Altered traveling wave propagation and reduced endocochlear potential associated with cochlear dysplasia in the BETA2/NeuroD1 null mouse

JARO - Journal of the Association for Research in Otolaryngology

Volumn 8, Issue 4, 2007, Pages 447-463

  Xia, Anping ^a   Visosky, Ann Marie B ^a   Cho, Jang Hyeon ^a   Tsai, Ming Jer ^a   Pereira, Fred A ^a,b   Oghalai, John S ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b Rice University   (United States)

Author keywords

Cochlea; Cochlear malformation; Cochlear mechanics; Cochlear partition; Hearing loss; Incomplete partition

Indexed keywords

MEMBRANE PROTEIN; PRESTIN; UNCLASSIFIED DRUG;

ACOUSTICS; ANALYTIC METHOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COCHLEA DUCT; COCHLEA POTENTIAL; COCHLEAR DYSPLASIA; DISTORTION PRODUCT OTOACOUSTIC EMISSION; EAR DYSPLASIA; FENESTRATION; HAIR CELL; HETEROZYGOTE; LASER DOPPLER VIBROMETRY; MECHANICAL STIMULATION; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPIRAL GANGLION; STAPES; STIMULUS RESPONSE; WAVEFORM; WILD TYPE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BIOMECHANICS; COCHLEA; COCHLEAR MICROPHONIC POTENTIALS; EVOKED POTENTIALS, AUDITORY, BRAIN STEM; FEMALE; MALE; MICE; MICE, TRANSGENIC; OTOACOUSTIC EMISSIONS, SPONTANEOUS;

EID: 35848954541     PISSN: 15253961     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10162-007-0092-9     Document Type: Article

References (82)

1. Bamiou DE, Savy L, O'Mahoney C, Phelps P, Sirimanna T. Unilateral sensorineural hearing loss and its aetiology in childhood: the contribution of computerised tomography in aetiological diagnosis and management. Int J Pediatr Otorhinolaryngol 51(2):91-99, 1999.
2. Brownell WE, Bader CR, Bertrand D, de Ribaupierre Y. Evoked mechanical responses of isolated cochlear outer hair cells. Science 227(4683):194-196, 1985.
3. Cai H, Manoussaki D, Chadwick R. Effects of coiling on the micromechanics of the mammalian cochlea. J R Soc Interface 2(4):341-348, 2005.
4. Cai H, Shoelson B, Chadwick RS. Evidence of tectorial membrane radial motion in a propagating mode of a complex cochlear model. Proc Natl Acad Sci USA 101(16):6243-6248, 2004.
5. Chadwick RS, Fourney ME, Neiswander P. Modes and waves in a cochlear model. Hear Res 2(3-4):475-483, 1980.
6. Chan DK, Hudspeth AJ. Ca(2+) current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat Neurosci 8(2):149-155, 2005.
7. Cheatham MA, Dallos P. Two-tone interactions in the cochlear microphonic. Hear Res 8(1):29-48, 1982.
8. Cheatham MA, Dallos P. Low-frequency modulation of inner hair cell and organ of Corti responses in the guinea pig cochlea. Hear Res 108(1-2):191-212, 1997.
9. Cody AR, Johnstone BM. Single auditory neuron response during acute acoustic trauma. Hear Res 3(1):3-16, 1980.
10. Cooper NP, Rhode WS. Nonlinear mechanics at the apex of the guinea-pig cochlea. Hear Res 82(2):225-243, 1995.
11. Cooper NP, Rhode WS. Fast traveling waves, slow traveling waves and their interactions in experimental studies of cochlear mechanics. Auditory Neuroscience 2:289-299, 1996.
12. Coticchia JM, Gokhale A, Waltonen J, Sumer B. Characteristics of sensorineural hearing loss in children with inner ear anomalies. Am J Otolaryngol 27(1):33-38, 2006.
13. Cremers CW, Admiraal RJ, Huygen PL, Bolder C, Everett LA, Joosten FB, Green ED, van Camp G, Otten BJ. Progressive hearing loss, hypoplasia of the cochlea and widened vestibular aqueducts are very common features in Pendred's syndrome. Int J Pediatr Otorhinolaryngol 45(2):113-123, 1998.
14. Dallos P. Electrical correlates of mechanical events in the cochlea. Audiology 14(5-6):408-418, 1975.
15. Dallos P, Hallworth R, Evans BN. Theory of electrically driven shape changes of cochlear outer hair cells. J Neurophysiol 70(1):299-323, 1993.
16. Davis H. An active process in cochlear mechanics. Hear Res 9(1):79-90, 1983.
17. Fettiplace R, Hackney CM. The sensory and motor roles of auditory hair cells. Nat Rev Neurosci 7(1):19-29, 2006.
18. Gale JE, Marcotti W, Kennedy HJ, Kros CJ, Richardson GP. FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J Neurosci 21(18):7013-7025, 2001.
19. Geisler CD. From sound to synapse: physiology of the mammalian ear. New York: Oxford University Press. xiv, 381 p, 1998.
20. Griesinger CB, Richards CD, Ashmore JF. Fm1-43 reveals membrane recycling in adult inner hair cells of the mammalian cochlea. J Neurosci 22(10):3939-3952, 2002.
21. Griesinger CB, Richards CD, Ashmore JF. Apical endocytosis in outer hair cells of the mammalian cochlea. Eur J Neurosci 20(1):41-50, 2004.
22. Griesinger CB, Richards CD, Ashmore JF. Fast vesicle replenishment allows indefatigable signalling at the first auditory synapse. Nature 435(7039):212-215, 2005.
23. Gummer AW, Hemmert W, Zenner HP. Resonant tectorial membrane motion in the inner ear: its crucial role in frequency tuning. Proc Natl Acad Sci USA 93(16):8727-8732, 1996.
24. Gummer AW, Meyer J, Frank G, Scherer MP, Preyer S. Mechanical transduction in outer hair cells. Audiol Neurootol 7(1):13-16, 2002.
25. Halsey K, Fegelman K, Raphael Y, Grosh K, Dolan DF. Long-term effects of acoustic trauma on electrically evoked otoacoustic emission. J Assoc Res Otolaryngol 6(4):324-340, 2005.
26. Helmholtz Hv, Ellis AJ. On the sensations of tone as a physiological basis for the theory of music. New York,: Dover Publications. xix, 576 p., 1954.
27. Hemmert W, Zenner H, Gummer AW. Characteristics of the travelling wave in the low-frequency region of a temporal-bone preparation of the guinea-pig cochlea. Hear Res 142(1-2):184-202, 2000.
28. Hubbard AE, Mountain DC. Haircell forward and reverse transduction: differential suppression and enhancement. Hear Res 43(2-3):269-272, 1990.
29. Jackler RK, De La Cruz A. The large vestibular aqueduct syndrome. Laryngoscope 99(12):1238-1242; discussion 1242-1243, 1989.
30. Jackler RK, Luxford WM, House WF. Congenital malformations of the inner ear: a classification based on embryogenesis. Laryngoscope 97(3 Pt 2 Suppl 40):2-14, 1987.
31. Jia S, He DZ. Motility-associated hair-bundle motion in mammalian outer hair cells. Nat Neurosci 8(8):1028-1034, 2005.
32. Kaneko T, Harasztosi C, Mack AF, Gummer AW. Membrane traffic in outer hair cells of the adult mammalian cochlea. Eur J Neurosci 23(10):2712-2722, 2006.
33. Kennedy HJ, Evans MG, Crawford AC, Fettiplace R. Depolarization of cochlear outer hair cells evokes active hair bundle motion by two mechanisms. J Neurosci 26(10):2757-2766, 2006.
34. Khanna SM, Ulfendahl M, Steele CR. Vibration of reflective beads placed on the basilar membrane. Hear Res 116(1-2):71-85, 1998.
35. Kim WY, Fritzsch B, Serls A, Bakel LA, Huang EJ, Reichardt LF, Barth DS, Lee JE. NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 128(3):417-426, 2001.
36. Lee JE, Hollenberg SM, Snider L, Turner DL, Lipnick N, Weintraub H. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268(5212):836-844, 1995.
37. Legan PK, Lukashkina VA, Goodyear RJ, Kossi M, Russell IJ, Richardson GP. A targeted deletion in alpha-tectorin reveals that the tectorial membrane is required for the gain and timing of cochlear feedback. Neuron 28(1):273-285, 2000.
38. Legan PK, Lukashkina VA, Goodyear RJ, Lukashkin AN, Verhoeven K, Van Camp G, Russell IJ, Richardson GP. A deafness mutation isolates a second role for the tectorial membrane in hearing. Nat Neurosci 8(8):1035-1042, 2005.
39. Liberman MC. The cochlear frequency map for the cat: labeling auditory-nerve fibers of known characteristic frequency. J Acoust Soc Am 72(5):1441-1449, 1982.
40. Liberman MC, Gao J, He DZ, Wu X, Jia S, Zuo J. Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419(6904):300-304, 2002.
41. Liberman MC, Zuo J, Guinan JJ, Jr. Otoacoustic emissions without somatic motility: can stereocilia mechanics drive the mammalian cochlea? J Acoust Soc Am 116(3):1649-1655, 2004.
42. Liu M, Pereira FA, Price SD, Chu MJ, Shope C, Himes D, Eatock RA, Brownell WE, Lysakowski A, Tsai MJ. Essential role of BETA2/NeuroD1 in development of the vestibular and auditory systems. Genes Dev 14(22):2839-2854, 2000a.
43. Liu M, Pleasure SJ, Collins AE, Noebels JL, Naya FJ, Tsai MJ, Lowenstein DH. Loss of BETA2/NeuroD leads to malformation of the dentate gyrus and epilepsy. Proc Natl Acad Sci USA 97(2):865-870, 2000b.
44. Mammano F, Ashmore JF. Reverse transduction measured in the isolated cochlea by laser Michelson interferometry. Nature 365(6449):838-841, 1993.
45. Mammano F, Ashmore JF. A laser interferometer for sub-nanometre measurements in the cochlea. J Neurosci Methods 60(1-2):89-94, 1995.
46. Manoussaki D, Dimitriadis EK, Chadwick RS. Cochlea's graded curvature effect on low frequency waves. Phys Rev Lett 96(8):088701, 2006.
47. Meyers JR, MacDonald RB, Duggan A, Lenzi D, Standaert DG, Corwin JT, Corey DP. Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J Neurosci 23(10):4054-4065, 2003.
48. Morioka I, Reuter G, Reiss P, Gummer AW, Hemmert W, Zenner HP. Sound-induced displacement responses in the plane of the organ of Corti in the isolated guinea-pig cochlea. Hear Res 83(1-2):142-150, 1995.
49. Morsli H, Choo D, Ryan A, Johnson R, Wu DK. Development of the mouse inner ear and origin of its sensory organs. J Neurosci 18(9):3327-3335, 1998.
50. Mountain DC, Hubbard AE. Rapid force production in the cochlea. Hear Res 42(2-3):195-202, 1989.
51. Muller M, von Hunerbein K, Hoidis S, Smolders JW. A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 202(1-2):63-73, 2005.
52. Naya FJ, Stellrecht CM, Tsai MJ. Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev 9(8):1009-1019, 1995.
53. Nowotny M, Gummer AW. Nanomechanics of the subtectorial space caused by electromechanics of cochlear outer hair cells. Proc Natl Acad Sci USA 103(7):2120-2125, 2006.
54. Nuttall AL, Dolan DF, Avinash G. Laser Doppler velocimetry of basilar membrane vibration. Hear Res 51(2):203-213, 1991.
55. Nuttall AL, Zheng J, Ren T, de Boer E. Electrically evoked otoacoustic emissions from apical and basal perilymphatic electrode positions in the guinea pig cochlea. Hear Res 152(1-2):77-89, 2001.
56. Oghalai JS. Chlorpromazine inhibits cochlear function in guinea pigs. Hear Res 198(1-2):59-68, 2004.
57. Ohlemiller KK. Contributions of mouse models to understanding of age- and noise-related hearing loss. Brain Res 1091(1):89-102, 2006.
58. Ohlemiller KK, Lett JM, Gagnon PM. Cellular correlates of age-related endocochlear potential reduction in a mouse model. Hear Res 220:10-26, 2006.
59. Olson ES. Direct measurement of intra-cochlear pressure waves. Nature 402(6761):526-529, 1999.
60. Ou HC, Harding GW, Bohne BA. An anatomically based frequency-place map for the mouse cochlea. Hear Res 145(1-2):123-129, 2000.
61. Overstreet EH, 3rd, Temchin AN, Ruggero MA. Passive basilar membrane vibrations in gerbil neonates: mechanical bases of cochlear maturation. J Physiol 545(Pt 1):279-288, 2002.
62. Patuzzi R. Cochlear micromechanics and macromechanics. In: Dallos P, Popper AN, Fay RR (eds) The Cochlea: Springer Handbook Of Auditory Research; v. 8. New York: Springer. p xii, 551 p., 1996.
63. Patuzzi R, Moleirinho A. Automatic monitoring of mechano-electrical transduction in the guinea pig cochlea. Hear Res 125(1-2):1-16, 1998.
64. Patuzzi RB, Yates GK, Johnstone BM. The origin of the low-frequency microphonic in the first cochlear turn of guinea-pig. Hear Res 39(1-2):177-188, 1989.
65. Paylor R, Glaser B, Mupo A, Ataliotis P, Spencer C, Sobotka A, Sparks C, Choi CH, Oghalai J, Curran S, Murphy KC, Monks S, Williams N, O'Donovan MC, Owen MJ, Scambler PJ, Lindsay E. Tbx1 haploinsufficiency is linked to behavioral disorders in mice and humans: implications for 22q11 deletion syndrome. Proc Natl Acad Sci USA 103(20):7729-7734, 2006.
66. Ren T. Longitudinal pattern of basilar membrane vibration in the sensitive cochlea. Proc Natl Acad Sci USA 99(26):17101-17106, 2002.
67. Ren T, Nuttall AL. Extracochlear electrically evoked otoacoustic emissions: a model for in vivo assessment of outer hair cell electromotility. Hear Res 92(1-2):178-183, 1995.
68. Ren T, Nuttall AL. Fine structure and multicomponents of the electrically evoked otoacoustic emission in gerbil. Hear Res 143(1-2):58-68, 2000.
69. Rhode WS. Observations of the vibration of the basilar membrane in squirrel monkeys using the Mossbauer technique. J Acoust Soc Am 49(4):Suppl 2:1218+, 1971.
70. Robles L, Ruggero MA. Mechanics of the mammalian cochlea. Physiol Rev 81(3):1305-1352, 2001.
71. Ruggero MA. Cochlear delays and traveling waves: comments on 'Experimental look at cochlear mechanics'. Audiology 33(3):131-142, 1994.
72. Ruggero MA, Rich NC. Furosemide alters organ of corti mechanics: evidence for feedback of outer hair cells upon the basilar membrane. J Neurosci 11(4):1057-1067, 1991.
73. Schrott A, Melichar I, Popelar J, Syka J. Deterioration of hearing function in mice with neural crest defect. Hear Res 46(1-2):1-7, 1990.
74. Schuknecht HF. Pathology of the ear. Philadelphia: Lea & Febiger. xv, 672 p, 1993.
75. Steel KP, Barkway C. Another role for melanocytes: their importance for normal stria vascularis development in the mammalian inner ear. Development 107(3):453-463, 1989.
76. Steel KP, Barkway C, Bock GR. Strial dysfunction in mice with cochleo-saccular abnormalities. Hear Res 27(1):11-26, 1987.
77. Stinckens C, Huygen PL, Joosten FB, Van Camp G, Otten B, Cremers CW. Fluctuant, progressive hearing loss associated with Meniere like vertigo in three patients with the Pendred syndrome. Int J Pediatr Otorhinolaryngol 61(3):207-215, 2001.
78. Ulfendahl M, Khanna SM, Flock A. Effects of opening and resealing the cochlea on the mechanical response in the isolated temporal bone preparation. Hear Res 57(1):31-37, 1991.
79. von Bekesy G. Experiments in hearing: McGraw-Hill, 1960.
80. Wenzel GI, Anvari B, Mazhar A, Pikkula B, Oghalai JS. Laser induced collagen remodeling and deposition within the basilar membrane of the mouse Cochlea. J Biomed Opt 12:021007, 2006.
81. Xue S, Mountain DC, Hubbard AE. Acoustic enhancement of electrically-evoked otoacoustic emissions reflects basilar membrane tuning: experiment results. Hear Res 70(1):121-126, 1993.
82. Zheng J, Shen W, He DZ, Long KB, Madison LD, Dallos P. Prestin is the motor protein of cochlear outer hair cells. Nature 405(6783):149-155, 2000.