Cited by 370Neurobiology and Insect Physiology ResearchNeuroscience and Neuropharmacology ResearchMemory and Neural Mechanisms

A connectome of a learning and memory center in the adult Drosophila brain

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Takemura, Shin-ya, Aso, Yoshinori, Hige, Toshihide, Wong, Allan, Lu, Zhiyuan, Xu, C Shan, Rivlin, Patricia K, Hess, Harald +20 more·2017·eLife

Abstract

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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Crossref · 10.7554/elife.26975

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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.”
  • 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).”
  • 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

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1 of the 152 references couldn’t be matched to a known paper.

Research works printed but not linked: 4

  1. Eichler K LI, F Litwin-Kumar A Park Y Andrade I Schneider-Mizell C Saumweber T Huser A Eschbach C Gerber B Fetter RD Truman JW Priebe C Abbott LF Thum A Zlatic M Cardona A 2017 The complete wiring diagram of the larval Drosophila mushroom body Nature In press
  2. Qin H Cressy M Li W Coravos JS Izzi SA Dubnau J 2012b Gamma neurons mediate dopaminergic input during aversive olfactory memory formation in Drosophila Current Biology 22 608 614 10.1016/j.cub.2012.02.014 22425153 PMC3326180 · DOI
  3. Schürmann FW 1974 [On the functional anatomy of the corpora pedunculata in insects (author's transl)] Experimental Brain Research 19 406 432 4827867
  4. Yu D Keene AC Srivatsan A Waddell S Davis RL 2005b Drosophila DPM neurons form a delayed and branch-specific memory trace after olfactory classical conditioning Cell 123 945 957 10.1016/j.cell.2005.09.037 16325586 · DOI

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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
Venue
eLife
Published
2017-07-18
Volume
6
ISSN
2050-084X (ISSN-L)
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
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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