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The neural basis of Drosophila gravity-sensing and hearing

Nature volume 458, pages 165–171 (2009)Cite this article

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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Figure 1: Mechanically evoked calcium signals in JO neurons.
Figure 2: Responses of JO neuron subgroups.
Figure 3: Requirement of JO neuron subgroups for gravity detection.
Figure 4: Requirement of JO neuron subgroups for hearing.
Figure 5: Expression of nan and nompC.
Figure 6: Higher-order neurons in the AMMC.

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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.

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Author notes

  1. Hidehiko K. Inagaki

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

  2. Azusa Kamikouchi and Hidehiko K. Inagaki: These authors contributed equally to this work.

Authors and 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. Department of Genetics and Neurobiology, Theodor-Boveri-Institute, Julius-Maximilians-University of Würzburg, Am Hubland, 97074 Würzburg, Germany,

    André Fiala

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Supplementary information

Supplementary Information

This file contains Supplementary Footnotes S1-S10, Supplementary Figures S1-S7 with Legends, Supplementary Table S1, Supplementary Methods and Supplementary References (PDF 3463 kb)

Supplementary Movie 1

This movie shows the spatial activation of the JO somata array (see file s1 for full legend). (MOV 1354 kb)

Supplementary Movie 2

This movie shows the 3D structure of the zones in the AMMC (see file s1 for full legend). (MOV 4859 kb)

Supplementary Movie 3

This movie shows the serial section of AMMC from the anterior to posterior (see file s1 for full legend). (MOV 9141 kb)

Supplementary Movie 4

This movie shows the counter-current apparatus in action (see file s1 for full legend). (MOV 4315 kb)

Supplementary Movie 5

This movie shows the response of the flies to a synthesized courtship pulse song (see file s1 for full legend). (MOV 8041 kb)

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Kamikouchi, A., Inagaki, H., Effertz, T. et al. The neural basis of Drosophila gravity-sensing and hearing. Nature 458, 165–171 (2009). https://doi.org/10.1038/nature07810

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