Letter | Published:

Thermosensory processing in the Drosophila brain

Nature volume 519, pages 353357 (19 March 2015) | Download Citation

Abstract

In Drosophila, just as in vertebrates, changes in external temperature are encoded by bidirectional opponent thermoreceptor cells: some cells are excited by warming and inhibited by cooling, whereas others are excited by cooling and inhibited by warming1,2. The central circuits that process these signals are not understood. In Drosophila, a specific brain region receives input from thermoreceptor cells2,3. Here we show that distinct genetically identified projection neurons (PNs) in this brain region are excited by cooling, warming, or both. The PNs excited by cooling receive mainly feed-forward excitation from cool thermoreceptors. In contrast, the PNs excited by warming (‘warm-PNs’) receive both excitation from warm thermoreceptors and crossover inhibition from cool thermoreceptors through inhibitory interneurons. Notably, this crossover inhibition elicits warming-evoked excitation, because warming suppresses tonic activity in cool thermoreceptors. This in turn disinhibits warm-PNs and sums with feed-forward excitation evoked by warming. Crossover inhibition could cancel non-thermal activity (noise) that is positively correlated among warm and cool thermoreceptor cells, while reinforcing thermal activity which is anti-correlated. Our results show how central circuits can combine signals from bidirectional opponent neurons to construct sensitive and robust neural codes.

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Acknowledgements

We are grateful to C. -H. Lee for the gift of LexAOp-HA-Ort flies, P. Garrity for Gr28b.d-Gal4, and A. Rajan for Gad1-Gal4 (line 2B). A. DiAntonio kindly supplied the anti-dVGluT antibody. We thank the Wilson laboratory, A. Samuel, P. Garrity, L. Griffith and D. Ginty for comments on the manuscript. D. Rogulja’s laboratory and M. Y. Wong shared reagents and expertise. A portion of this work was supported by NIH grant R01 DC008174. W.W.L. is supported by an HHMI International Research Fellowship and a Presidential Scholarship from the MD–PhD Program at Harvard Medical School. R.I.W. is a Howard Hughes Investigator.

Author information

Affiliations

  1. Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA

    • Wendy W. Liu
    • , Ofer Mazor
    •  & Rachel I. Wilson
  2. Harvard NeuroDiscovery Center, Harvard Medical School, 220 Longwood Avenue, Boston, Massachusetts 02115, USA

    • Ofer Mazor

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Contributions

W.W.L. and R.I.W. conceived the experiments. O.M. and W.W.L. made the thermal stimulation device. W.W.L. performed the experiments. W.W.L. and R.I.W. analysed the data and wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Rachel I. Wilson.

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DOI

https://doi.org/10.1038/nature14170

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