Chlorpromazine alters cochlear mechanics and amplification: In vivo evidence for a role of stiffness modulation in the organ of Corti

Journal of Neurophysiology

Volumn 97, Issue 2, 2007, Pages 994-1004

  Zheng, Jiefu ^a   Deo, Niranjan ^b   Zou, Yuan ^a   Grosh, Karl ^b   Nuttall, Alfred L ^a,c,d,e,f  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d SHANGHAI JIAO TONG UNIVERSITY   (China)

^e Oregon Health and Science University Department of Biomedical Engineering   (United States)

^f OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORPROMAZINE; PRISTINAMYCIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASILAR MEMBRANE; BIOMECHANICS; COCHLEA; CONTROLLED STUDY; CORTI ORGAN; EVOKED AUDITORY RESPONSE; GUINEA PIG; HAIR CELL; IN VIVO STUDY; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; SOUND;

EID: 33846904945     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00774.2006     Document Type: Article

References (70)

1. Adachi M, Iwasa KH. Effect of diamide on force generation and axial stiffness of the cochlear outer hair cell. Biophys J 73: 2809-2818, 1997.
2. Awad A, Voruganti LNP. Neuroleptic dysphoria: revisiting the concept 50 years later. Acta Psychiatr Scand Suppl 427: 6-13, 2005.
3. Batta TJ, Panyi G, Gaspar R, Sziklai I. Active and passive behaviour in the regulation of stiffness of the lateral wall in outer hair cells of the guinea-pig. Pfluegers-Eur J Physiol 447: 328-336, 2003.
4. Borko R, Batta TJ, Sziklai I. Slow motility, electromotility and lateral wall stiffness in the isolated outer hair cells. Hear Res 207: 68-75, 2005.
5. Brownell WE, Bader CR, Bertrand D, de Ribaupierre Y. Evoked mechanical responses of isolated cochlear outer hair cells. Science 227: 194-196, 1985.
6. Brownell WE, Spector AA, Raphael RM, Popel AS. Micro- and nanomechanics of the cochlear outer hair cell. Annu Rev Biomed Eng 3: 169-194, 2001.
7. Chan E, Suneson A, Ulfendahl M. Acoustic trauma causes reversible stiffness changes in auditory sensory cell. Neuroscience 83: 961-968, 1998.
8. Cooper NP, Guinan JJ Jr. Separate mechanical processes underlie fast and slow effects of medial olivocochlear efferent activity. J Physiol 548: 307-312, 2003.
9. Dallos P. The active cochlea. J Neurosci 12: 4575-4585, 1992.
10. Dallos P. Overview: cochlear neurobiology. In: The Cochlea, edited by Dallos P, Popper AN, Fay RR. New York: Springer, 1996, p. 1-43.
11. Dallos P, Fakler B. Prestin, a new type of motor protein. Nat Rev Mol Cell Biol 3: 104-111, 2002.
12. Dallos P, He DZ, Lin X, Sziklai I, Mehta S, Evans BN. Acetylcholine, outer hair cell electromotility, and the cochlear amplifier. J Neurosci 17: 2212-2226, 1997.
13. Deo N, Grosh K. Simplified nonlinear outer hair cell models. J Acoust Soc Am 117: 2141-2146, 2005.
14. Dieler R, Shehata-Dieler WE, Brownell WE. Concomitant salicylate-induced alterations of outer hair cell subsurface cisternae and electromotility. J Neurocytol 20: 637-653, 1991.
15. Emadi G, Richter CP, Dallos P. Stiffness of the gerbil basilar membrane: radial and longitudinal variations. J Neurophysiol 91: 474-488, 2004.
16. Ernster JA, Meyers AD. Drug-induced alterations in cochlear blood flow as recorded by the laser Doppler flowmeter. Otolaryngol Head Neck Surg 95: 233-238, 1986.
17. Erostegui C, Norris CH, Bobbin RP. In vitro pharmacologic characterization of a cholinergic receptor on outer hair cells. Hear Res 74: 135-147, 1994.
18. Eybalin M. Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol Rev 73: 309-373, 1993.
19. Flock A, Flock B, Fridberger A, Scarfone E, Ulfendahl M. Supporting cells contribute to control of hearing sensitivity. J Neurosci 19: 4498-4507, 1999.
20. Frank G, Hemmert W, Gummer A. Limiting dynamics of high-frequency electromechanical transduction of outer hair cells. Proc Natl Acad Sci USA 96: 4420-4425, 1999.
21. Grosh K, Zheng J, Zou Y, de Boer E, Nuttall AL. High-frequency electromotile responses in the cochlea. J Acoust Soc Am 115: 2178-2184, 2004.
22. Gummer AW, Johnstone BM, Armstrong NJ. Direct measurement of basilar-membrane stiffness in the guinea pig. J Acoust Soc Am 70: 1298-1309, 1981.
23. Gutknecht J, Tosteson DC. Diffusion of weak acids across lipid bilayer membranes: effects of chemical reactions in the unstirred layers. Science 182: 1258-1261, 1973.
24. Hallworth R. Passive compliance and active force generation in the guinea pig outer hair cell. J Neurophysiol 74: 2319-2328, 1995.
25. Hallworth R. Modulation of outer hair cell compliance and force by agents that affect hearing. Hear Res 114: 204-212, 1997.
26. He DZ, Dallos P. Somatic stiffness of cochlear outer hair cells is voltage-dependent. Proc Natl Acad Sci USA 96: 8223-8228, 1999.
27. He DZ, Jia S, Dallos P. Prestin and the dynamic stiffness of cochlear outer hair cells. J Neurosci 23: 9089-9096, 2003.
28. Holley MC, Ashmore JF. A cytoskeletal spring in cochlear outer hair cells. Nature 335: 635-637, 1988.
29. Housley GD, Ashmore JF. Direct measurement of the action of acetylcholine on isolated outer hair cells of the guinea pig cochlea. Proc Biol Sci 244: 161-167, 1991.
30. Housley GD, Ashmore JF. Ionic currents of outer hair cells isolated from the guinea pig cochlea. J Physiol 448: 73-98, 1992.
31. Iwasa KH. Effect of membrane motor on the axial stiffness of the cochlear outer hair cell. J Acoust Soc Am 107: 2764-2766, 2000.
32. Iwasa KH, Adachi M. Force generation in the outer hair cell of the cochlea. Biophys J 73: 546-555, 1997.
33. Kakehata S, Santos-Sacchi J. Membrane tension directly shifts voltage dependence of outer hair cell motility and associated gating charge. Biophys J 68: 2190-2197, 1995.
34. Kakehata S, Santos-Sacchi J. Effects of salicylate and lanthanides on outer hair cell motility and associated gating charge. J Neurosci 16: 4881-4889, 1996.
35. Kalinec F, Zhang M, Urrutia R, Kalinec G. Rho GTPases mediate the regulation of cochlear outer hair cell motility by acetylcholine. J Biol Chem 275: 28000-28005, 2000.
36. Kennedy HJ, Crawford AC, Fettiplace R. Force generation by mammalian hair bundles supports a role in cochlear amplification. Nature 433: 880-883, 2005.
37. 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: 300-304, 2002.
38. Lue AJ, Brownell WE. Salicylate induced changes in outer hair cell lateral wall stiffness. Hear Res 135: 163-168, 1999.
39. Lue AJ, Zhao HB, Brownell WE. Chlorpromazine alters outer hair cell electromotility. Otolaryngol Head Neck Surg 125: 71-76, 2001.
40. McLaughlin S. Salicylates and phospholipid bilayer membranes. Nature 203: 234-236, 1973.
41. Mammano F, Ashmore JF. Reverse transduction measured in the isolated cochlea by laser Michelson interferometry. Nature 365: 838-841, 1993.
42. Morimoto N, Raphael RM, Nygren A, Brownell WE. Excess plasma membrane and effects of ionic amphipaths on mechanics of outer hair cell lateral wall. Am J Physiol Cell Physiol 282: 1076-1086, 2002.
43. Mountain DC, Hubbard AE. A piezoelectric model of outer hair cell function. J Acoust Soc Am 95: 350-354, 1994.
44. Murdock DR, Ermilov S, Spector AA, Popel AS, Brownell WE, Anvari B. Effects of chlorpromazine on mechanical properties of the outer hair cell plasma membrane. Biophys J 89: 4090-4095, 2005.
45. Murugasu E, Russell IJ. Salicylate ototoxicity: the effects on basilar membrane displacement, cochlear microphonics, and neural responses in the basal turn of the guinea pig cochlea. Auditory Neurosci 1: 139-150, 1995.
46. Naidu RC, Mountain DC. Measurements of the stiffness map challenge a basic tenet of cochlear theories. Hear Res 124: 124-131, 1998.
47. Nuttall AL, Dolan DF, Avinash G. Laser doppler velocimetry o basilar membrane vibration. Hear Res 51: 203-214, 1991.
48. Nuttall AL, Ren T. Electromotile hearing: evidence from basilar membrane motion and otoacoustic emissions. Hear Res 92: 170-177, 1995.
49. Oghalai JS. Chlorpromazine inhibits cochlear function in guinea pigs. Hear Res 198: 59-68, 2004.
50. Oghalai JS, Choi C-H, Spector AA. Modulation of cochlear mechanics: model predictions and experimental findings of the effect of changing perilymph osmolarity. In: Auditory Mechanisms: Processes and Models, edited by Nuttall AL, Ren T, Gillespie P, Grosh K, de Boer E. New Jersey, London, Singapore, Hong Kong: World Scientific, 2006, p. 41-48.
51. Oghalai JS, Zhao HB, Kutz JW, Brownell WE. Voltage- and tension-dependent lipid mobility in the outer hair cell plasma membrane. Science 287: 658-661, 2000.
52. Oliver D, He DZ, Klocker N, Ludwig J, Schulte U, Waldegger S, Ruppersberg JP, Dallos P, Fakler B. Intracellular anions as the voltage sensor of prestin, the outer hair cell motor protein. Science 292: 2340-2343, 2001.
53. Olson ES, Mountain DC. Mapping the cochlear partition's stiffness to its cellular architecture. J Acoust Soc Am 95: 395-400, 1994.
54. Park T, Bae S, Choi S, Kang B, Kim K. Inhibition of nicotinic acetylcholine receptors and calcium channels by clozapine in bovine adrenal chromaffin cells. Biochem Pharmacol 61: 1011-1019, 2001.
55. Parthasarathi AA, Grosh K, Zheng J, Nuttall AL. Effect of current stimulus on in vivo cochlear mechanics. J Acoust Soc Am 113: 442-52, 2003.
56. Robles L, Ruggero MA. Mechanics of the mammalian cochlea. Physiol Rev 81: 1305-1352, 2001.
57. Russell I, Schauz C. Salicylate ototoxicity: effects on the stiffness and electromotility of outer hair cells isolated from the guinea pig cochlea. Audit Neurosci 1: 309-319, 1995.
58. Santos-Sacchi J. Reversible inhibition of voltage-dependent outer hair cell motility and capacitance. J Neurosci 1110: 3096-110, 1991.
59. Santos-Sacchi J, W Shen, Zheng J, Dallos P. Effects of membrane potential and tension on prestin, the outer hair cell lateral membrane motor protein. J Physiol 531: 661-666, 2001.
60. Scherer MP, Gummer AW. Vibration pattern of the organ of Corti up to 50 kHz: evidence for resonant electromechanical force. Proc Natl Acad Sci USA 101: 17652-17657, 2004.
61. Sheetz MP, Singer SJ. Biological membranes as bilayer couples: a molecular mechanism of drug-erythrocyte interactions. Proc Natl Acad Sci USA 71: 4457-4461, 1974.
62. Shehata WE, Brownell WE, Dieler R. Effects of salicylate on shape, electromotility and membrane characteristics of isolated outer hair cells from guinea pig cochlea. Acta Otolaryngol 111: 707-718, 1991.
63. Slepecky NB. Structure of the mammalian cochlea. In: The Cochlea, edited by Dallos P, Popper AN, and Fay RR. New York: Springer, 1996, p. 44-129.
64. Spector AA, Brownell WE, Polet AS. Effect of outer hair cell piezoelectricity on high-frequency receptor potentials. J Acoust Soc Am 113: 453-461, 2003.
65. Ulfendahl M, Chan E, McConnaughey WB, Prost-Domasky S, Elson EL. Axial and transverse stiffness measures of cochlear outer hair cells suggest a common mechanical basis. Pfluegers 436: 9-15, 1998.
66. Weitzel EK, Tasker R, Brownell WE. Outer hair cell piezoelectricity: frequency response enhancement and resonance behavior. J Acoust Soc Am 114: 1462-1466, 2003.
67. Zeng C, Wang D, Yang Z, Wang Z, Asico LD, Christopher S, Eisner GM, Welch WJ, Felder RA, Jose PA. Dopamine D1 receptor augmentation of D3 receptor action in rat aortic or mesenteric vascular smooth muscles. Hypertension 43: 673-679, 2004.
68. Zenner HP, Gitter AH, Rudert M, Ernst A. Stiffness, compliance, elasticity and force generation of outer hair cells. Acta Otolaryngol 112: 248-253, 1992.
69. Zhang PC, Keleshian AM, Sachs F. Voltage-induced membrane movement. Nature 413: 428-432, 2001.
70. Zheng J, Shen W, He DZ, Long KB, Madison LD, Dallos P. Prestin is the motor protein of cochlear outer hair cells Nature 405: 149-55, 2000.