not include it in our dataset.”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [25]
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“DPM has been found to express the fast-acting transmitter GABA the monoamine serotonin and several neuropeptides (sparkly, nplp1, proctolin, orcokinin, eclosion hormone, CG34136).25,56,60”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [25]
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“Kenyon cells may also express the neuropeptide sparkly.25,174”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [25]
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Metadata
- Authors
- Aso, Y., Ray, R. P., Long, X., Bushey, D., Cichewicz, K., Ngo, T.-T., Sharp, B., Christoforou, C., Hu, A., Lemire, A. L., Tillberg, P., Hirsh, J., Litwin-Kumar, A., & Rubin, G. M.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Virginia (US)
- Columbia University (US)
- Corresponding author
- Aso, Yoshinori
- Rubin, Gerald M
- ORCID
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2019-11-14
- Volume
- 8
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC6948953
- OpenAlex
- W2987761357
- Cited by
- 141
- References
- 148
- Citations by year
- 2026: 10 · 2025: 27 · 2024: 27 · 2023: 24 · 2022: 15 · 2021: 19 · 2020: 19
- FWCI
- 6.33
- Type
- journal article
- Language
- en
- Update notices
- correction (2020-10-22)
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (R01 GM84128)
- Simons Foundation (Global Brain)
- Burroughs Wellcome Fund
- Gatsby Charitable Foundation
- National Science Foundation (DBI-1707398)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- nitric oxide, co-transmitter, dopaminergic neurons, mushroom body, Kenyon cells, soluble guanylate cyclase, dopamine, memory dynamics, associative learning, memory updating, memory decay, parallel memory systems, Drosophila, odor prediction
- MeSH terms
- Animals, Dopamine, Drosophila melanogaster, Learning, Memory, Nitric Oxide, Odorants, Smell, Neurotransmitter Agents, Mushroom Bodies, Drosophila Proteins, Dopaminergic Neurons
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