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Rapid threat assessment in the Drosophila thermosensory system

Author

Listed:
  • Genevieve C. Jouandet

    (Northwestern University)

  • Michael H. Alpert

    (Northwestern University)

  • José Miguel Simões

    (Northwestern University)

  • Richard Suhendra

    (Northwestern University)

  • Dominic D. Frank

    (Northwestern University
    The Rockefeller University)

  • Joshua I. Levy

    (Northwestern University
    The Scripps Research Institute)

  • Alessia Para

    (Northwestern University)

  • William L. Kath

    (Northwestern University
    Northwestern University
    National Institute for Theory and Mathematics in Biology, Northwestern University)

  • Marco Gallio

    (Northwestern University)

Abstract

Neurons that participate in sensory processing often display “ON” responses, i.e., fire transiently at the onset of a stimulus. ON transients are widespread, perhaps universal to sensory coding, yet their function is not always well-understood. Here, we show that ON responses in the Drosophila thermosensory system extrapolate the trajectory of temperature change, priming escape behavior if unsafe thermal conditions are imminent. First, we show that second-order thermosensory projection neurons (TPN-IIIs) and their Lateral Horn targets (TLHONs), display ON responses to thermal stimuli, independent of direction of change (heating or cooling) and of absolute temperature. Instead, they track the rate of temperature change, with TLHONs firing exclusively to rapid changes (>0.2 °C/s). Next, we use connectomics to track TLHONs’ output to descending neurons that control walking and escape, and modeling and genetic silencing to demonstrate how ON transients can flexibly amplify aversive responses to small thermal change. Our results suggest that, across sensory systems, ON transients may represent a general mechanism to systematically anticipate and respond to salient or dangerous conditions.

Suggested Citation

  • Genevieve C. Jouandet & Michael H. Alpert & José Miguel Simões & Richard Suhendra & Dominic D. Frank & Joshua I. Levy & Alessia Para & William L. Kath & Marco Gallio, 2023. "Rapid threat assessment in the Drosophila thermosensory system," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42864-5
    DOI: 10.1038/s41467-023-42864-5
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    References listed on IDEAS

    as
    1. Ricardo Zacarias & Shigehiro Namiki & Gwyneth M. Card & Maria Luisa Vasconcelos & Marta A. Moita, 2018. "Speed dependent descending control of freezing behavior in Drosophila melanogaster," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    2. Wendy W. Liu & Ofer Mazor & Rachel I. Wilson, 2015. "Thermosensory processing in the Drosophila brain," Nature, Nature, vol. 519(7543), pages 353-357, March.
    3. Dominic D. Frank & Genevieve C. Jouandet & Patrick J. Kearney & Lindsey J. Macpherson & Marco Gallio, 2015. "Temperature representation in the Drosophila brain," Nature, Nature, vol. 519(7543), pages 358-361, March.
    4. Vanessa Ruta & Sandeep Robert Datta & Maria Luisa Vasconcelos & Jessica Freeland & Loren L. Looger & Richard Axel, 2010. "A dimorphic pheromone circuit in Drosophila from sensory input to descending output," Nature, Nature, vol. 468(7324), pages 686-690, December.
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