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Diversity of visual inputs to Kenyon cells of the Drosophila mushroom body

Author

Listed:
  • Ishani Ganguly

    (Columbia University
    Columbia University
    Columbia University)

  • Emily L. Heckman

    (University of Michigan)

  • Ashok Litwin-Kumar

    (Columbia University
    Columbia University
    Columbia University)

  • E. Josephine Clowney

    (University of Michigan
    University of Michigan)

  • Rudy Behnia

    (Columbia University
    Columbia University
    Columbia University)

Abstract

The arthropod mushroom body is well-studied as an expansion layer representing olfactory stimuli and linking them to contingent events. However, 8% of mushroom body Kenyon cells in Drosophila melanogaster receive predominantly visual input, and their function remains unclear. Here, we identify inputs to visual Kenyon cells using the FlyWire adult whole-brain connectome. Input repertoires are similar across hemispheres and connectomes with certain inputs highly overrepresented. Many visual neurons presynaptic to Kenyon cells have large receptive fields, while interneuron inputs receive spatially restricted signals that may be tuned to specific visual features. Individual visual Kenyon cells randomly sample sparse inputs from combinations of visual channels, including multiple optic lobe neuropils. These connectivity patterns suggest that visual coding in the mushroom body, like olfactory coding, is sparse, distributed, and combinatorial. However, the specific input repertoire to the smaller population of visual Kenyon cells suggests a constrained encoding of visual stimuli.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49616-z
    DOI: 10.1038/s41467-024-49616-z
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    References listed on IDEAS

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    1. Zeynep Okray & Pedro F. Jacob & Ciara Stern & Kieran Desmond & Nils Otto & Clifford B. Talbot & Paola Vargas-Gutierrez & Scott Waddell, 2023. "Multisensory learning binds neurons into a cross-modal memory engram," Nature, Nature, vol. 617(7962), pages 777-784, May.
    2. Gang Liu & Holger Seiler & Ai Wen & Troy Zars & Kei Ito & Reinhard Wolf & Martin Heisenberg & Li Liu, 2006. "Distinct memory traces for two visual features in the Drosophila brain," Nature, Nature, vol. 439(7076), pages 551-556, February.
    3. Sophie J. C. Caron & Vanessa Ruta & L. F. Abbott & Richard Axel, 2013. "Random convergence of olfactory inputs in the Drosophila mushroom body," Nature, Nature, vol. 497(7447), pages 113-117, May.
    4. Tyler A. Ofstad & Charles S. Zuker & Michael B. Reiser, 2011. "Visual place learning in Drosophila melanogaster," Nature, Nature, vol. 474(7350), pages 204-207, June.
    5. Kaitlyn Elizabeth Ellis & Sven Bervoets & Hayley Smihula & Ishani Ganguly & Eva Vigato & Thomas O. Auer & Richard Benton & Ashok Litwin-Kumar & Sophie Jeanne Cécile Caron, 2024. "Evolution of connectivity architecture in the Drosophila mushroom body," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    6. 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.
    7. Antoine Couto & Fletcher J. Young & Daniele Atzeni & Simon Marty & Lina Melo‐Flórez & Laura Hebberecht & Monica Monllor & Chris Neal & Francesco Cicconardi & W. Owen McMillan & Stephen H. Montgomery, 2023. "Rapid expansion and visual specialisation of learning and memory centres in the brains of Heliconiini butterflies," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Li Liu & Reinhard Wolf & Roman Ernst & Martin Heisenberg, 1999. "Context generalization in Drosophila visual learning requires the mushroom bodies," Nature, Nature, vol. 400(6746), pages 753-756, August.
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