Skip to main content
SpringerLink
Log in

Transduction and Amplification in the Ear: Insights from Insects

  • Chapter
  • First Online:
Insights from Comparative Hearing Research

Part of the book series: Springer Handbook of Auditory Research ((SHAR,volume 49))

Abstract

Of all the senses, it is the mechanical ones that have kept most of their molecular secrets, and of all the mechanical senses it is arguably the sense of hearing that has been the most reticent. Most centrally, auditory transducer channels have not been identified in any group of animals. This lack of molecular knowledge stands in stark contrast to an impressive body of biophysical knowledge about the general operation of mechanotransducers. During the last decade, an insect has entered the race for the molecules of hearing. Auditory neurons in the ear of the genetically tractable fruit fly Drosophila melanogaster were shown to operate according to the same principles as the sensory cells that mediate hearing in vertebrates. Just like our own ears, the ears of flies actively amplify sound-induced stimuli. Just like in vertebrate hair cells, the fly’s transducers for hearing are spring-gated, mechanically adapting ion channels. This chapter reviews the current state of molecular and mechanistic knowledge about auditory transduction in fruit flies and shows how active transducer modules contribute to sensitive hearing and the creation of species-specific acoustic communication channels.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Albert, J. T., Nadrowksi, B., & Göpfert, M. C. (2007a). Drosophila mechanotransduction:Linking proteins and functions. Fly, 1(4), 238–241.

    PubMed  Google Scholar 

  • Albert, J. T., Nadrowksi, B., & Göpfert, M. C. (2007b). Mechanical signatures of transducer gating in the Drosophila ear. Current Biology, 17(11), 1000–1006.

    Article  CAS  PubMed  Google Scholar 

  • Arnadottir, J., & Chalfie, M. (2010). Eukaryotic mechanosensitive channels. Annual review of biophysics ,(Vol. 39, pp. 111–137). Palo Alto: Annual Reviews.

    Google Scholar 

  • Assad, J. A., & Corey, D. P. (1992). An active motor model for adaptation by vertebrate hair-cells. Journal of Neuroscience, 12(9), 3291–3309.

    CAS  PubMed  Google Scholar 

  • Avitabile, D., Homer, M., Champneys, A. R., Jackson, J. C., & Robert, D. (2010). Mathematical modelling of the active hearing process in mosquitoes. Journal of the Royal Society Interface, 7(42), 105–122.

    Article  CAS  PubMed Central  Google Scholar 

  • Bechstedt, S., Albert, J. T., Kreil, D. P., Muller-Reichert, T., Göpfert, M. C., & Howard, J. (2010). A doublecortin containing microtubule-associated protein is implicated in mechanotransduction in Drosophila sensory cilia. Nature Communications, 1(1), 1–11.

    Article  CAS  PubMed Central  Google Scholar 

  • Ben-Arie, N., Hassan, B. A., Bermingham, N. A., Malicki, D. M., Armstrong, D., Matzuk, M., Bellen, H. J., & Zoghbi, H. Y. (2000). Functional conservation of atonal and Math1 in the CNS and PNS. Development, 127(5), 1039–1048.

    CAS  PubMed  Google Scholar 

  • Bermingham, N. A., Hassan, B. A., Price, S. D., Vollrath, M. A., Ben-Arie, N., Eatock, R. A., Bellen, H. J., Lysakowski, A., & Zoghbi, H. Y. (1999). Math1: An essential gene for the generation of inner ear hair cells. Science, 284(5421), 1837–1841.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, L. E., Song, W., Looger, L. L., Jan, L. Y., & Jan, Y. N. (2010). The role of the TRP channel NompC in Drosophila larval and adult locomotion. Neuron, 67(3), 373–380.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Christensen, A. P., & Corey, D. P. (2007). TRP channels in mechanosensation: Direct or indirect activation? Nature Reviews Neuroscience, 8(7), 510–521.

    Article  CAS  PubMed  Google Scholar 

  • Chung, Y. D., Zhu, J., Han, Y., & Kernan, M. J. (2001). nompA encodes a PNS-specific, ZP domain protein required to connect mechanosensory dendrites to sensory structures. Neuron, 29(2), 415–428.

    Article  CAS  PubMed  Google Scholar 

  • Cooper, N. P., & Guinan, J. J. (2006). Efferent-mediated control of basilar membrane motion. Journal of Physiology London, 576(1), 49–54.

    Google Scholar 

  • Corey, D. P., & Hudspeth, A. J. (1979). Response latency of vertebrate hair-cells. Biophysical Journal, 26(3), 499–506.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eberl, D. F., Hardy, R. W., & Kernan, M. J. (2000). Genetically similar transduction mechanisms for touch and hearing in Drosophila. Journal of Neuroscience, 20(16), 5981–5988.

    CAS  PubMed  Google Scholar 

  • Effertz, T., Wiek, R., & Göpfert, M. C. (2011). NompC TRP channel is essential for Drosophila sound receptor function. Current Biology, 21(7), 592–597.

    Article  CAS  PubMed  Google Scholar 

  • Effertz, T., Nadrowski, B., Piepenbrock, D., Albert, J. T., & Göpfert, M. C. (2012). Direct gating and mechanical integrity of Drosophila auditory transducers require TRPN1. Nature Neurosci, 15(9), 1198–1200.

    Article  CAS  PubMed  Google Scholar 

  • Field, L. H., & Matheson, T. (1998). Chordotonal organs of insects. In Advances in insect physiology (Vol. 27, pp. 1–228). San Diego: Academic Press.

    Google Scholar 

  • French, A. S. (1992). Mechanotransduction. Annual Review of Physiology, 54, 135–152.

    Article  CAS  PubMed  Google Scholar 

  • Gibson, G., Warren, B., & Russell, I. J. (2010). Humming in tune: Sex and species recognition by mosquitoes on the wing.. JARO: Journal of the Association for Research in Otolaryngology, 11(4), 527–540.

    Article  PubMed Central  PubMed  Google Scholar 

  • Gong, Z. F., Son, W. S., Chung, Y. D., Kim, J. W., Shin, D. W., McClung, C. A., Lee, Y., Lee, H. W., Chang, D. J., Kaang, B. K., Cho, H. W., Oh, U., Hirsh, J., Kernan, M. J., & Kim, C. S. (2004). Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. Journal of Neuroscience, 24(41), 9059–9066.

    Article  CAS  PubMed  Google Scholar 

  • Göpfert, M. C., & Robert, D. (2001a). Biomechanics: Turning the key on Drosophila audition. Nature, 411(6840), 908.

    Article  PubMed  Google Scholar 

  • Göpfert, M. C., & Robert, D. (2001b). Active auditory mechanics in mosquitoes. Proceedings of the Royal Society of London Series B: Biological Sciences, 268(1465), 333–339.

    Article  PubMed  Google Scholar 

  • Göpfert, M. C., & Robert, D. (2002). The mechanical basis of Drosophila audition. Journal of Experimental Biology, 205(Pt 9), 1199–1208.

    PubMed  Google Scholar 

  • Göpfert, M. C., & Robert, D. (2003). Motion generation by Drosophila mechanosensory neurons. Proceedings of the National Academy of Sciences of the USA, 100(9), 5514–5519.

    Article  PubMed  Google Scholar 

  • Göpfert, M. C., Humphris, A. D. L., Albert, J. T., Robert, D., & Hendrich, O. (2005). Power gain exhibited by motile mechanosensory neurons in Drosophila ears. Proceedings of the National Academy of Sciences of the USA, 102(2), 325–330.

    Article  PubMed  Google Scholar 

  • Göpfert, M. C., Albert, J. T., Nadrowski, B., & Kamikouchi, A. (2006). Specification of auditory sensitivity by Drosophila TRP channels. Nature Neuroscience, 9(8), 999–1000.

    Article  PubMed  Google Scholar 

  • Hall, J. C. (1994). The mating of a fly. Science, 264(5166), 1702–1714.

    Article  CAS  PubMed  Google Scholar 

  • Howard, J., & Hudspeth, A. J. (1988). Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron, 1(3), 189–199.

    Article  CAS  PubMed  Google Scholar 

  • Howard, J., & Bechstedt, S. (2004). Hypothesis: A helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Current Biology, 14(6), R224–226.

    Article  CAS  PubMed  Google Scholar 

  • Hudspeth, A. J., Choe, Y., Mehta, A. D., & Martin, P. (2000). Putting ion channels to work: Mechanoelectrical transduction, adaptation, and amplification by hair cells. Proceedings of the National Academy of Sciences of the USA, 97(22), 11765–11772.

    Article  CAS  PubMed  Google Scholar 

  • Jackson, J. C., Windmill, J. F. C., Pook, V. G., & Robert, D. (2009). Synchrony through twice-frequency forcing for sensitive and selective auditory processing. Proceedings of the National Academy of Sciences of the USA, 106(25), 10177–10182.

    Article  CAS  PubMed  Google Scholar 

  • Jarman, A. P., Grau, Y., Jan, L. Y., & Jan, Y. N. (1993). atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous System. Cell, 73(7), 1307–1321.

    Article  CAS  PubMed  Google Scholar 

  • Kamikouchi, A., Shimada, T., & Ito, K. (2006). Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. Journal of Comparative Neurology, 499(3), 317–356.

    Article  PubMed  Google Scholar 

  • Kamikouchi, A., Inagaki, H. K., Effertz, T., Hendrich, O., Fiala, A., Göpfert, M. C., & Ito, K. (2009). The neural basis of Drosophila gravity-sensing and hearing. Nature, 458(7235), 165–171.

    Article  CAS  PubMed  Google Scholar 

  • Kamikouchi, A., Albert, J. T., & Göpfert, M. C. (2010). Mechanical feedback amplification in Drosophila hearing is independent of synaptic transmission. European Journal of Neuroscience, 31(4), 697–703.

    Article  PubMed  Google Scholar 

  • Kang, L. J., Gao, J. W., Schafer, W. R., Xie, Z. X., & Xu, X. Z. S. (2010). C. elegans TRP Family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron, 67(3), 381–391.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kavlie, R. G., Kernan, M. J., & Eberl, D. F. (2010). Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics, 185(1), 177–188.

    Article  CAS  PubMed  Google Scholar 

  • Keil, T. A. (1997). Functional morphology of insect mechanoreceptors. Microscopy Research and Technique, 39(6), 506–531.

    Article  CAS  PubMed  Google Scholar 

  • Kernan, M., Cowan, D., & Zuker, C. (1994). Genetic dissection of mechanosensory transduction: Mechanoreception-defective mutations of Drosophila. Neuron, 12(6), 1195–1206.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J., Chung, Y. D., Park, D. Y., Choi, S., Shin, D. W., Soh, H., Lee, H. W., Son, W., Yim, J., Park, C. S., Kernan, M. J., & Kim, C. (2003). A TRPV family ion channel required for hearing in Drosophila. Nature, 424(6944), 81–84.

    Article  CAS  PubMed  Google Scholar 

  • Lee, J., Moon, S., Cha, Y., & Chung, Y. D. (2010). Drosophila TRPN(=NOMPC) channel localizes to the distal end of mechanosensory cilia. PLoS ONE, 5(6).

    Google Scholar 

  • Liang, X., Madrid, J., Saleh, H. S., & Howard, J. (2011). NOMPC, a member of the TRP channel family, localizes to the tubular body and distal cilium of Drosophila campaniform and chordotonal receptor cells. Cytoskeleton, 68(1), 1–7.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Markow, T. A., & O'Grady, P. M. (2005). Evolutionary genetics of reproductive behavior in Drosophila: Connecting the dots. Annual Review of Genetics, 39, 263–291.

    Article  CAS  PubMed  Google Scholar 

  • Nadrowski, B., Albert, J. T., & Göpfert, M. C. (2008). Transducer-based force generation explains active process in Drosophila hearing. Current Biology, 18(18), 1365–1372.

    Article  CAS  PubMed  Google Scholar 

  • Pennetier, C., Warren, B., Dabire, K. R., Russell, I. J., & Gibson, G. (2010). "Singing on the wing" as a mechanism for species recognition in the malarial mosquito Anopheles gambiae. Current Biology, 20(2), 131–136.

    Article  CAS  PubMed  Google Scholar 

  • Riabinina, O., Dai, M., Duke, T., & Albert, J. T. (2011). Active process mediates species-specific tuning of Drosophila ears. Current Biology, 21(8), 658–664.

    Article  CAS  PubMed  Google Scholar 

  • Senthilan, P. R., Piepenbrock, D., Ovezmyradov, G., Nadrowski, B., Bechstedt, S., Pauls, S., Winkler, M., Möbius, W., Howard, J., & Göpfert, M. C. (2012). Drosophila auditory organ genes and genetic hearing defects. Cell, 150(5), 1042–1054.

    Article  CAS  PubMed  Google Scholar 

  • Walker, R. G., Willingham, A. T., & Zuker, C. S. (2000). A Drosophila mechanosensory transduction channel. Science, 287(5461), 2229–2234.

    Article  CAS  PubMed  Google Scholar 

  • Warmke, J. W., Reenan, R. A. G., Wang, P. Y., Qian, S., Arena, J. P., Wang, J. X., Wunderler, D., Liu, K., Kaczorowski, G. J., VanderPloeg, L. H. T., Ganetzky, B., & Cohen, C. J. (1997). Functional expression of Drosophila para sodium channels: Modulation by the membrane protein TipE and toxin pharmacology. Journal of General Physiology, 110(2), 119–133.

    Article  CAS  PubMed  Google Scholar 

  • Warren, B., Gibson, G., & Russell, I. J. (2009). Sex recognition through midflight mating Duets in Culex Mosquitoes Is Mediated by Acoustic Distortion. Current Biology, 19(6), 485–491.

    Article  CAS  PubMed  Google Scholar 

  • Warren, B., Lukashkin, A. N., & Russell, I. J. (2010). The dynein-tubulin motor powers active oscillations and amplification in the hearing organ of the mosquito. [Article]. Proceedings of the Royal Society B: Biological Sciences, 277(1688), 1761–1769.

    Article  PubMed  Google Scholar 

  • Yorozu, S., Wong, A., Fischer, B. J., Dankert, H., Kernan, M. J., Kamikouchi, A., Ito, K., & Anderson, D. J. (2009). Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature, 458(7235), 201–U204.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Ear Institute, University College London, 332 Gray’s Inn Rd, London, WC1X 8EE, UK

    Ryan G. Kavlie & Joerg T. Albert

Authors
  1. Ryan G. Kavlie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Joerg T. Albert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joerg T. Albert .

Editor information

Editors and Affiliations

  1. School of Medicine and Health Science, Carl von Ossietzky University, Oldenburg, Niedersachsen, Germany

    Christine Köppl

  2. School of Medicine and Health Science, Carl von Ossietzky University, Oldenburg, Niedersachsen, Germany

    Geoffrey A. Manley

  3. Department of Biology, University of Maryland, College Park, Maryland, USA

    Arthur N. Popper

  4. Falmouth, Massachusetts, USA

    Richard R. Fay

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media New York

About this chapter

Cite this chapter

Kavlie, R.G., Albert, J.T. (2013). Transduction and Amplification in the Ear: Insights from Insects. In: Köppl, C., Manley, G., Popper, A., Fay, R. (eds) Insights from Comparative Hearing Research. Springer Handbook of Auditory Research, vol 49. Springer, New York, NY. https://doi.org/10.1007/2506_2013_22

Download citation

Publish with us

Policies and ethics

Search

Navigation