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Identification and function of thermosensory neurons in Drosophila larvae

Nature Neuroscience volume 6, pages 267–273 (2003)Cite this article

Abstract

Although the ability to sense temperature is critical for many organisms, the underlying mechanisms are poorly understood. Using the calcium reporter yellow cameleon 2.1 and electrophysiological recordings, we identified thermosensitive neurons and examined their physiologic response in Drosophila melanogaster larvae. In the head, terminal sensory organ neurons showed increased activity in response to cooling by ≤1 °C, heating reduced their basal activity, and different units showed distinct response patterns. Neither cooling nor heating affected dorsal organ neurons. Body wall neurons showed a variety of distinct response patterns to both heating and cooling; the diverse thermal responses were strikingly similar to those described in mammals. These data establish a functional map of thermoresponsive neurons in Drosophila larvae and provide a foundation for understanding mechanisms of thermoreception in both insects and mammals.

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Figure 1: Neuronal expression of cameleon and larval response to a temperature gradient.
Figure 2: Optical recording of cameleon fluorescence in terminal and dorsal organs.
Figure 3: Extracellular electrophysiologic recording from terminal organ neurons.
Figure 4: Electrophysiologic response of terminal organ neurons to temperature.
Figure 5: Behavioral preference for cold and warm temperatures in larvae with disrupted terminal organ function.
Figure 6: Optical recording of cameleon fluorescence in the dorsal, lateral body wall segment.

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References

  1. Bullock, T.H. & Diecke, F.P.J. Properties of an infra-red receptor. J. Physiol. 134, 47–87 (1956).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Hart, S. Beetle mania: an attraction to fire. BioScience 48, 3–5 (1998).

    Article  Google Scholar 

  3. Schmitz, H. & Bleckmann, H. The photomechanic infrared receptor for the detection of forest fires in the beetle Melanophila acuminata (Coleoptera: Buprestidae). J. Comp. Physiol. [A] 182, 647–657 (1998).

    Article  Google Scholar 

  4. Martin, J.H. & Jessell, T.M. Modality coding in the somatic sensory system. in Principles of Neural Science (eds. Kandel, E.R., Schwartz, J.H. & Jessell, T.M.) 341–352 (Elsevier Science Ltd., New York, 1991).

    Google Scholar 

  5. Campbell, A.L., Naik, R.R., Sowards, L. & Stone, M.O. Biological infrared imaging and sensing. Micron 33, 211–225 (2002).

    Article  PubMed  Google Scholar 

  6. Sayeed, O. & Benzer, S. Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc. Natl. Acad. Sci. USA 93, 6079–6084 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Brewster, R. & Bodmer, R. Origin and specification of type II sensory neurons in Drosophilia. Development 121, 2923–2936 (1995).

    CAS  PubMed  Google Scholar 

  8. Grueber, W.B., Jan, L.Y. & Jan, Y.N. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867–2878 (2002).

    CAS  PubMed  Google Scholar 

  9. Miyawaki, A., Griesbeck, O., Heim, R. & Tsien, R.Y. Dynamic and quantitative Ca2+ measurements using improved cameleons. Proc. Natl. Acad. Sci. USA 96, 2135–2140 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Miyawaki, A. et al. Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388, 882–887 (1997).

    Article  CAS  PubMed  Google Scholar 

  11. Kerr, R. et al. Optical imaging of calcium transients in neurons and pharyngeal muscle of C. elegans. Neuron 26, 583–594 (2000).

    Article  CAS  PubMed  Google Scholar 

  12. Python, F. & Stocker, R.F. Adult-like complexity of the larval antennal lobe of D. melanogaster despite markedly low numbers of odorant receptor neurons. J. Comp. Neurol. 445, 374–387 (2002).

    Article  PubMed  Google Scholar 

  13. Campero, M., Serra, J., Bostock, H. & Ochoa, J.L. Slowly conducting afferents activated by innocuous low temperature in human skin. J. Physiol. 535, 855–865 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Dykes, R.W. Coding of steady and transient temperatures by cutaneous 'cold' fibers serving the hand of monkeys. Brain Res. 98, 485–500 (1975).

    Article  CAS  PubMed  Google Scholar 

  15. Kenshalo, D.R. & Duclaux, R. Response characteristics of cutaneous cold receptors in the monkey. J. Neurophysiol. 40, 319–332 (1977).

    Article  CAS  PubMed  Google Scholar 

  16. Long, R.R. Sensitivity of cutaneous cold fibers to noxious heat: paradoxical cold discharge. J. Neurophysiol. 40, 489–502 (1977).

    Article  CAS  PubMed  Google Scholar 

  17. Heimbeck, G., Bugnon, V., Gendre, N., Haberlin, C. & Stocker, R.F. Smell and taste perception in Drosophila melanogaster larva: toxin expression studies in chemosensory neurons. J. Neurosci. 19, 6599–6609 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sweeney, S.T., Broadie, K., Keane, J., Niemann, H. & O'Kane, C.J. Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron 14, 341–351 (1995).

    Article  CAS  PubMed  Google Scholar 

  19. Opplinger, F.Y., Guerin, P.M. & Vlimant, M. Neurophysiological and behavioural evidence for an olfactory function for the dorsal organ and a gustatory one for the terminal organ in Drosophila melanogaster larvae. J. Insect Physiol. 46, 135–144 (2000).

    Article  Google Scholar 

  20. Darian-Smith, I., Johnson, K.O. & Dykes, R. 'Cold' fiber population innervating palmar and digital skin of the monkey: responses to cooling pulses. J. Neurophysiol. 36, 325–346 (1973).

    Article  CAS  PubMed  Google Scholar 

  21. Iggo, A. Cutaneous thermoreceptors in primates and sub-primates. J. Physiol. 200, 403–430 (1969).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Viana, F., de la Pena, E. & Belmonte, C. Specificity of cold thermotransduction is determined by differential ionic channel expression. Nat. Neurosci. 5, 254–260 (2002).

    Article  CAS  PubMed  Google Scholar 

  23. Susser, E., Sprecher, E. & Yarnitsky, D. Paradoxical heat sensation in healthy subjects: peripherally conducted by A delta or C fibres? Brain 122, 239–246 (1999).

    Article  PubMed  Google Scholar 

  24. Caterina, M.J. & Julius, D. The vanilloid receptor: a molecular gateway to the pain pathway. Annu. Rev. Neurosci. 24, 487–517 (2001).

    Article  CAS  PubMed  Google Scholar 

  25. Brand, A.H. & Perrimon, N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401–415 (1993).

    CAS  PubMed  Google Scholar 

  26. Rubin, G.M. et al. Germ line specificity of P-element transposition and some novel patterns of expression of transduced copies of the white gene. Cold Spring Harb. Symp. Quant. Biol. 50, 329–335 (1985).

    Article  CAS  PubMed  Google Scholar 

  27. Wu, C.F., Suzuki, N. & Poo, M.M. Dissociated neurons from normal and mutant Drosophila larval central nervous system in cell culture. J. Neurosci. 3, 1888–1899 (1983).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Grynkiewicz, G., Poenie, M. & Tsien, R.Y. A new generation of Ca2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440–3450 (1985).

    CAS  PubMed  Google Scholar 

  29. Stewart, B.A., Atwood, H.L., Renger, J.J., Wang, J. & Wu, C.F. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. Physiol. [A] 175, 179–191 (1994).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank T. Mayhew for assistance, L.L. Wallrath for fly stocks and facility and L.B. Solly for assistance in measuring larval locomotion. We also thank the DNA Core of the Diabetes and Endocrine Research Center (DK25295). This work was supported by the Howard Hughes Medical Institute and the National Institutes of Health (HL14388). M.J.W. is an Investigator of the Howard Hughes Medical Institute.

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Authors and Affiliations

  1. Department of Internal Medicine, University of Iowa, Roy J. and Lucille A. Carver College of Medicine, 500 EMRB, Iowa City, 52242, Iowa, USA

    Lei Liu, Olena Yermolaieva, Francois M. Abboud & Michael J. Welsh

  2. Department of Physiology and Biophysics, University of Iowa, Roy J. and Lucille A. Carver College of Medicine, 500 EMRB, Iowa City, 52242, Iowa, USA

    Wayne A. Johnson, Francois M. Abboud & Michael J. Welsh

  3. Howard Hughes Medical Institute, 500 EMRB, Iowa City, 52242, Iowa, USA

    Michael J. Welsh

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Correspondence to Michael J. Welsh.

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Liu, L., Yermolaieva, O., Johnson, W. et al. Identification and function of thermosensory neurons in Drosophila larvae. Nat Neurosci 6, 267–273 (2003). https://doi.org/10.1038/nn1009

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