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The complete connectome of a learning and memory centre in an insect brain

Author

Listed:
  • Katharina Eichler

    (Howard Hughes Medical Institute Janelia Research Campus
    University of Konstanz)

  • Feng Li

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Ashok Litwin-Kumar

    (Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University)

  • Youngser Park

    (Whiting School of Engineering, Johns Hopkins University, 100 Whitehead Hall)

  • Ingrid Andrade

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Casey M. Schneider-Mizell

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Timo Saumweber

    (Leibniz Institut für Neurobiologie)

  • Annina Huser

    (University of Konstanz)

  • Claire Eschbach

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Bertram Gerber

    (Leibniz Institut für Neurobiologie
    Otto von Guericke Universität Magdeburg, Institut für Biologie, Verhaltensgenetik
    Otto-von-Guericke University Magdeburg, Center for Behavioral Brain Sciences)

  • Richard D. Fetter

    (Howard Hughes Medical Institute Janelia Research Campus)

  • James W. Truman

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Carey E. Priebe

    (Whiting School of Engineering, Johns Hopkins University, 100 Whitehead Hall)

  • L. F. Abbott

    (Mortimer B. Zuckerman Mind Brain Behavior Institute, Columbia University
    Columbia University, Russ Berrie Pavilion)

  • Andreas S. Thum

    (University of Konstanz
    University of Leipzig)

  • Marta Zlatic

    (Howard Hughes Medical Institute Janelia Research Campus
    University of Cambridge, Downing Street)

  • Albert Cardona

    (Howard Hughes Medical Institute Janelia Research Campus
    Development and Neuroscience, University of Cambridge)

Abstract

Associating stimuli with positive or negative reinforcement is essential for survival, but a complete wiring diagram of a higher-order circuit supporting associative memory has not been previously available. Here we reconstruct one such circuit at synaptic resolution, the Drosophila larval mushroom body. We find that most Kenyon cells integrate random combinations of inputs but that a subset receives stereotyped inputs from single projection neurons. This organization maximizes performance of a model output neuron on a stimulus discrimination task. We also report a novel canonical circuit in each mushroom body compartment with previously unidentified connections: reciprocal Kenyon cell to modulatory neuron connections, modulatory neuron to output neuron connections, and a surprisingly high number of recurrent connections between Kenyon cells. Stereotyped connections found between output neurons could enhance the selection of learned behaviours. The complete circuit map of the mushroom body should guide future functional studies of this learning and memory centre.

Suggested Citation

  • Katharina Eichler & Feng Li & Ashok Litwin-Kumar & Youngser Park & Ingrid Andrade & Casey M. Schneider-Mizell & Timo Saumweber & Annina Huser & Claire Eschbach & Bertram Gerber & Richard D. Fetter & J, 2017. "The complete connectome of a learning and memory centre in an insect brain," Nature, Nature, vol. 548(7666), pages 175-182, August.
  • Handle: RePEc:nat:nature:v:548:y:2017:i:7666:d:10.1038_nature23455
    DOI: 10.1038/nature23455
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    Cited by:

    1. Tao Guo & Shasha Li & Y. Norman Zhou & Wei D. Lu & Yong Yan & Yimin A. Wu, 2024. "Interspecies-chimera machine vision with polarimetry for real-time navigation and anti-glare pattern recognition," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Zhihao Zheng & Christopher S. Own & Adrian A. Wanner & Randal A. Koene & Eric W. Hammerschmith & William M. Silversmith & Nico Kemnitz & Ran Lu & David W. Tank & H. Sebastian Seung, 2024. "Fast imaging of millimeter-scale areas with beam deflection transmission electron microscopy," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    3. Chung, Jaewon & Bridgeford, Eric & Arroyo, Jesus & Pedigo, Benjamin D. & Saad-Eldin, Ali & Gopalakrishnan, Vivek & Xiang, Liang & Priebe, Carey E. & Vogelstein, Joshua T., 2020. "Statistical Connectomics," OSF Preprints ek4n3, Center for Open Science.
    4. Ishani Ganguly & Emily L. Heckman & Ashok Litwin-Kumar & E. Josephine Clowney & Rudy Behnia, 2024. "Diversity of visual inputs to Kenyon cells of the Drosophila mushroom body," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Fangmin Zhou & Alexandra-Madelaine Tichy & Bibi Nusreen Imambocus & Shreyas Sakharwade & Francisco J. Rodriguez Jimenez & Marco González Martínez & Ishrat Jahan & Margarita Habib & Nina Wilhelmy & Van, 2023. "Optimized design and in vivo application of optogenetically functionalized Drosophila dopamine receptors," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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