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A multilevel multimodal circuit enhances action selection in Drosophila

Author

Listed:
  • Tomoko Ohyama

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Casey M. Schneider-Mizell

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Richard D. Fetter

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Javier Valdes Aleman

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Romain Franconville

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Marta Rivera-Alba

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Brett D. Mensh

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Kristin M. Branson

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Julie H. Simpson

    (Howard Hughes Medical Institute Janelia Research Campus)

  • James W. Truman

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Albert Cardona

    (Howard Hughes Medical Institute Janelia Research Campus)

  • Marta Zlatic

    (Howard Hughes Medical Institute Janelia Research Campus)

Abstract

Natural events present multiple types of sensory cues, each detected by a specialized sensory modality. Combining information from several modalities is essential for the selection of appropriate actions. Key to understanding multimodal computations is determining the structural patterns of multimodal convergence and how these patterns contribute to behaviour. Modalities could converge early, late or at multiple levels in the sensory processing hierarchy. Here we show that combining mechanosensory and nociceptive cues synergistically enhances the selection of the fastest mode of escape locomotion in Drosophila larvae. In an electron microscopy volume that spans the entire insect nervous system, we reconstructed the multisensory circuit supporting the synergy, spanning multiple levels of the sensory processing hierarchy. The wiring diagram revealed a complex multilevel multimodal convergence architecture. Using behavioural and physiological studies, we identified functionally connected circuit nodes that trigger the fastest locomotor mode, and others that facilitate it, and we provide evidence that multiple levels of multimodal integration contribute to escape mode selection. We propose that the multilevel multimodal convergence architecture may be a general feature of multisensory circuits enabling complex input–output functions and selective tuning to ecologically relevant combinations of cues.

Suggested Citation

  • Tomoko Ohyama & Casey M. Schneider-Mizell & Richard D. Fetter & Javier Valdes Aleman & Romain Franconville & Marta Rivera-Alba & Brett D. Mensh & Kristin M. Branson & Julie H. Simpson & James W. Truma, 2015. "A multilevel multimodal circuit enhances action selection in Drosophila," Nature, Nature, vol. 520(7549), pages 633-639, April.
  • Handle: RePEc:nat:nature:v:520:y:2015:i:7549:d:10.1038_nature14297
    DOI: 10.1038/nature14297
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    Cited by:

    1. Nicole Pogodalla & Holger Kranenburg & Simone Rey & Silke Rodrigues & Albert Cardona & Christian Klämbt, 2021. "Drosophila ßHeavy-Spectrin is required in polarized ensheathing glia that form a diffusion-barrier around the neuropil," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    2. Stefano Recanatesi & Gabriel Koch Ocker & Michael A Buice & Eric Shea-Brown, 2019. "Dimensionality in recurrent spiking networks: Global trends in activity and local origins in connectivity," PLOS Computational Biology, Public Library of Science, vol. 15(7), pages 1-29, July.
    3. Máté Fellner & Bálint Varga & Vince Grolmusz, 2020. "The frequent complete subgraphs in the human connectome," PLOS ONE, Public Library of Science, vol. 15(8), pages 1-12, August.
    4. Mami Nakamizo-Dojo & Kenichi Ishii & Jiro Yoshino & Masato Tsuji & Kazuo Emoto, 2023. "Descending GABAergic pathway links brain sugar-sensing to peripheral nociceptive gating in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

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