Memory-Relevant Mushroom Body Output Synapses Are Cholinergic
Open accessAbstract
Memories are stored in the fan-out fan-in neural architectures of the mammalian cerebellum and hippocampus and the insect mushroom bodies. However, whereas key plasticity occurs at glutamatergic synapses in mammals, the neurochemistry of the memory-storing mushroom body Kenyon cell output synapses is unknown. Here we demonstrate a role for acetylcholine (ACh) in Drosophila. Kenyon cells express the ACh-processing proteins ChAT and VAChT, and reducing their expression impairs learned olfactory-driven behavior. Local ACh application, or direct Kenyon cell activation, evokes activity in mushroom body output neurons (MBONs). MBON activation depends on VAChT expression in Kenyon cells and is blocked by ACh receptor antagonism. Furthermore, reducing nicotinic ACh receptor subunit expression in MBONs compromises odor-evoked activation and redirects odor-driven behavior. Lastly, peptidergic corelease enhances ACh-evoked responses in MBONs, suggesting an interaction between the fast- and slow-acting transmitters. Therefore, olfactory memories in Drosophila are likely stored as plasticity of cholinergic synapses.
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Co-transmission of a fast-acting transmitter and a neuropeptide was more common.
“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 [55]
The Discussion (page not available) says that αβ and γ Kenyon cells can corelease acetylcholine with the sNPF neuropeptide, supporting the Kenyon-cell example of fast-transmitter and neuropeptide co-transmission. The cited paper does not establish that such co-transmission was “more common,” nor does the relevant passage identify sparkly as a Kenyon-cell transmitter. (LLM, conf=0.84)
Experimental — accuracy not yet measuredImmunohistochemistry and RNA sequencing data have shown that Kenyon cells express the machinery necessary for cholinergic transmission.
“Immunohistochemistry and RNA sequencing data have shown that Kenyon cells express the machinery necessary for cholinergic transmission.21,55,164”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [55]
The Results section (“Drosophila Kenyon Cell Function Requires ChAT Expression”; page unavailable) reports immunohistochemical evidence that Kenyon cells express ChAT and VAChT, proteins needed for cholinergic transmission. It also cites microarray-based gene-expression data, not RNA sequencing data, so this source does not support the claim’s RNA-sequencing method. (LLM, conf=0.88)
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Arena, P., Calí, M., Patané, L., Portera, A., & Spinosa, A. G. (2018) · Nonlinear Dynamics · doi:10.1007/s11071-018-4673-4 · Cited by 12 · see citing works
Optogenetics: Illuminating neuronal circuits of memory formation
Ehmann, N., & Pauls, D. (2020) · Journal of Neurogenetics · doi:10.1080/01677063.2019.1708352 · Cited by 11 · see citing works
Christesen, D., Yang, Y. T., Chen, W., Batterham, P., & Perry, T. (2021) · Genetics · doi:10.1093/genetics/iyab112 · Cited by 11 · see citing works
Gerber, B., König, C., Fendt, M., Andreatta, M., Romanos, M., Pauli, P., & Yarali, A. (2019) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2018.12.001 · Cited by 11 · see citing works
- Authors
- Barnstedt, O., Owald, D., Felsenberg, J., Brain, R., Moszynski, J.-P., Talbot, C. B., Perrat, P. N., & Waddell, S.
- Affiliations
- University of Oxford (GB)
- University of Massachusetts Chan Medical School (US)
- Corresponding author
- Owald, David
- Waddell, Scott
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2016-03
- Volume
- 89
- Issue
- 6
- Pages
- 1237-1247
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC4819445
- OpenAlex
- W2290925166
- Cited by
- 197
- References
- 91
- Citations by year
- 2026: 9 · 2025: 15 · 2024: 20 · 2023: 28 · 2022: 17 · 2021: 21 · 2020: 22 · 2019: 17 · 2018: 19 · 2017: 21 · 2016: 8
- FWCI
- 12.19
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Neuron (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion, cc-by)
- Funders
- Wellcome Trust (090309/Z/09/Z, 090924)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- mushroom body, Kenyon cells, mushroom body output neurons, acetylcholine, cholinergic synapses, nicotinic acetylcholine receptors, vesicular acetylcholine transporter, choline acetyltransferase, olfactory memory, synaptic plasticity, Drosophila
- MeSH terms
- Animals, Animals, Newborn, Calcium, Choline O-Acetyltransferase, Conditioning, Classical, Drosophila, Gene Expression Regulation, Glutamate Decarboxylase, Memory, Neurons, Synapses, Transcription Factors, Cholinergic Agents, Mushroom Bodies, Drosophila Proteins, Animals, Genetically Modified, RNA Interference, Vesicular Acetylcholine Transport Proteins, Vesicular Inhibitory Amino Acid Transport Proteins, Vesicular Glutamate Transport Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
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