Active Processes in Insect Hearing

  • Martin C. Göpfert
  • Daniel Robert
Part of the Springer Handbook of Auditory Research book series (SHAR, volume 30)


Transient Receptor Potential Channel Hair Bundle Chordotonal Organ Hearing Organ Cochlear Amplifier 


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  1. Atema J (1973) Microtubule theory of sensory transduction. J Theor Biol 38:181–190.PubMedCrossRefGoogle Scholar
  2. Atema J (1975) Stimulus transmission along microtubules in sensory cells: an hypothesis. In: Borgers M, deBrabander M (eds) Microtubules and Microtubule Inhibitors. Amsterdam: North-Holland, pp. 247–257.Google Scholar
  3. Baker JD, Adhikarakunnathu S, Kernan MJ (2004) Mechanosensory-defective, male-sterile unc mutants identify a novel basal body protein required for ciliogenesis in Drosophila. Development 131:3411–3422.PubMedCrossRefGoogle Scholar
  4. Bennet-Clark HC (1971) Acoustics of insect song. Nature 234:255–259.CrossRefGoogle Scholar
  5. Bialek, W (1987) Physical limits to sensation and perception. Annu Rev Biophys Biophys Chem 16:455–468PubMedCrossRefGoogle Scholar
  6. Boekhoff-Falk G (2005) Hearing in Drosophila: development of Johnston’s organ and emerging parallels to vertebrate ear development. Dev Dyn 232:550–558.PubMedCrossRefGoogle Scholar
  7. Boo KS, Richards AG (1975) Fine structure of the scolopidia in Johnston’s organ of female Aedes aegypti compared with that of male. J Insect Physiol 21:1129–1139.PubMedCrossRefGoogle Scholar
  8. Boyan GS (1993) Another look at insect audition: the tympanic receptors as an evolutionary specialization of the chordotonal system. J Insect Physiol 39:187–200.CrossRefGoogle Scholar
  9. Caldwell, J, Eberl DF (2002) Towards a molecular understanding of Drosophila hearing. J Neurobiol 53:172–189.PubMedCrossRefGoogle Scholar
  10. Chan DK, Hudspeth AJ (2005) Ca2+ current-driven nonlinear amplification in vitro. Nat Neurosci 8:149–155.PubMedCrossRefGoogle Scholar
  11. Corey DP et al. (2004) TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 432:723–730.PubMedCrossRefGoogle Scholar
  12. Coro F, Kössl M (1998) Distortion-product otoacoustic emissions from the tympanic organ in two noctuid moths. J Comp Physiol A 183:525–531.CrossRefGoogle Scholar
  13. Coro F, Kössl M (2001) Components of the 2f1 − f2 distortion-product otoacoustic emission in a moth. Hear Res 162:126–133.PubMedCrossRefGoogle Scholar
  14. Eberl DF (1999) Feeling the vibes: chordotonal mechanisms in insect hearing. Curr Opin Neurobiol 9:389–393.PubMedCrossRefGoogle Scholar
  15. Eberl DF, Hardy RW, Kernan MJ (2000) Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci 20:5981–5988.PubMedGoogle Scholar
  16. Erler G (1983) Sensitivity of an insect mechanoreceptor after destruction of dendritic microtubules by means of vinblastine. Cell Tissue Res 229:673–684.PubMedCrossRefGoogle Scholar
  17. Erwin DH, Davidson EH (2002) The last common bilaterian ancestor. Development 129:3021–3032.PubMedGoogle Scholar
  18. Fettiplace R, Ricci AJ, Hackney CM (2001) Clues to the cochlear amplifier from the turtle ear. Trends Neurosci 24:169–175.PubMedCrossRefGoogle Scholar
  19. Field LH, Matheson T (1998) Chordotonal organs in insects. Adv Insect Physiol 27:1–28.Google Scholar
  20. French AS (1988) Transduction mechanisms of mechanosensilla. Annu Rev Entomol 33:39–58.CrossRefGoogle Scholar
  21. Fritzsch B, Beisel KW (2004) Keeping sensory cells and evolving neurons to connect them to the brain: molecular conservation and novelties in vertebrate ear development. Brain Behav Evol 64:182–197.PubMedCrossRefGoogle Scholar
  22. Gillespie PG, Cyr JL (2003) Myosin-1c, the hair cell’s adaptation motor. Annu Rev Physiol 66:521–545.CrossRefGoogle Scholar
  23. Gillespie PG, Walker RG (2001) Molecular basis of mechanosensory transduction. Nature 413:194–202.PubMedCrossRefGoogle Scholar
  24. Gong Z, Son W, Chung YD, Kim J, Shin DW, McClung CA, Lee Y, Lee H, Chang D-J, Kaang B-K, Cho H, Oh U, Hirsh J, Kernan MJ, Kim C (2004) Two interdependent TRPV channel subunits, Inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 41:9059–9066.Google Scholar
  25. Göpfert MC, Albert JT, Nadrowksi B & Kamikouchi A (2006) Specification of auditory sensitivity by Drosophila TRP channels. Nat Neurosci 9:999–1000.PubMedCrossRefGoogle Scholar
  26. Göpfert MC, Robert D (2000) Nanometre-range acoustic sensitivity in male and female mosquitoes. Proc R Soc Lond B 267:453–457.CrossRefGoogle Scholar
  27. Göpfert MC, Robert D (2001a) Active auditory mechanics in mosquitoes. Proc R Soc Lond B 268:333–339.CrossRefGoogle Scholar
  28. Göpfert MC, Robert D (2001b) Turning the key on Drosophila audition. Nature 411:908.Google Scholar
  29. Göpfert MC, Robert D (2002) The mechanical basis of Drosophila audition. J Exp Biol 205:1199–1208.PubMedGoogle Scholar
  30. Göpfert MC, Robert D (2003) Motion generation by Drosophila mechanosensory neurons. Proc Natl Acad Sci USA 100:5514–5519.PubMedCrossRefGoogle Scholar
  31. Göpfert MC, Briegel H, Robert D (1999) Mosquito hearing: sound-induced antennal vibrations in male and female Aedes aegypti. J Exp Biol 202:2727–2738.PubMedGoogle Scholar
  32. Göpfert MC, Humphris ADL, Albert JT, Robert D, Hendrich O (2005) Power gain exhibited by motile mechanosensory neurons in Drosophila ears. Proc Natl Acad Sci USA 102:325–330.PubMedCrossRefGoogle Scholar
  33. Hall JC (1994) The mating of a fly. Science 264:1702–1714.PubMedCrossRefGoogle Scholar
  34. Hassan BA, Bellen HJ (2000) Doing the MATH: is the mouse a good model for fly development? Genes Dev 14:1852–1865.Google Scholar
  35. Höger U, Seyfarth E-A (2001) Structural correlates of mechanosensory transduction and adaptation in identified neurons of spider split sensilla. J Comp Phys A 187:727–736.CrossRefGoogle Scholar
  36. Howard J, Bechstedt S (2004) Hypothesis: a helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Curr Biol 14:R224–R226.Google Scholar
  37. Howard J, Roberts WM and Hudspeth AJ (1988) Mechanoelectrical transduction by hair cells. Annu Rev Biophys Biophys Chem 17:99–124.Google Scholar
  38. Hoy RR, Robert D (1996) Tympanal hearing in insects. Annu Rev Entomol 41:433–450.PubMedCrossRefGoogle Scholar
  39. Hoy RR, Popper AN, Fay RR (eds) (1998). Comparative Hearing: Insects. New York: Springer-Verlag.Google Scholar
  40. Jarman AP (2002) Studies of mechanosensation using the fly. Hum Mol Genet 11:1215–1218.PubMedCrossRefGoogle Scholar
  41. Kennedy HU, Crawford AC, Fettiplace R (2005) Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 433:880–833.PubMedCrossRefGoogle Scholar
  42. Kernan M, Zuker C (1995) Genetic approaches to mechanosensory transduction. Curr Opin Neurobiol 5:443–448.PubMedCrossRefGoogle Scholar
  43. Kim J, Chung YD, Park DY, Choi S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, Kim C (2003) A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84.PubMedCrossRefGoogle Scholar
  44. Kössl M, Boyan GS (1998a) Acoustic distortion products from the ear of a grasshopper. J Acoust Soc Am 104:326–335.CrossRefGoogle Scholar
  45. Kössl M, Boyan GS (1998b) Otoacoustic emissions from a nonvertebrate ear. Naturwissenschaften 85:124–127.CrossRefGoogle Scholar
  46. Kramer-Zucker AG, Olale F, Haycraft CJ, Yoder BK, Schier AF, Drummond IA (2005) Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer’s vesicle is required for normal organogenesis. Development132:1907–1921.Google Scholar
  47. Kuster JE, French AS, Sanders EJ (1983) The effect of microtubule dissociating agents on the physiology and cytology of the sensory neuron in the femoral tactile spine of the cockroach, Periplaneta americana L. Proc R Soc Lond B 219:397–412.PubMedCrossRefGoogle Scholar
  48. Manley GA (2001) Evidence for an active process and a cochlear amplifier in nonmammals. J Neurophysiol 86:541–549.PubMedGoogle Scholar
  49. Martin P, Hudspeth AJ (2001) Compressive nonlinearity in the hair bundle’s active response to mechanical stimulation. Proc Natl Acad Sci USA 98:14386–14391.PubMedCrossRefGoogle Scholar
  50. Martin P, Hudspeth AJ, Jülicher F (2001) Comparison of a hair bundle’s spontaneous oscillations with its response to mechanical stimulation reveals the underlying active process. Proc Natl Acad Sci USA 98:14380–14385.PubMedCrossRefGoogle Scholar
  51. Martin P, Bozovic D, Choe Y, Hudspeth AJ (2003) Spontaenous oscillation by hair bundles of the bullfrog’s sacculus. J Neurosci 23:4533–4548.PubMedGoogle Scholar
  52. Michelsen A (1968) Frequency discrimination in the locust ear by means of four groups of receptor cells. Nature 220:585–586.PubMedCrossRefGoogle Scholar
  53. Miller LA, Surlykke A (2001) How some insects detect and avoid being eaten by bats: Tactics and countertactics of prey and predator. Bioscience 51:570–581.CrossRefGoogle Scholar
  54. Mills DM, Rubel EW (1996) Development of the cochlear amplifier. J Acoust Soc Am 100:428–441.PubMedCrossRefGoogle Scholar
  55. Moran DT, Varela FJ, Rowley III JC (1977) Evidence for active role of cilia in sensory transduction. Proc Natl Acad Sci USA 74:793–797.PubMedCrossRefGoogle Scholar
  56. Nicolson T (2005) Fishing for key players in mechanotransduction. Trends Neurosci 28:140–144.PubMedCrossRefGoogle Scholar
  57. Nonaka S, Tanaka Y, Okada Y, Takeda S, Harada A, Yoshimitsu K, Kido M, Hirokawada N (1998) Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95:829–837.Google Scholar
  58. Odor DL, Blandau RJ (1985) Observations of the solitary cilium of rabbit oviductal epithelium: its motility and ultrastructure. Am J Anat 174:437–453.PubMedCrossRefGoogle Scholar
  59. Robert D (1989) The auditory behaviour of flying locusts. J Exp Biol 147:279–301.Google Scholar
  60. Robert D, Göpfert MC (2002) Novel schemes for hearing and acoustic orientation in insects. Curr Opin Neurobiol 12:715–720.PubMedCrossRefGoogle Scholar
  61. Robert D, Göpfert MC (2004) (eds) The Biology of Insect Audition. Micr Res Tech 63:311–412.CrossRefGoogle Scholar
  62. Robert D, Hoy RR (1998) The evolutionary innovation of tympanal hearing in Diptera. In: Hoy RR, Popper AN, Fay RR (eds), Comparative Hearing: Insects. New York: Springer-Verlag, pp. 197–227.Google Scholar
  63. Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81:1305–1352.PubMedGoogle Scholar
  64. Roeder KD, Treat AE (1957) Ultrasonic reception by the tympanic organ of noctuid moths. J Exp Zool 134:127–157.PubMedCrossRefGoogle Scholar
  65. Salisbury JL, Baron A, and Surek B (1984) Striated flagellar roots: isolation and characterization of a calcium-modulated contractile organelle. J Cell Biol 99:962–970.PubMedCrossRefGoogle Scholar
  66. Sarpal R, Todi SV, Sivan-Loukianova E, Shirolikar S, Subramanian N, Raff EC, Erickson JW, Ray K, Eberl DF (2003) Drosophila KAP interacts with the kinesin II motor subunit KLP64D to assemble chordotonal sensory cilia, but not sperm tails. Curr Biol 13:1687–1696.PubMedCrossRefGoogle Scholar
  67. Schiebel E, Bornens M (1995) In search of a function for centrins. Trends Cell Biol 5:197–201.PubMedCrossRefGoogle Scholar
  68. Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–99.PubMedCrossRefGoogle Scholar
  69. Surlykke A (1984) Hearing in notodontid moths—a tympanic organ with a single auditory neurons. J Exp Biol 113:323–335.Google Scholar
  70. Thurm U, Küppers J (1980) Epithelial physiology of insect sensilla. In: Locke M, Smith DS (eds) Insect Biology in Future. New York: Academic Press, pp. 735–763.Google Scholar
  71. Thurm U, Erler G, Goedde J, Kastrup H, Keil T, Voelker W and Vohwinkel B (1983). Cilia specialized for mechanoreception. J Submicrosc Cytol 15:151–155.Google Scholar
  72. Tischner H (1953) Über den Gehörsinn von Stechmücken. Acustica 3:335–343.Google Scholar
  73. Todi SV, Sharma Y, Eberl DF (2004) Anatomical and molecular design of the Drosophila antenna as a flagellar auditory organ. Microsc Res Tech 63:388–399.PubMedCrossRefGoogle Scholar
  74. van Staaden MJ, Römer H (1998) Evolutionary transition from stretch to hearing organs in ancient grasshoppers. Nature 394:773–776.CrossRefGoogle Scholar
  75. von Schilcher F (1976) The role of auditory stimuli in the courtship of Drosophila melanogaster. Anim Behav 24:18–26.CrossRefGoogle Scholar
  76. Walker RG, Willingham AT and Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234.Google Scholar
  77. Weber T, Göpfert MC, Winter H, Zimmermann U, Kohler H, Meier A, Hendrich O, Rohbock K, Robert D, Knipper M. (2003) Expression of prestin-homologous solute carrier (SLC26) in auditory organs of insects and lower vertebrates. Proc Natl Acad Sci USA 100:7690–7695.PubMedCrossRefGoogle Scholar
  78. Windmill J, Göpfert MC, Robert D (2005) Tympanal travelling wave in migratory locusts. J Exp Biol 208:157–168.PubMedCrossRefGoogle Scholar
  79. Wolfrum U (1991) Centrin- and UPalpha-actinin-like immunoreactivity in the ciliary rootlets of insect sensilla. Cell Tissue Res 266:321–238.CrossRefGoogle Scholar
  80. Wolfrum U (1992) Cytoskeletal elements in arthropod sensilla and mammalian photoreceptors. Biol Cell 76:373–381.PubMedCrossRefGoogle Scholar
  81. Yack JE (2004) The structure and function of auditory chordotonal organs in insects. Microsc Res Tech 63:315–337.PubMedCrossRefGoogle Scholar
  82. Yager DD (1999) Structure, development and evolution of insect auditory systems. Microsc Res Tech 47:380–400.PubMedCrossRefGoogle Scholar
  83. Yates GK (1995) Cochlear structure and function. In: Moore BCJ (ed), Hearing. San Diego, CA: Academic Press, pp. 41–74.Google Scholar
  84. Zheng J, Shen W, He DZ, Long KB, Madison LD, Dallos P (2000) Prestin is the motor protein of cochlear outer hair cells. Nature 405:149–155.PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Martin C. Göpfert
  • Daniel Robert

There are no affiliations available

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