A connectome of a learning and memory center in the adult Drosophila brain
Open accessAbstract
Understanding memory formation, storage and retrieval requires knowledge of the underlying neuronal circuits. In Drosophila, the mushroom body (MB) is the major site of associative learning. We reconstructed the morphologies and synaptic connections of all 983 neurons within the three functional units, or compartments, that compose the adult MB’s α lobe, using a dataset of isotropic 8 nm voxels collected by focused ion-beam milling scanning electron microscopy. We found that Kenyon cells (KCs), whose sparse activity encodes sensory information, each make multiple en passant synapses to MB output neurons (MBONs) in each compartment. Some MBONs have inputs from all KCs, while others differentially sample sensory modalities. Only 6% of KC>MBON synapses receive a direct synapse from a dopaminergic neuron (DAN). We identified two unanticipated classes of synapses, KC>DAN and DAN>MBON. DAN activation produces a slow depolarization of the MBON in these DAN>MBON synapses and can weaken memory recall.
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The MBs are known to be a centre for learning and memory in the fly brain.
“For example, the MBs are known to be a centre for learning and memory in the fly brain32.”
From Network statistics of the whole-brain connectome of Drosophila (2024) · cites this paper as [32]
The higher post-synapse counts in the hemibrain mushroom body lobes are explained by certain connections, especially KC-to-KC connections, being much more prevalent in the hemibrain than in FlyWire.
“This appears to be explained by certain connections (especially KC to KC connections, which are predominantly arranged with an unusual rosette configuration along axons and of which the functional significance is poorly understood121) being much more prevalent in the hemibrain than in FlyWire (Extended Data Fig. 7d).”
From Whole-brain annotation and multi-connectome cell typing of Drosophila (2024) · cites this paper as [121]
Previous dense reconstructions have demonstrated that existing catalogs of cell types are incomplete, even in well-covered regions.
“Previous dense reconstructions have demonstrated that existing catalogs of cell types are incomplete, even in well-covered regions (Takemura et al., 2017).”
From A connectome and analysis of the adult Drosophila central brain (2020) · cites this paper as Takemura et al., 2017
Previous EM reconstructions were either dense in much smaller volumes or sparse in larger volumes.
“Previous reconstructions were either dense in much smaller EM volumes (such as Meinertzhagen and O'Neil, 1991; Helmstaedter et al., 2013; Takemura et al., 2017) or sparse in larger volumes (such as Eichler et al., 2017 or Zheng et al., 2018).”
From A connectome and analysis of the adult Drosophila central brain (2020) · cites this paper as Takemura et al., 2017
Two previous connectomics efforts are available as well.
“Two previous connectomics efforts are available as well (a seven-column optic lobe reconstruction [Takemura et al., 2015] and the alpha lobe of the mushroom body [Takemura et al., 2017]).”
From A connectome and analysis of the adult Drosophila central brain (2020) · cites this paper as Takemura et al., 2017
The least tightly bound large motif is a cell that connects either to or from (but not both) all cells of a given type; this motif is very common, with more than 500 examples in the fly's brain.
“The least tightly bound large motif is a cell that connects either to or from (but not both) all cells of a given type, as shown in Figure 22(c). Examples include the mushroom body output neurons (Takemura et al., 2017). This is a very common motif, found in many regions. We find more than 500 examples of this in the fly’s brain.”
From A connectome and analysis of the adult Drosophila central brain (2020) · cites this paper as Takemura et al., 2017
Broadcasters include a large number of Mi1 and Tm3 neurons-excitatory cells in the ME known to have key roles in the motion detection circuit.
“Broadcasters include a large number of Mi1 and Tm3 neurons—excitatory cells in the ME known to have key roles in the motion detection circuit32,40.”
From Network statistics of the whole-brain connectome of Drosophila (2024) · cites this paper as [32]
The Introduction (Figure 1) and Results (Cell type identification) describe mushroom-body circuits, not medulla motion-detection neurons. Searches for Mi1, Tm3, broadcasters, and the motion-detection circuit found no passage in our copy addressing the attributed claim. (LLM, conf=0.78)
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The Drosophila Split Gal4 System for Neural Circuit Mapping
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RETRACTED ARTICLE: Multisensory learning binds neurons into a cross-modal memory engram
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“This recent history gives us reason to expect that connectomics (Eichler et al., 2017; Ohyama et al., 2015; Schlegel et al., 2020; Takemura et al., 2017a; Takemura et al., 2017b; White et al., 1986; Zheng et al., 2018) will continue to accelerate studies of circuit function (Bentley et al., 2016;…”
BackgroundInfluentialSelf-citationReward signaling in a recurrent circuit of dopaminergic neurons and peptidergic Kenyon cells
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Dopamine-mediated interactions between short- and long-term memory dynamics
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NeuTu: Software for Collaborative, Large-Scale, Segmentation-Based Connectome Reconstruction
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Fully-Automatic Synapse Prediction and Validation on a Large Data Set
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Circuits for integrating learned and innate valences in the insect brain.
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The making of the Drosophila mushroom body
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Drosophila species learn dialects through communal living
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Predictive olfactory learning in Drosophila
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- Authors
- Takemura, S.-Y., Aso, Y., Hige, T., Wong, A., Lu, Z., Xu, C. S., Rivlin, P. K., Hess, H., Zhao, T., Parag, T., Berg, S., Huang, G., Katz, W., Olbris, D. J., Plaza, S., Umayam, L., Aniceto, R., Chang, L.-A., Lauchie, S., Ogundeyi, O., Ordish, C., Shinomiya, A., Sigmund, C., Takemura, S., Tran, J., Turner, G. C., Rubin, G. M., & Scheffer, L. K.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Takemura, Shin-ya
- Scheffer, Louis K
- ORCID
- Takemura, Shin-ya
- Aso, Yoshinori
- Hige, Toshihide
- Wong, Allan
- Lu, Zhiyuan
- Xu, C Shan
- Rivlin, Patricia K
- Hess, Harald
- Zhao, Ting
- Berg, Stuart
- Huang, Gary
- Katz, William
- Olbris, Donald J
- Plaza, Stephen
- Umayam, Lowell
- Aniceto, Roxanne
- Lauchie, Shirley
- Ogundeyi, Omotara
- Ordish, Christopher
- Shinomiya, Aya
- Takemura, Satoko
- Tran, Julie
- Turner, Glenn C
- Rubin, Gerald M
- Scheffer, Louis K
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2017-07-18
- Volume
- 6
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5550281
- OpenAlex
- W2737808707
- Cited by
- 367
- References
- 152
- Citations by year
- 2026: 16 · 2025: 18 · 2024: 44 · 2023: 32 · 2022: 35 · 2021: 47 · 2020: 59 · 2019: 54 · 2018: 53 · 2017: 8 · 2014: 1
- FWCI
- 23.30
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, 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
- 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, dopaminergic neurons, synaptic connectivity, memory retrieval, associative learning, Drosophila, connectome, neuronal morphology, sensory modality specificity
- MeSH terms
- Animals, Drosophila, Learning, Memory, Mushroom Bodies, Connectome
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