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An internal thermal sensor controlling temperature preference in Drosophila

Nature volume 454, pages 217–220 (2008)Cite this article

Abstract

Animals from flies to humans are able to distinguish subtle gradations in temperature and show strong temperature preferences1,2,3,4. Animals move to environments of optimal temperature and some manipulate the temperature of their surroundings, as humans do using clothing and shelter. Despite the ubiquitous influence of environmental temperature on animal behaviour, the neural circuits and strategies through which animals select a preferred temperature remain largely unknown. Here we identify a small set of warmth-activated anterior cell (AC) neurons located in the Drosophila brain, the function of which is critical for preferred temperature selection. AC neuron activation occurs just above the fly’s preferred temperature and depends on dTrpA1, an ion channel that functions as a molecular sensor of warmth. Flies that selectively express dTrpA1 in the AC neurons select normal temperatures, whereas flies in which dTrpA1 function is reduced or eliminated choose warmer temperatures. This internal warmth-sensing pathway promotes avoidance of slightly elevated temperatures and acts together with a distinct pathway for cold avoidance to set the fly’s preferred temperature. Thus, flies select a preferred temperature by using a thermal sensing pathway tuned to trigger avoidance of temperatures that deviate even slightly from the preferred temperature. This provides a potentially general strategy for robustly selecting a narrow temperature range optimal for survival.

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Figure 1: dTrpA1 is required for warmth avoidance.
Figure 2: AC neurons are thermosensors.
Figure 3: AC neurons are necessary for warmth avoidance.
Figure 4: dTrpA1 is a warmth sensor.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

The sequence for agTrpA1 has been deposited in the GenBank database under accession number EU624401.

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Acknowledgements

We thank Garrity laboratory members and L. Griffith, L. Huang, R. Huey, E. Marder, C. Miller, M. Rosbash, P. Sengupta, G. Turrigiano and their laboratories for advice and manuscript comments. Supported by NINDS (PO1 NS044232, P30 NS045713S10 and RR16780), NEI (RO1 EY13874, P.A.G.), NIMH (RO1 MH067284, to L. Griffith (for S.P. and A.G.)), and Japan Society for the Promotion of Science (F.N.H.)

Author Contributions F.N.H., M.R., S.R.P., K.K. and P.A.G. designed experiments; F.N.H. performed behaviour and imaging; M.R. created the dTrpA1 mutant, Gal4, RNAi and rescue strains; K.K. performed oocyte electrophysiology and dTrpA1 overexpression; S.R.P. performed NMJ electrophysiology, A.G. assisted with imaging; T.J.J. isolated agTrpA1 cDNA; and P.A.G. performed bioinformatics and assisted with knockdown studies. F.N.H. and P.A.G. wrote the paper with assistance from M.R., K.K., S.R.P. and A.G.

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Authors and Affiliations

  1. Biology Department, National Center for Behavioral Genomics, Volen Center for Complex Systems, Brandeis University MS-008, 415 South Street, Waltham, Massachusetts 02454, USA,

    Fumika N. Hamada, Mark Rosenzweig, Kyeongjin Kang, Stefan R. Pulver, Alfredo Ghezzi & Paul A. Garrity

  2. Department of Cell Biology and Institute for Childhood and Neglected Diseases, The Scripps Research Institute, 10550 North Torrey Pines Road, La Jolla, California 92037, USA,

    Timothy J. Jegla

Authors
  1. Fumika N. Hamada
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  5. Alfredo Ghezzi
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  7. Paul A. Garrity
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Corresponding author

Correspondence to Paul A. Garrity.

Supplementary information

Supplementary Figures

The file contains Supplementary Figures 1-7 with Legends. (PDF 6902 kb)

Supplementary Movie

The file contains Supplementary Movie 1. Flies that express dTRPA1 in all neurons (c155-Gal4;UAS-dTRPA1; right-hand vial) were temporarily incapacitated by heating to 35°C for 60 seconds, while control flies (which contain only the c155-Gal4 source or the UAS-dTRPA1 transgene alone; left-hand and middle vials, respectively) were not. All flies were heated by submerging their vials in a 35°C water bath for 60 seconds. Heat treatment was done off camera. Some empty frames recorded during heat treatment were removed. The movie is accelerated 8-fold. (MOV 2595 kb)

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Hamada, F., Rosenzweig, M., Kang, K. et al. An internal thermal sensor controlling temperature preference in Drosophila. Nature 454, 217–220 (2008). https://doi.org/10.1038/nature07001

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