Mechanical feedback amplification in Drosophila hearing is independent of synaptic transmission

European Journal of Neuroscience

Volumn 31, Issue 4, 2010, Pages 697-703

  Kamikouchi, Azusa ^a   Albert, Jörg T ^b   Göpfert, Martin C ^c  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

Efferent control; Hearing; Mechanical feedback; Neurotransmission; Tetanus toxin

Indexed keywords

ACOUSTIC NERVE FIBER; AMPLIFIER; ANIMAL EXPERIMENT; ARTICLE; AUDITORY THRESHOLD; AUDITORY TUBE; BRAIN ELECTROPHYSIOLOGY; COCHLEA; DROSOPHILA; EFFERENT NERVE; EVOKED AUDITORY RESPONSE; FEEDBACK SYSTEM; HEARING; IMMUNOHISTOCHEMISTRY; INNERVATION; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SYNAPSE; SYNAPTIC TRANSMISSION; VIBRATION;

ACOUSTIC STIMULATION; ACTION POTENTIALS; ANIMALS; AUDITORY PATHWAYS; DROSOPHILA; FEEDBACK, SENSORY; HEARING; MECHANORECEPTORS; R-SNARE PROTEINS; SENSORY RECEPTOR CELLS; SYNAPTIC TRANSMISSION;

EID: 76949089578     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07099.x     Document Type: Article

References (57)

1. Albert, J.T., Nadrowski, B., Kamikouchi, A. Göpfert, M.C. (2006) Mechanical tracing of protein function in the Drosophila ear. Nat. Protoc., in press (doi :).
2. Albert, J.T., Nadrowski, B. Göpfert, M.C. (2007) Mechanical signatures of transducer gating in the Drosophila ear. Curr. Biol., 17, 1000 1006.
3. Ashmore, J. Gale, J. (2004) The cochlear amplifier. Curr. Biol., 14, R403 R404.
4. Brand, A.H. Perrimon, N. (1993) Targeted gene-expression as a means of altering cell fates and generating dominant phenotypes. Development, 118, 401 415.
5. Bräunig, P. Eder, M. (1998) Locust dorsal unpaired median (DUM) neurones directly innervate and modulate hindleg proprioceptors. J. Exp. Biol., 201, 3333 3338.
6. Cooper, N.P. Guinan, J.J. (2006) Efferent-mediated control of basilar membrane motion. J. Physiol. (Lond.), 576, 49 54.
7. Dambly-Chaudiere, C., Sapede, D., Soubiran, F., Decorde, K., Gompel, N. Ghysen, A. (2003) The lateral line of zebrafish: a model system for the analysis of morphogenesis and neural development in vertebrates. Biol. Cell, 95, 579 587.
8. Davis, H. (1983) An active process in cochlear mechanics. Hear. Res., 9, 79 90.
9. Dolan, D.F., Guo, M.H. Nuttall, A.L. (1997) Frequency-dependent enhancement of basilar membrane velocity during olivocochlear bundle stimulation. J. Acoust. Soc. Am., 102, 3587 3596.
10. Estes, P.S., Ho, G.L.Y., Narayanan, R. Ramaswami, M. (2000) Synaptic localization and restricted diffusion of a Drosophila neuronal synaptobrevin - green fluorescent protein chimera in vivo. J. Neurogenet., 13, 233 255.
11. Fabian-Fine, R., Meinertzhagen, I.A. Seyfarth, E.A. (2000) Organization of efferent peripheral synapses at mechanosensory neurons in spiders. J. Comp. Neurol., 420, 195 210.
12. Fettiplace, R. Hackney, C.M. (2006) The sensory and motor roles of auditory hair cells. Nat. Rev. Neurosci., 7, 19 29. (Pubitemid 41828928)
13. Field, L.H. Matheson, T. (1998) Chordotonal organs of insects. Advances in Insect Physiology, Vol. 27. Academic Press Inc, San Diego, pp. 1 228.
14. Foelix, R.F. (1975) Occurrence of synapses in peripheral sensory nerves of arachnids. Nature, 254, 146 148.
15. Frolenkov, G.I. (2006) Regulation of electromotility in the cochlear outer hair cell. J. Physiol. (Lond.), 576, 43 48.
16. 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. J. Neurosci., 24, 9059 9066.
17. Göpfert, M.C. Albert, J.T. (2005) Mechanical energy contributed by motile neurons in the Drosophila ear. In Nuttal, A.L. (Ed. 9th International Symposium on Auditory Mechani Portland, OR, Jul 23-28, 2005. World Scientific Publ Co Pte Ltd, Singapore, pp. 489 495.
18. Göpfert, M.C. Robert, D. (2001) Active auditory mechanics in mosquitoes. Proc. R. Soc. Lond. Ser. B Biol. Sci., 268, 333 339.
19. Göpfert, M.C. Robert, D. (2002) The mechanical basis of Drosophila audition. J. Exp. Biol., 205, 1199 1208.
20. Göpfert, M.C. Robert, D. (2008) Active processes in insect hearing. In Manley, G.A., Fay, R.R. Popper, A.N. (Eds Active Mechanics and Otoacoustic Emissions. Springer, Berlin, New York, pp. 191 210.
21. Göpfert, M.C., Briegel, H. Robert, D. (1999) Mosquito hearing: sound-induced antennal vibrations in male and female Aedes aegypti. J. Exp. Biol., 202, 2727 2738.
22. 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. Proc. Natl Acad. Sci. USA, 102, 325 330.
23. Göpfert, M.C., Albert, J.T., Nadrowski, B. Kamikouchi, A. (2006) Specification of auditory sensitivity by Drosophila TRP channels. Nat. Neurosci., 9, 999 1000.
24. Guinan, J.J., Warr, W.B. Norris, B.E. (1983) Differential olivocochlear projections from lateral versus medial zones of the superior olivary complex. J. Comp. Neurol., 221, 358 370.
25. Hilfiker, S., Pieribone, V.A., Czernik, A.J., Kao, H.T., Augustine, G.J. Greengard, P. (1999) Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. Lond. B Biol. Sci., 354, 269 279.
26. Hudspeth, A.J. (1997) Mechanical amplification of stimuli by hair cells. Curr. Opin. Neurobiol., 7, 480 486.
27. Jackson, J.C. Robert, D. (2006) Nonlinear auditory mechanism enhances female sounds for male mosquitoes. Proc. Natl Acad. Sci. USA, 103, 16734 16739.
28. Jackson, J.C., Windmill, J.F.C., Pook, V.G. Robert, D. (2009) Synchrony through twice-frequency forcing for sensitive and selective auditory processing. Proc. Natl Acad. Sci. USA, 106, 10177 10182.
29. Kamikouchi, A., Shimada, T. Ito, K. (2006) Comprehensive classification of the auditory sensory projections in the brain of the fruit fly Drosophila melanogaster. J. Comp. Neurol., 499, 317 356.
30. 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, 165 171.
31. Kemp, D.T. (1978) Stimulated acoustic emissions from within human auditory-system. J. Acoust. Soc. Am., 64, 1386 1391.
32. Kernan, M., Cowan, D. Zuker, C. (1994) Genetic dissection of mechanosensory transduction - mechanoreception-defective mutations of Drosophila. Neuron, 12, 1195 1206.
33. 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, 81 84.
34. Kitamoto, T. (2001) Conditional modification of behavior in drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. J. Neurobiol., 47, 81 92.
35. Klagges, B.R.E., Heimbeck, G., Godenschwege, T.A., Hofbauer, A., Pflugfelder, G.O., Reifegerste, R., Reisch, D., Schaupp, M., Buchner, S. Buchner, E. (1996) Invertebrate synapsins: a single gene codes for several isoforms in Drosophila. J. Neurosci., 16, 3154 3165.
36. Küppers, J. (1974) Measurements on the ionic mileu of the receptor terminal in mechanoreceptive sensilla of insects. In Schwartzkopf, J. (Ed. Symposium on Mechanoreception. Westdeutscher Verlag, Opladen, pp. 387 394.
37. Lin, D.M. Goodman, C.S. (1994) Ectopic and increased expression of fasciclin-II alters motoneuron growth cone guidance. Neuron, 13, 507 523.
38. Lu, Q., Senthilan, P.R., Effertz, T., Nadrowksi, B. Göpfert, M.C. (2009) Using Drosophila for studying fundamental processes in hearing. Integr. Comp. Biol., 49, 674 680.
39. Martin, P. Hudspeth, A.J. (2001) Compressive nonlinearity in the hair bundle's active response to mechanical stimulation. Proc. Natl Acad. Sci. USA, 98, 14386 14391.
40. McGuire, S.E., Le, P.T., Osborn, A.J., Matsumoto, K. Davis, R.L. (2003) Spatiotemporal rescue of memory dysfunction in Drosophila. Science, 302, 1765 1768.
41. Møller, A.R. (1983) Auditory Physiology. Academic Press, New York.
42. Nadrowski, B., Albert, J.T. Göpfert, M.C. (2008) Transducer-based force generation explains active process in Drosophila hearing. Curr. Biol., 18, 1365 1372.
43. Probst, R. Hauser, R. (1990) Distortion product otoacoustic emissions in normal and hearing-impaired ears. Am. J. Otolaryngol., 11, 236 243.
44. Rister, J. Heisenberg, M. (2006) Distinct functions of neuronal synaptobrevin in developing and mature fly photoreceptors. J. Neurobiol., 66, 1271 1284.
45. Roberts, D. Meredith, G.E. (1989) The Efferent System. Springer, New York.
46. Robles, L. Ruggero, M.A. (2001) Mechanics of the mammalian cochlea. Physiol. Rev., 81, 1305 1352.
47. Ruggero, M.A., Kramek, B. Rich, N.C. (1984) Spontaneous otoacoustic emissions in a dog. Hear. Res., 13, 293 296.
48. Russell, I.J. (1971) Role of lateral-line efferent system in Xenopus laevis. J. Exp. Biol., 54, 621 641.
49. Simmons, D.D. (2002) Development of the inner ear efferent system across vertebrate species. J. Neurobiol., 53, 228 250.
50. Sivan-Loukianova, E. Eberl, D.F. (2005) Synaptic ultrastructure of Drosophila Johnston's organ axon terminals as revealed by an enhancer trap. J. Comp. Neurol., 491, 46 55.
51. Sweeney, S.T., Broadie, K., Keane, J., Niemann, H. Okane, C.J. (1995) Targeted expression of tetanus toxin light-chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects. Neuron, 14, 341 351.
52. Thum, A.S., Knapek, S., Rister, J., Dierichs-Schmitt, E., Heisenberg, M. Tanimoto, H. (2006) Differential potencies of effector genes in adult Drosophila. J. Comp. Neurol., 498, 194 203.
53. Wangemann, P. (2006) Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J. Physiol. (Lond.), 576, 11 21.
54. Warr, W.B. (1992) Organization of olivocochlear efferent systems in mammals. In Webster, D.B., Popper, A.N. Fay, R.R. (Eds The Mammalian Auditory Pathway: Neuroanatomy. Springer, New York, pp. 410 448.
55. Warr, W.B. Guinan, J.J. (1979) Efferent innervation of the organ of corti - 2 separate systems. Brain Res., 173, 152 155.
56. Williamson, R. (1989) Secondary hair-cells and afferent neurons of the squid statocyst receive both inhibitory and excitatory efferent inputs. J. Comp. Physiol. A., 165, 847 860.
57. Wishart, G., Sickle, G.R. Riordan, D.F. (1962) Orientation of males of Aedes aegypti (L.) (Diptera: Culicidae) to sound. Can. Entomol., 94, 613 626.