Letter | Published:

Temperature representation in the Drosophila brain

Nature volume 519, pages 358361 (19 March 2015) | Download Citation

Subjects

Abstract

In Drosophila, rapid temperature changes are detected at the periphery by dedicated receptors forming a simple sensory map for hot and cold in the brain1. However, flies show a host of complex innate and learned responses to temperature, indicating that they are able to extract a range of information from this simple input. Here we define the anatomical and physiological repertoire for temperature representation in the Drosophila brain. First, we use a photolabelling strategy2 to trace the connections that relay peripheral thermosensory information to higher brain centres, and show that they largely converge onto three target regions: the mushroom body, the lateral horn (both of which are well known centres for sensory processing) and the posterior lateral protocerebrum, a region we now define as a major site of thermosensory representation. Next, using in vivo calcium imaging3, we describe the thermosensory projection neurons selectively activated by hot or cold stimuli. Fast-adapting neurons display transient ON and OFF responses and track rapid temperature shifts remarkably well, while slow-adapting cell responses better reflect the magnitude of simple thermal changes. Unexpectedly, we also find a population of broadly tuned cells that respond to both heating and cooling, and show that they are required for normal behavioural avoidance of both hot and cold in a simple two-choice temperature preference assay. Taken together, our results uncover a coordinated ensemble of neural responses to temperature in the Drosophila brain, demonstrate that a broadly tuned thermal line contributes to rapid avoidance behaviour, and illustrate how stimulus quality, temporal structure, and intensity can be extracted from a simple glomerular map at a single synaptic station.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    , , , & The coding of temperature in the Drosophila brain. Cell 144, 614–624 (2011)

  2. 2.

    et al. A dimorphic pheromone circuit in Drosophila from sensory input to descending output. Nature 468, 686–690 (2010)

  3. 3.

    , , , & Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell 112, 271–282 (2003)

  4. 4.

    et al. A systematic nomenclature for the insect brain. Neuron 81, 755–765 (2014)

  5. 5.

    et al. The Drosophila pheromone cVA activates a sexually dimorphic neural circuit. Nature 452, 473–477 (2008)

  6. 6.

    et al. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nature Biotechnol. 22, 1567–1572 (2004)

  7. 7.

    et al. A GAL4-driver line resource for Drosophila neurobiology. Cell Rep. 2, 991–1001 (2012)

  8. 8.

    et al. GFP Reconstitution Across Synaptic Partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57, 353–363 (2008)

  9. 9.

    & Motor control in a Drosophila taste circuit. Neuron 61, 373–384 (2009)

  10. 10.

    et al. Genetically encoded dendritic marker sheds light on neuronal connectivity in Drosophila. Proc. Natl Acad. Sci. USA 107, 20553–20558 (2010)

  11. 11.

    , & Living synaptic vesicle marker: synaptotagmin-GFP. Genesis 34, 142–145 (2002)

  12. 12.

    , , , & Altered electrical properties in Drosophila neurons developing without synaptic transmission. J. Neurosci. 21, 1523–1531 (2001)

  13. 13.

    & Atypical expression of Drosophila gustatory receptor genes in sensory and central neurons. J. Comp. Neurol. 506, 548–568 (2008)

  14. 14.

    et al. A gustatory receptor paralogue controls rapid warmth avoidance in Drosophila. Nature 500, 580–584 (2013)

  15. 15.

    , , & Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136, 149–162 (2009)

  16. 16.

    et al. A hard-wired glutamatergic circuit pools and relays UV signals to mediate spectral preference in Drosophila. Neuron 81, 603–615 (2014)

  17. 17.

    et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature 499, 295–300 (2013)

  18. 18.

    , , & Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res. 262, 9–34 (1990)

  19. 19.

    , & Organization of antennal lobe-associated neurons in adult Drosophila melanogaster brain. J. Comp. Neurol. 520, 4067–4130 (2012)

  20. 20.

    et al. BrainGazer–visual queries for neurobiology research. IEEE Trans. Vis. Comput. Graph. 15, 1497–1504 (2009)

  21. 21.

    , , & Auditory circuit in the Drosophila brain. Proc. Natl Acad. Sci. USA 109, 2607–2612 (2012)

  22. 22.

    , , & Taste representations in the Drosophila brain. Cell 117, 981–991 (2004)

Download references

Acknowledgements

We thank V. Ruta and B. Noro for providing PA-GFP flies and reagents, and especially G. Rubin for providing access to the FlyLight collection before publication. We are grateful to N. Ryba, D. Yarmolinsky, C. Zuker and members of the Gallio laboratory for critical comments on the manuscript. Z. Turan and A. Kuang provided technical assistance and we thank C. Ulmer and a number of undergraduate students for fly husbandry. This work was supported by NIH grant 1R01NS086859-01 (to M.G.) and by training grant 2T32MH067564 (to D.D.F.).

Author information

Affiliations

  1. Department of Neurobiology, Northwestern University, Evanston, Illinois 60208, USA

    • Dominic D. Frank
    • , Genevieve C. Jouandet
    • , Patrick J. Kearney
    •  & Marco Gallio
  2. Departments of Biochemistry and Molecular Biophysics, Columbia University, New York, New York 10032, USA

    • Lindsey J. Macpherson

Authors

  1. Search for Dominic D. Frank in:

  2. Search for Genevieve C. Jouandet in:

  3. Search for Patrick J. Kearney in:

  4. Search for Lindsey J. Macpherson in:

  5. Search for Marco Gallio in:

Contributions

M.G. and D.D.F. designed the study, carried out the imaging experiments, analysed data (with help from G.C.J.), and wrote the paper; D.D.F., G.C.J. and M.G. ran and analysed all behavioural experiments; P.J.K. carried out GRASP experiments using transgenic lines produced by M.G. and L.J.M.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Marco Gallio.

Extended data

Supplementary information

PDF files

  1. 1.

    Supplementary Tables

    This file contains Supplementary Tables listing the genotypes relevant to this study.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature14284

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.