Article

TRPA1 mediates sensation of the rate of temperature change in Drosophila larvae

  • Nature Neuroscience volume 20, pages 3441 (2017)
  • doi:10.1038/nn.4416
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Abstract

Avoidance of noxious ambient heat is crucial for survival. A well-known phenomenon is that animals are sensitive to the rate of temperature change. However, the cellular and molecular underpinnings through which animals sense and respond much more vigorously to fast temperature changes are unknown. Using Drosophila larvae, we found that nociceptive rolling behavior was triggered at lower temperatures and at higher frequencies when the temperature increased rapidly. We identified neurons in the brain that were sensitive to the speed of the temperature increase rather than just to the absolute temperature. These cellular and behavioral responses depended on the TRPA1 channel, whose activity responded to the rate of temperature increase. We propose that larvae use low-threshold sensors in the brain to monitor rapid temperature increases as a protective alert signal to trigger rolling behaviors, allowing fast escape before the temperature of the brain rises to dangerous levels.

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Acknowledgements

We thank M. Macdonald (UC Santa Barbara) and H. Luo (Shanghai Jiao Tong University) for assistance in generating the knock-in fly lines; J. Liu and H. Chen (UC Santa Barbara) for assistance in performing blind optogenetic experiments; B. Afonso (Janelia Research Campus), M. Zlatic (Janelia Research Campus), M. Gershow (Harvard University) and A.D.T. Samuel (Harvard University) for help building the software and hardware for the larval tracking system; W.D. Tracey (Indiana University) for trpA1-BAC (ref. 14); K. Scott (UC Berkeley) for GRASP flies36; P.A. Garrity (Brandeis University) for the pOX-trpA1-A construct43; and G.M. Rubin and J.W. Truman (Janelia Research Campus) for the expression data corresponding to the adult and larval Janelia GAL4 lines. W.L.S. was supported by National Nature Science Foundation of China (X-0402-14-002). This work was supported by grants to C.M. from the National Eye Institute (EY010852) and the National Institute on Deafness and Other Communication Disorders (DC007864).

Author information

Author notes

    • Wei L Shen

    Present address: ShanghaiTech University, Shanghai, China.

Affiliations

  1. Neuroscience Research Institute, University of California Santa Barbara, Santa Barbara, California, USA.

    • Junjie Luo
    •  & Craig Montell
  2. Department of Molecular, Cellular and Developmental Biology, University of California Santa Barbara, Santa Barbara, California, USA.

    • Junjie Luo
    •  & Craig Montell
  3. Department of Biological Chemistry, The Johns Hopkins University School of Medicine, Baltimore, Maryland, USA.

    • Junjie Luo
    •  & Wei L Shen

Authors

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Contributions

The study was designed by J.L., W.L.S. and C.M., and directed and coordinated by C.M. The behavioral experiments were performed by J.L. and W.L.S. J.L. generated the trpA1 alleles and performed the immunohistochemistry experiments and Ca2+ imaging experiments. W.L.S. and J.L. performed two-electrode recordings in Xenopus oocytes. The manuscript was prepared by J.L., W.L.S. and C.M.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Craig Montell.

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Supplementary information