Article | Published:

The neural basis of Drosophila gravity-sensing and hearing

Nature volume 458, pages 165171 (12 March 2009) | Download Citation

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Abstract

The neural substrates that the fruitfly Drosophila uses to sense smell, taste and light share marked structural and functional similarities with ours, providing attractive models to dissect sensory stimulus processing. Here we focus on two of the remaining and less understood prime sensory modalities: graviception and hearing. We show that the fly has implemented both sensory modalities into a single system, Johnston’s organ, which houses specialized clusters of mechanosensory neurons, each of which monitors specific movements of the antenna. Gravity- and sound-sensitive neurons differ in their response characteristics, and only the latter express the candidate mechanotransducer channel NompC. The two neural subsets also differ in their central projections, feeding into neural pathways that are reminiscent of the vestibular and auditory pathways in our brain. By establishing the Drosophila counterparts of these sensory systems, our findings provide the basis for a systematic functional and molecular dissection of how different mechanosensory stimuli are detected and processed.

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Acknowledgements

We thank D. F. Eberl for JO15, C. J. O’Kane for UFWTRA19, B. J. Dickson for UAS-GFP S65T and eyFLP fly strains, H. Tanimoto for flies carrying tubulin-GAL80ts and UAS-tetanus toxin, C. Kim for nandy5, M. J. Kernan for nan36a, L. Liu for nompC-GAL4.25, A. Wong and G. Struhl for UAS > CD2, y > CD8::GFP, J. Urban and G. Technau for MZ-series enhancer trap strains, the members of the NP consortium (a group of eight laboratories in Japan that together produced a large collection of GAL4 lines) and D. Yamamoto for the NP-series strains, Bloomington Stock Centre for elavc155-GAL4, D. F. Eberl and C. P. Kyriacou for courtship sound data, S. Fujita for 22C10 antibody, the Developmental Studies Hybridoma Bank for antibodies anti-Elav and nc82, T. Völler for help with calcium imaging, H. Otsuna and K. Shinomiya for preparing some figures, M. Dübbert, K. Öchsner, M. Matsukuma, S. Shuto and K. Yamashita for technical assistance, J. T. Albert, E. D. Hoopfer, B. Nadrowski, K. Endo, H. Otsuna, Y. Hiromi, E. Buchner and N. J. Strausfeld for discussion, and D. J. Anderson and S. Yorozu for sharing unpublished data. This work was supported by the Japanese Cell Science Research Foundation, the Alexander von Humboldt Foundation, and the Japan Society for the Promotion of Science (to A.K.), the DFG Collaborative Research Centre 554 (to A.F.), the Volkswagen Foundation, the BMBF Bernstein Network for Computational Neuroscience, and the DFG Research Centre Molecular Physiology of the Brain (to M.C.G.), and the Human Frontier Science Program Organisation, BIRD/Japan Science and Technology Agency, and the Japan Society for the Promotion of Science (to K.I.).

Author Contributions A.K., M.C.G. and K.I. designed research; A.K. and A.F. performed calcium imaging. A.K. and H.K.I. performed fly genetics; H.K.I. performed behavioural and anatomical experiments; T.E. performed nerve recordings; A.K., H.K.I. and O.H. performed histology; A.K., H.K.I., M.C.G. and K.I. wrote the paper; and M.C.G. and K.I. supervised the work. All authors discussed the concepts and results, and commented on the manuscript.

Author information

Author notes

    • Azusa Kamikouchi
    •  & Hidehiko K. Inagaki

    These authors contributed equally to this work.

    • Hidehiko K. Inagaki

    Present address: Division of Biology 216-76, California Institute of Technology, Pasadena, California 91125, USA.

Affiliations

  1. Sensory Systems Laboratory, Institute of Zoology, University of Cologne, 50923 Cologne, Germany

    • Azusa Kamikouchi
    • , Thomas Effertz
    • , Oliver Hendrich
    •  & Martin C. Göpfert
  2. Institute of Molecular and Cellular Biosciences, University of Tokyo, Yayoi, Bunkyo-ku, 113-0032 Tokyo, Japan

    • Azusa Kamikouchi
    • , Hidehiko K. Inagaki
    •  & Kei Ito
  3. School of Life Sciences, Tokyo University of Pharmacy and Life Sciences, 1432-1, Horinouchi, Hachioji, 192-0392 Tokyo, Japan

    • Azusa Kamikouchi
  4. Johann-Friedrich-Blumenbach-Institute, University of Göttingen, 37073 Göttingen, Germany

    • Thomas Effertz
    • , Oliver Hendrich
    • , André Fiala
    •  & Martin C. Göpfert
  5. Theodor-Boveri-Institute, Department of Genetics and Neurobiology, Julius-Maximilians-University of Würzburg, Am Hubland, 97074 Würzburg, Germany

    • André Fiala

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Corresponding authors

Correspondence to Martin C. Göpfert or Kei Ito.

Supplementary information

PDF files

  1. 1.

    Supplementary Information

    This file contains Supplementary Footnotes S1-S10, Supplementary Figures S1-S7 with Legends, Supplementary Table S1, Supplementary Methods and Supplementary References

Videos

  1. 1.

    Supplementary Movie 1

    This movie shows the spatial activation of the JO somata array (see file s1 for full legend).

  2. 2.

    Supplementary Movie 2

    This movie shows the 3D structure of the zones in the AMMC (see file s1 for full legend).

  3. 3.

    Supplementary Movie 3

    This movie shows the serial section of AMMC from the anterior to posterior (see file s1 for full legend).

  4. 4.

    Supplementary Movie 4

    This movie shows the counter-current apparatus in action (see file s1 for full legend).

  5. 5.

    Supplementary Movie 5

    This movie shows the response of the flies to a synthesized courtship pulse song (see file s1 for full legend).

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DOI

https://doi.org/10.1038/nature07810

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