Active amplification in insect ears: mechanics, models and molecules

Abstract

Active amplification in auditory systems is a unique and sophisticated mechanism that expends energy in amplifying the mechanical input to the auditory system, to increase its sensitivity and acuity. Although known for decades from vertebrates, active auditory amplification was only discovered in insects relatively recently. It was first discovered from two dipterans, mosquitoes and flies, who hear with their light and compliant antennae; only recently has it been observed in the stiffer and heavier tympanal ears of an orthopteran. The discovery of active amplification in two distinct insect lineages with independently evolved ears, suggests that the trait may be ancestral, and other insects may possess it as well. This opens up extensive research possibilities in the field of acoustic communication, not just in auditory biophysics, but also in behaviour and neurobiology. The scope of this review is to establish benchmarks for identifying the presence of active amplification in an auditory system and to review the evidence we currently have from different insect ears. I also review some of the models that have been posited to explain the mechanism, both from vertebrates and insects and then review the current mechanical, neurobiological and genetic evidence for each of these models.

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Abbreviations

BF:

Best frequency

CAP:

Compound action potentials

Iav:

Inactive

IHC:

Inner hair cell

JO:

Johnston’s organ

OHC:

Outer hair cell

Nan:

Nanchung

NompC:

No mechanoreceptor potential C

SRS:

Stimulus receiver structure

TilB:

Touch insensitive larvae B

TRP:

Transient receptor potential

References

  1. Ajdari A, Prost J, Jülicher F (1997) Modeling molecular motors. Rev Mod Phys 69:1269–1281

    Google Scholar 

  2. Albert JT, Nadrowski B, Göpfert MC (2007) Mechanical signatures of transducer gating in the Drosophila ear. Curr Biol 17:1000–1006. doi:10.1016/j.cub.2007.05.004

    CAS  PubMed  Google Scholar 

  3. Arthur BJ, Wyttenbach Ra, Harrington LC, Hoy RR (2010) Neural responses to one- and two-tone stimuli in the hearing organ of the dengue vector mosquito. J Exp Biol 213:1376–1385. doi:10.1242/jeb.033357

    PubMed Central  PubMed  Google Scholar 

  4. Ashmore J, Avan P, Brownell WE et al (2010) The remarkable cochlear amplifier. Hear Res 266:1–17. doi:10.1016/j.heares.2010.05.001

    CAS  PubMed  Google Scholar 

  5. Avitabile D, Homer M, Champneys AR et al (2010) Mathematical modelling of the active hearing process in mosquitoes. J R Soc Interface 7:105–122. doi:10.1098/rsif.2009.0091

    CAS  PubMed Central  PubMed  Google Scholar 

  6. Avitabile D, Homer M, Jackson J et al (2011) Modelling the active hearing process in mosquitoes. AIP Conf Proc 1403:447–452. doi:10.1063/1.3658129

    Google Scholar 

  7. Barral J, Martin P (2012) Phantom tones and suppressive masking by active nonlinear oscillation of the hair-cell bundle. Proc Natl Acad Sci 109:E1344–E1351. doi:10.1073/pnas.1202426109

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Belyantseva IA, Adler H, Curi R et al (2000) Expression and localization of prestin and the sugar transporter GLUT-5 during development of electromotility in cochlear outer hair cells. J Neurosci 20:RC116

    CAS  PubMed  Google Scholar 

  9. Beurg M, Tan X, Fettiplace R (2013) A prestin motor in chicken auditory hair cells: active force generation in a nonmammalian species. Neuron 79:69–81. doi:10.1016/j.neuron.2013.05.018

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Bialek W (1987) Physical limits to sensation and perception. Annu Rev Biophys Biophys Chem 16:455–478. doi:10.1146/annurev.bb.16.060187.002323

  11. Boekhoff-Falk G (2005) Hearing in Drosophila: development of Johnston’s organ and emerging parallels to vertebrate ear development. Dev Dyn 232:550–558. doi:10.1002/dvdy.20207

    CAS  PubMed  Google Scholar 

  12. Camalet S, Jülicher F, Prost J (1999) Self-organized beating and swimming of internally driven filaments. Phys Rev Lett 82:1590–1593. doi:10.1103/PhysRevLett.82.1590

    CAS  Google Scholar 

  13. Camalet S, Duke T, Jülicher F, Prost J (2000) Auditory sensitivity provided by self-tuned critical oscillations of hair cells. Proc Natl Acad Sci USA 97:3183–3188

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Cator LJ, Arthur BJ, Harrington LC, Hoy RR (2009) Harmonic convergence in the love songs of the dengue vector mosquito. Science 323(5917):1077–1079. doi:10.1126/science.1166541

    CAS  PubMed Central  PubMed  Google Scholar 

  15. Champneys AR, Avitabile D, Homer M et al (2011) The mechanics of hearing: a comparative case study in bio-mathematical modelling. ANZIAM J 52:225–249. doi:10.1017/S1446181111000733

    Google Scholar 

  16. Choe Y, Magnasco MO, Hudspeth AJ (1998) A model for amplification of hair-bundle motion by cyclical binding of Ca2+ to mechanoelectrical-transduction channels. Proc Natl Acad Sci 95:15321–15326

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Christensen AP, Corey DP (2007) TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci 8:510–521. doi:10.1038/nrn2149

    CAS  PubMed  Google Scholar 

  18. Coro F, Kossl M (1998) Distortion-product otoacoustic emissions from the tympanic organ in two noctuoid moths. J Comp Physiol A 183:525–531

    Google Scholar 

  19. Duke TAJ, Jülicher F (2007) Critical oscillators as active elements in hearing. In: Manley GA, Fay RR, Popper AN (eds) Active processes and otoacoustic emissions in hearing. Springer, New York, pp 63–92

    Google Scholar 

  20. Eberl DF, Hardy RW, Kernan MJ (2000) Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci 20:5981–5988

    CAS  PubMed  Google Scholar 

  21. Effertz T, Wiek R, Göpfert MC (2011) NompC TRP channel is essential for Drosophila sound receptor function. Curr Biol 21:592–597. doi:10.1016/j.cub.2011.02.048

    CAS  PubMed  Google Scholar 

  22. Effertz T, Nadrowski B, Piepenbrock D et al (2012) Direct gating and mechanical integrity of Drosophila auditory transducers require TRPN1. Nat Neurosci 15:1198–1200. doi:10.1038/nn.3175

    CAS  PubMed  Google Scholar 

  23. Fettiplace R, Hackney CM (2006) The sensory and motor roles of auditory hair cells. Nat Rev Neurosci 7:19–29. doi:10.1038/nrn1828

    CAS  PubMed  Google Scholar 

  24. Fischer S, Samietz J, Wäckers F, Dorn S (2001) Interaction of vibrational and visual cues in parasitoid host location. J Comp Physiol A 187:785–791. doi:10.1007/s00359-001-0249-7

    CAS  PubMed  Google Scholar 

  25. Gerhardt HC, Huber F (2002) Acoustic communications in insects and anurans. The University of Chicago press, Chicago and London

    Google Scholar 

  26. Gibson G, Russell I (2006) Flying in tune: sexual recognition in mosquitoes. Curr Biol 16(13):1311–1316. doi:10.1016/j.cub.2006.05.053

    CAS  PubMed  Google Scholar 

  27. Gillespie PG, Cyr JL (2004) Myosin-1c, the hair cell’s adaptation motor. Annu Rev Physiol 66:521–545. doi:10.1146/annurev.physiol.66.032102.112842

    CAS  PubMed  Google Scholar 

  28. Gong ZF, Son WS, Chung YD et al (2004) Two interdependent TRPV channel subunits, Inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 24:9059–9066

    CAS  PubMed  Google Scholar 

  29. Göpfert MC (2008) Amplification and feedback in invertebrates. In: Allan IB, Akimichi K, Gordon MS et al (eds) Senses: a comprehensive reference. Academic press, New York, pp 293–299

    Google Scholar 

  30. Göpfert MC, Robert D (2001) Active auditory mechanics in mosquitoes. Proc R Soc B 268:333–339. doi:10.1098/rspb.2000.1376

    PubMed Central  PubMed  Google Scholar 

  31. Göpfert MC, Robert D (2002) The mechanical basis of Drosophila audition. J Exp Biol 205:1199–1208

    PubMed  Google Scholar 

  32. Göpfert MC, Robert D (2003) Motion generation by Drosophila mechanosensory neurons. Proc Natl Acad Sci USA 100:5514–5519. doi:10.1073/pnas.0737564100

    PubMed Central  PubMed  Google Scholar 

  33. Göpfert MC, Robert D (2007) Active processes in insect hearing. In: Manley GA, Fay RR, Popper AN (eds) Active processes and otoacoustic emissions in hearing. Springer, New York, pp 191–209

    Google Scholar 

  34. 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

    PubMed  Google Scholar 

  35. Göpfert MC, Humphris ADL, Albert JT et al (2005) Power gain exhibited by motile mechanosensory neurons in Drosophila ears. Proc Natl Acad Sci USA 102:325–330. doi:10.1073/pnas.0405741102

    PubMed Central  PubMed  Google Scholar 

  36. Göpfert MC, Albert JT, Nadrowski B, Kamikouchi A (2006) Specification of auditory sensitivity by Drosophila TRP channels. Nat Neurosci 9:999–1000. doi:10.1038/nn1735

    PubMed  Google Scholar 

  37. Gray EG (1960) The fine structure of the insect ear. Phil Trans Roy Soc B 243:75–94

    Google Scholar 

  38. He DZZ, Lovas S, Ai Y et al (2014) Prestin at year 14: progress and prospect. Hear Res 311:25–35. doi:10.1016/j.heares.2013.12.002

    CAS  PubMed  Google Scholar 

  39. Holt JR, Gillespie SKH, Provance DW et al (2002) A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108:371–381. doi:10.1016/S0092-8674(02)00629-3

    CAS  PubMed  Google Scholar 

  40. Homma K, Dallos P (2011a) Dissecting the electromechanical coupling mechanism of the motor-protein prestin. Commun Integr Biol 4:450–453

    CAS  PubMed Central  PubMed  Google Scholar 

  41. Homma K, Dallos P (2011b) Evidence that prestin has at least two voltage- dependent steps. J Biol Chem 286:2297–2307

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Hudspeth AJ (1989) How the ear’s works work. Nature 341:397–404. doi:10.1038/341397a0

    CAS  Google Scholar 

  43. Hudspeth AJ (2008) Making an effort to listen: mechanical amplification in the ear. Neuron 59:530–545. doi:10.1016/j.neuron.2008.07.012

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Hudspeth AJ, Choe Y, Mehta AD, Martin P (2000) Putting ion channels to work: mechanoelectrical transduction, adaptation, and amplification by hair cells. Proc Natl Acad Sci USA 97:11765–11772. doi:10.1073/pnas.97.22.11765

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Hudspeth AJ, Jülicher F, Martin P (2010) A critique of the critical cochlea: Hopf—a bifurcation—is better than none. J Neurophysiol 104:1219–1229. doi:10.1152/jn.00437.2010

    CAS  PubMed Central  PubMed  Google Scholar 

  46. Humphries S (2013) A physical explanation of the temperature dependence of physiological processes mediated by cilia and flagella. Proc Natl Acad Sci USA 110:14693–14698. doi:10.1073/pnas.1300891110

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Jackson JC, Robert D (2006) Nonlinear auditory mechanism enhances female sounds for male mosquitoes. Proc Natl Acad Sci USA 103:16734–16739. doi:10.1073/pnas.0606319103

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Jarman AP, Grell EH, Ackerman L et al (1994) Atonal is the proneural gene for Drosophila photoreceptors. Nature 369:398–400. doi:10.1038/369398a0

    CAS  PubMed  Google Scholar 

  49. Jarman AP, Sun Y, Jan LY, Jan YN (1995) Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 121:2019–2030

    CAS  PubMed  Google Scholar 

  50. Jülicher F, Andor D, Duke T (2001) Physical basis of two-tone interference in hearing. Proc Natl Acad Sci 98:9080–9085. doi:10.1073/pnas.151257898

    PubMed Central  PubMed  Google Scholar 

  51. 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. doi:10.1002/cne.21075

    PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  53. Kavlie RG, Albert JT (2014) Transduction and amplification in the ear : insights from insects. In: Köppl C, Manley GA, Popper A, Fay RR (eds) Insights from comparative hearing research. Springer, New York, pp 13–35. doi:10.1007/2506

    Google Scholar 

  54. Kavlie RG, Kernan MJ, Eberl DF (2010) Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility. Genetics 185:177–188. doi:10.1534/genetics.110.114009

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Kavlie RG, Fritz JL, Nies F et al (2014) Prestin is an anion transporter dispensable for mechanical feedback amplification in Drosophila hearing. J Comp Physiol A. doi:10.1007/s00359-014-0960-9

  56. Kernan MJ (2007) Mechanotransduction and auditory transduction in Drosophila. Pflugers Arch Eur J Physiol 454:703–720. doi:10.1007/s00424-007-0263-x

    CAS  Google Scholar 

  57. Kernan M, Cowan D, Zuker C (1994) Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12:1195–1206. doi:10.1016/0896-6273(94)90437-5

    CAS  PubMed  Google Scholar 

  58. Kim J, Chung YD, Park D-Y et al (2003) A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84. doi:10.1038/nature01733

    CAS  PubMed  Google Scholar 

  59. Kindt KS, Finch G, Nicolson T (2012) Kinocilia mediate mechanosensitivity in developing zebrafish hair cells. Dev Cell 23:329–341. doi:10.1016/j.devcel.2012.05.022

    CAS  PubMed Central  PubMed  Google Scholar 

  60. Kössl M, Boyan GS (1998) Acoustic distortion products from the ear of a grasshopper. J Acoust Soc Am 104:326–335

    Google Scholar 

  61. Larsen ON, Kleindienst HU, Michelsen A (1989) Biophysical aspects of sound reception. In: Huber F, Moore TE, Loher W (eds) Cricket behaviour and neurobiology. Cornell University Press, Ithaca and London, pp 364–390

    Google Scholar 

  62. Lee E, Sivan-Loukianova E, Eberl DF, Kernan MJ (2008) An IFT-A protein is required to delimit functionally distinct zones in mechanosensory cilia. Curr Biol 18:1899–1906. doi:10.1016/j.cub.2008.11.020

    CAS  PubMed Central  PubMed  Google Scholar 

  63. Lee J, Moon S, Cha Y, Chung YD (2010) Drosophila TRPN(= NOMPC) channel localizes to the distal end of mechanosensory cilia. PLoS One 5:e11012. doi:10.1371/journal.pone.0011012

    PubMed Central  PubMed  Google Scholar 

  64. Lehnert BP, Baker AE, Gaudry Q et al (2013) Distinct roles of TRP channels in auditory transduction and amplification in Drosophila. Neuron 77:115–128. doi:10.1016/j.neuron.2012.11.030

    CAS  PubMed  Google Scholar 

  65. LeMasurier M, Gillespie PG (2005) Hair-cell mechanotransduction and cochlear amplification. Neuron 48:403–415. doi:10.1016/j.neuron.2005.10.017

    CAS  PubMed  Google Scholar 

  66. Liang X, Madrid J, Ga R et al (2013) A NompC-dependent membrane-microtubule connector is a candidate for the gating spring in fly mechanoreceptors. Curr Biol 23:755–763. doi:10.1016/j.cub.2013.03.065

    CAS  PubMed  Google Scholar 

  67. Liberman MC, Gao J, He DZZ et al (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419:300–304

    CAS  PubMed  Google Scholar 

  68. Lillywhite PG (1977) Single photon signals and transduction in an insect eye. J Comp Physiol A 122:189–200. doi:10.1007/BF00611889

    Google Scholar 

  69. Malkin R, Mcdonagh TR, Mhatre N et al (2014) Energy localization and frequency analysis in the locust ear. J R Soc Interface 11:20130857

    PubMed  Google Scholar 

  70. Mammano F, Ashmore J (1993) Reverse transduction measured in the isolated cochlea by laser Michelson interferometry. Nature 365:838–841

    CAS  PubMed  Google Scholar 

  71. Manley GA (2000) Cochlear mechanisms from a phylogenetic viewpoint. Proc Natl Acad Sci USA 97:11736–11743. doi:10.1073/pnas.97.22.11736

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Manley GA (2001) Evidence for an active process and a cochlear amplifier in nonmammals. J Neurophysiol 86:541–549

    CAS  PubMed  Google Scholar 

  73. Manley GA, Ladher R (2008) Phylogeny and evolution of ciliated mechanoreceptor cells. In: Allan IB, Akimichi K, Gordon MS et al (eds) Senses: a comprehensive reference. Academic press, New York, pp 1–34

    Google Scholar 

  74. Maoiléidigh DO, Jülicher F (2010) The interplay between active hair bundle motility and electromotility in the cochlea. J Acoust Soc Am 128:1175–1190. doi:10.1121/1.3463804

    Google Scholar 

  75. 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. doi:10.1073/pnas.251530498

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Martin P, Mehta aD, Hudspeth aJ (2000) Negative hair-bundle stiffness betrays a mechanism for mechanical amplification by the hair cell. Proc Natl Acad Sci USA 97:12026–12031. doi:10.1073/pnas.210389497

    CAS  PubMed Central  PubMed  Google Scholar 

  77. 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 98:14380–14385

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Mhatre N, Robert D (2013) A tympanal insect ear exploits a critical oscillator for active amplification and tuning. Curr Biol 23:1952–1957. doi:10.1016/j.cub.2013.08.028

    CAS  PubMed Central  PubMed  Google Scholar 

  79. Michelsen A, Löhe G (1995) Tuned directionality in cricket ears. Nature 375:639

    CAS  Google Scholar 

  80. Michelsen A, Popov AV, Lewis B (1994) Physics of directional hearing in the cricket Gryllus bimaculatus. J Comp Physiol A 175:153–164

    Google Scholar 

  81. Miles RN, Robert D, Hoy RR (1995) Mechanically coupled ears for directional hearing in the parasitoid fly Ormia ochracea. J Acoust Soc Am 98:3059–3070

    CAS  PubMed  Google Scholar 

  82. Möckel D, Seyfarth E-A, Kössl M (2007) The generation of DPOAEs in the locust ear is contingent upon the sensory neurons. J Comp Physiol A 193:871–879. doi:10.1007/s00359-007-0239-5

    Google Scholar 

  83. Möckel D, Seyfarth E-A, Kössl M (2011) Otoacoustic emissions in bushcricket ears: general characteristics and the influence of the neuroactive insecticide pymetrozine. J Comp Physiol A 197:193–202. doi:10.1007/s00359-010-0599-0

    Google Scholar 

  84. Möckel D, Kössl M, Lang J, Nowotny M (2012) Temperature dependence of distortion-product otoacoustic emissions in tympanal organs of locusts. J Exp Biol 215:3309–3316. doi:10.1242/jeb.074377

    PubMed  Google Scholar 

  85. Moir HM, Jackson JC, Windmill JFC (2011) No evidence for DPOAEs in the mechanical motion of the locust tympanum. J Exp Biol 214:3165–3172. doi:10.1242/jeb.056465

    PubMed  Google Scholar 

  86. Montealegre-Z F, Jonsson T, Robson-Brown Ka et al (2012) Convergent evolution between insect and mammalian audition. Science 338:968–971. doi:10.1126/science.1225271

    CAS  PubMed  Google Scholar 

  87. Nadrowski B, Göpfert MC (2009a) Level-dependent auditory tuning. Commun Integr. Biol 2(1):7–10. doi:10.1016/j.cub.2008.07.095.www.landesbioscience.com

    Google Scholar 

  88. Nadrowski B, Göpfert MC (2009b) Modeling auditory transducer dynamics. Curr Opin Otolaryngol Head Neck Surg 17:400–406. doi:10.1097/MOO.0b013e3283303443

    PubMed  Google Scholar 

  89. Nadrowski B, Martin P, Jülicher F (2004) Active hair-bundle motility harnesses noise to operate near an optimum of mechanosensitivity. Proc Natl Acad Sci USA 101:12195–12200. doi:10.1073/pnas.0403020101

    CAS  PubMed Central  PubMed  Google Scholar 

  90. Nadrowski B, Albert JT, Göpfert MC (2008) Transducer-based force generation explains active process in Drosophila hearing. Curr Biol 18:1365–1372. doi:10.1016/j.cub.2008.07.095

    CAS  PubMed  Google Scholar 

  91. Nelson ME, MacIver MA (2006) Sensory acquisition in active sensing systems. J Comp Physiol A 192:573–586. doi:10.1007/s00359-006-0099-4

    CAS  Google Scholar 

  92. Nobili R, Mammano F, Ashmore J (1998) How well do we understand the cochlea? Trends Neurosci 21:159–167

    CAS  PubMed  Google Scholar 

  93. Paton JA, Capranica RR, Dragsten PR, Webb WW (1977) Physical basis for auditory frequency analysis in field crickets (Gryllidae). J Comp Physiol A 119:221–240. doi:10.1007/BF00656635

    Google Scholar 

  94. Peng AW, Ricci AJ (2011) Somatic motility and hair bundle mechanics, are both necessary for cochlear amplification? Hear Res 273:109–122. doi:10.1016/j.heares.2010.03.094

    PubMed Central  PubMed  Google Scholar 

  95. Riabinina O, Dai M, Duke T, Albert JTT (2011) Active process mediates species-specific tuning of Drosophila ears. Curr Biol 21:658–664. doi:10.1016/j.cub.2011.03.001

    CAS  PubMed  Google Scholar 

  96. Robert D (1989) The auditory behaviour of flying locusts. J Exp Biol 147:279–301

    Google Scholar 

  97. Robert D (2009) Insect bioacoustics : mosquitoes make an effort to listen to each other. Curr Biol 19:R446–R449. doi:10.1016/j.cub.2009.04.021

    CAS  PubMed  Google Scholar 

  98. Robert D, Miles RN, Hoy RR (1996) Directional hearing by mechanical coupling in the parasitoid fly Ormia ochracea. J Comp Physiol A 179:29–44

    CAS  PubMed  Google Scholar 

  99. Robert D, Miles RN, Hoy RR (1998) Tympanal mechanics in the parasitoid fly Ormia ochracea: intertympanal coupling during mechanical vibration. J Comp Physiol A 183:443–452

    Google Scholar 

  100. Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81:1305–1352

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Rossler W, Hubschen A, Schul J, Kalmring K (1994) Functional morphology of bushcricket ears: comparison between two species belonging to the Phaneropterinae and Decticinae (Insecta, Ensifera). Zoomorphology 114:39–46

    Google Scholar 

  102. Salazar VL, Krahe R, Lewis JE (2013) The energetics of electric organ discharge generation in gymnotiform weakly electric fish. J Exp Biol 216:2459–2468. doi:10.1242/jeb.082735

    CAS  PubMed  Google Scholar 

  103. Santos-Sacchi J (2003) New tunes from Corti’s organ: the outer hair cell boogie rules. Curr Opin Neurobiol 13:459–468. doi:10.1016/S0959-4388(03)00100-4

    CAS  PubMed  Google Scholar 

  104. Senthilan PR, Piepenbrock D, Ovezmyradov G et al (2012) Drosophila auditory organ genes and genetic hearing defects. Cell 150:1042–1054. doi:10.1016/j.cell.2012.06.043

    CAS  PubMed  Google Scholar 

  105. Siegel J (2008) Otoacoustic emissions. In: Allan IB, Akimichi K, Gordon MS et al (eds) Senses: a comprehensive reference. Academic press, New York, pp 237–261

    Google Scholar 

  106. Speakman JR, Anderson ME, Racey PA (1989) The energy cost of echolocation in pipistrelle bats (Pipistrellus pipistrellus). J Comp Physiol A 165:679–685

    Google Scholar 

  107. Stoop R, Kern A, Göpfert M et al (2006) A generalization of the van-der-Pol oscillator underlies active signal amplification in Drosophila hearing. Eur Biophys J 35:511–516. doi:10.1007/s00249-006-0059-5

    CAS  PubMed  Google Scholar 

  108. Szalai R, Champneys A, Homer M et al (2013) Comparison of nonlinear mammalian cochlear-partition models. J Acoust Soc Am 133:323–336

    PubMed  Google Scholar 

  109. 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. doi:10.1002/jemt.20053

    PubMed Central  PubMed  Google Scholar 

  110. Trautwein MD, Wiegmann BM, Beutel R et al (2012) Advances in insect phylogeny at the dawn of the postgenomic era. Annu Rev Entomol 57:449–468. doi:10.1146/annurev-ento-120710-100538

    CAS  PubMed  Google Scholar 

  111. Walker RG, Hudspeth aJ (1996) Calmodulin controls adaptation of mechanoelectrical transduction by hair cells of the bullfrog’s sacculus. Proc Natl Acad Sci USA 93:2203–2207. doi:10.1073/pnas.93.5.2203

    CAS  PubMed Central  PubMed  Google Scholar 

  112. Warren B, Gibson G, Russell IJ (2009) Sex recognition through midflight mating duets in Culex mosquitoes is mediated by acoustic distortion. Curr Biol 19:485–491. doi:10.1016/j.cub.2009.01.059

    CAS  PubMed  Google Scholar 

  113. Warren B, Lukashkin AN, Russell IJ (2010) The dynein-tubulin motor powers active oscillations and amplification in the hearing organ of the mosquito. Proc Biol Sci 277:1761–1769. doi:10.1098/rspb.2009.2355

    PubMed Central  PubMed  Google Scholar 

  114. Weber T, Goepfert M, Winter H et al (2003) Expression of prestin-homologous solute carrier (SLC26) in auditory organs of nonmammalian vertebrates and insects. Proc Natl Acad Sci USA 100:7690–7695

    CAS  PubMed Central  PubMed  Google Scholar 

  115. Windmill JFC, Göpfert MC, Robert D (2005) Tympanal travelling waves in migratory locusts. J Exp Biol 208:157–168. doi:10.1242/jeb.01332

    PubMed  Google Scholar 

  116. Windmill JFC, Jackson JC, Tuck EJ, Robert D (2006) Keeping up with bats: dynamic auditory tuning in a moth. Curr Biol 16:2418–2423. doi:10.1016/j.cub.2006.09.066

    CAS  PubMed  Google Scholar 

  117. Yack JE (2004) The structure and function of auditory chordotonal organs in insects. Microsc Res Tech 63:315–337. doi:10.1002/jemt.20051

    PubMed  Google Scholar 

  118. Yorozu S, Wong S, Fischer BJ et al (2009) Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 458:201–204

    CAS  PubMed Central  PubMed  Google Scholar 

  119. Young D (1977) Structure and function of the auditory system of the cicada, Cystosoma saundersii. J Comp Physiol A. 45:23–45

    Google Scholar 

  120. Young D, Ball E (1974) Structure and development of the auditory system in the prothoracic leg of the cricket Teleogryllus commodus (Walker); I. Adult structure. Z Zellforsch Mikrosk Anat 147:293–312

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The author would like to acknowledge the support of the UK India Education and Research Initiative, a Biotechnology and Biological Sciences Research Council Grant and a Marie Curie fellowship. I would also like to gratefully acknowledge the Wissenschaftskolleg zu Berlin for a College for Life Sciences fellowship (2013/2014) during which this review was partly written. I would also like to thank the editors of this special issue for inviting me to write this review and for their patience while I did. I would also like to thank two anonymous referees whose comments and suggestions greatly improved this manuscript.

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Mhatre, N. Active amplification in insect ears: mechanics, models and molecules. J Comp Physiol A 201, 19–37 (2015). https://doi.org/10.1007/s00359-014-0969-0

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Keywords

  • Acoustic communication
  • Active hearing
  • Insect hearing
  • Active auditory amplification
  • Active mechanosensation