Mechanical amplification by hair cells in the semicircular canals

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 8, 2010, Pages 3864-3869

  Rabbitt, Richard D ^a,b   Boyle, Richard ^c   Highstein, Stephen M ^b  

^a UNIVERSITY OF UTAH   (United States)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c NASA AMES RESEARCH CENTER   (United States)

Author keywords

Active process; Auditory; Hair bundle; Inner ear; Motor

Indexed keywords

ARTICLE; BRAIN REGION; CELL STIMULATION; CONTROLLED STUDY; HAIR CELL; IMPEDANCE; IN VIVO STUDY; MECHANICAL STIMULATION; MECHANOTRANSDUCTION; NONHUMAN; PRIORITY JOURNAL; SEMICIRCULAR CANAL; SYNAPTIC TRANSMISSION; TELEOST; VELOCITY;

ANIMALS; BATRACHOIDIFORMES; HAIR CELLS, AMPULLA; MECHANOTRANSDUCTION, CELLULAR; MOTION; SEMICIRCULAR CANALS;

OPSANUS TAU; TELEOSTEI;

EID: 77649255626     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0906765107     Document Type: Article

References (66)

1. Stensiö E (1927) The Downtonian and Devonian vertebrates of Spitsbergen. Part I, Family Cephalaspidae. Skr. Svalbard Nordishavet 12:1-391.
2. Hudspeth AJ (2008) Making an effort to listen: Mechanical amplification in the ear. Neuron 59:530-545.
3. Brownell WE, Bader CRB, Bertrand D, de Ribaupierre Y (1985) Evoked mechanical responses of isolated cochlear outer hair cells. Science 227:194-196.
4. Zheng J, et al. (2000) Prestin is the motor protein of cochlear outer hair cells. Nature 405:149-155.
5. Liberman MC, et al. (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419:300-304.
6. Liberman MC (1980) Efferent synapses in the inner hair cell area of the cat cochlea: An electron microscopic study of serial sections. Hear Res 3:189-204.
7. Murugasu E, Russell IJ (1996) The effect of efferent stimulation on basilar membrane displacement in the basal turn of the guinea pig cochlea. J Neurosci 16:325-332.
8. Russell IJ, Murugasu E (1997) Medial efferent inhibition suppresses basilar membrane responses to near characteristic frequency tones of moderate to high intensities. J Acoust Soc Am 102:1734-1738.
9. Dallos P, et al. (1997) Acetylcholine, outer hair cell electromotility, and the cochlear amplifier. J Neurosci 17:2212-2226.
10. Fuchs PA, Murrow BW (1992) Cholinergic inhibition of short (outer) hair cells of the chick's cochlea. J Neurosci 12:800-809.
11. Adler HJ, et al. (2003) Expression of prestin, a membrane motor protein, in the mammalian auditory and vestibular periphery. Hear Res 184:27-40.
12. Manley GA (2000) Cochlear mechanisms from a phylogenetic viewpoint. Proc Natl Acad Sci USA 97:11736-11743.
13. Manley GA, Köppl C (2008) What have lizard ears taught us about auditory physiology? Hear Res 238:3-11.
14. Manley GA (2006) Spontaneous otoacoustic emissions from free-standing stereovillar bundles of ten species of lizard with small papillae. Hear Res 212:33-47.
15. Tanaka K, Smith CA (1978) Structure of the chicken's inner ear: SEM and TEM study. Am J Anat 153:251-271.
16. 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.
17. He DZ, et al. (2003) Chick hair cells do not exhibit voltage-dependent somatic motility. J Physiol 546:511-520.
18. Fischer FP (1994) General pattern and morphological specializations of the avian cochlea. Scanning Microsc 8(2):351-363; discussion; 363-354.
19. Fettiplace R, Fuchs PA (1999) Mechanisms of hair cell tuning. Annu Rev Physiol 61:809-834.
20. Bozovic D, Hudspeth AJ (2003) Hair-bundle movements elicited by transepithelial electrical stimulation of hair cells in the sacculus of the bullfrog. Proc Natl Acad Sci USA 100:958-963.
21. Rüsch A, Thurm U (1990) Spontaneous and electrically induced movements of ampullary kinocilia and stereovilli. Hear Res 48:247-263.
22. 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.
23. Martin P, Bozovic D, Choe Y, Hudspeth AJ (2003) Spontaneous oscillation by hair bundles of the bullfrog's sacculus. J Neurosci 23:4533-4548.
24. Le Goff L, Bozovic D, Hudspeth AJ (2005) Adaptive shift in the domain of negative stiffness during spontaneous oscillation by hair bundles from the internal ear. Proc Natl Acad Sci USA 102:16996-17001.
25. Martin P, Hudspeth AJ (1999) Active hair-bundle movements can amplify a hair cell's response to oscillatory mechanical stimuli. Proc Natl Acad Sci USA 96:14306-14311.
26. Eguíluz VM, Ospeck M, Choe Y, Hudspeth AJ, Magnasco MO (2000) Essential nonlinearities in hearing. Phys Rev Lett 84:5232-5235.
27. Holt JC, Lysakowski A, Goldberg JM (2006) Mechanisms of efferent-mediated responses in the turtle posterior crista. J Neurosci 26:13180-13193.
28. Goldberg JM, Fernández C (1980) Efferent vestibular system in the squirrel monkey: Anatomical location and influence on afferent activity. J Neurophysiol 43:986-1025.
29. Boyle R, Highstein SM (1990) Resting discharge and response dynamics of horizontal semicircular canal afferents of the toadfish, Opsanus tau. J Neurosci 10:1557-1569.
30. Boyle R, Rabbitt RD, Highstein SM (2009) Efferent control of hair cell and afferent responses in the semicircular canals. J Neurophysiol 102:1513-1525.
31. Rabbitt RD, Boyle R, Highstein SM (1995) Mechanical indentation of the vestibular labyrinth and its relationship to head rotation in the toadfish, Opsanus tau. J Neurophysiol 73:2237-2260.
32. Boyle R, Highstein SM (1990) Efferent vestibular system in the toadfish: Action upon horizontal semicircular canal afferents. J Neurosci 10:1570-1582.
33. Rabbitt RD, et al. (2009) Dynamic displacement of normal and detached semicircular canal cupula. J Assoc Res Otolaryngol 10:497-509.
34. Hillman DE, McLaren JW (1979) Displacement configuration of semicircular canal cupulae. Neuroscience 4:1989-2000.
35. Rabbitt RD, Boyle R, Holstein GR, Highstein SM (2005) Hair-cell versus afferent adaptation in the semicircular canals. J Neurophysiol 93:424-436.
36. Ruggero MA, Rich NC, Recio A, Narayan SS, Robles L (1997) Basilar-membrane responses to tones at the base of the chinchilla cochlea. J Acoust Soc Am 101:2151-2163.
37. Kunuth KH (1998) Mathematics of distortion product otoacoustic emission generation: A tutorial. Otoacoustic Emissions. Basic Science and Clinical Applications, ed Berlin CI (Singular Publishing Group, San Diego) pp 149-159.
38. Long GR, Tubis A, Jones KL (1991) Modeling synchronization and suppression of spontaneous otoacoustic emissions using Van der Pol oscillators: Effects of aspirin administration. J Acoust Soc Am 89:1201-1212.
39. Sadeghi SG, Goldberg JM, Minor LB, Cullen KE (2009) Efferent-mediated responses in vestibular nerve afferents of the alert macaque. J Neurophysiol 101:988-1001.
40. Rabbitt RD, Damiano ER, Grant JW (2004) Biomechanics of the Semicircular Canals and Otolith Organs. The Vestibular System, Springer Handbook of Auditory Research, eds Highstein SM, Popper A, Fay R , Spirnger, New York), pp 153-201.
41. Ghanem TA, Rabbitt RD, Tresco PA (1998) Three-dimensional reconstruction of the membranous vestibular labyrinth in the toadfish, Opsanus tau. Hear Res 124:27-43.
42. Robles L, Ruggero MA (2001) Mechanics of the mammalian cochlea. Physiol Rev 81:1305-1352.
43. Rhode WS (1971) Observations of the vibration of the basilar membrane in squirrel monkeys using the Mössbauer technique. J Acoust Soc Am 49:(suppl 2)1218.
44. Brown MC, Nuttall AL, Masta RI (1983) Intracellular recordings from cochlear inner hair cells: Effects of stimulation of the crossed olivocochlear efferents. Science 222:69-72.
45. Manley GA (2001) Evidence for an active process and a cochlear amplifier in nonmammals. J Neurophysiol 86:541-549.
46. Howard J, Hudspeth AJ (1987) Mechanical relaxation of the hair bundle mediates adaptation in mechanoelectrical transduction by the bullfrog's saccular hair cell. Proc Natl Acad Sci USA 84:3064-3068.
47. Wu YC, Ricci AJ, Fettiplace R (1999) Two components of transducer adaptation in auditory hair cells. J Neurophysiol 82:2171-2181.
48. Kennedy HJ, Evans MG, Crawford AC, Fettiplace R (2003) Fast adaptation of mechanoelectrical transducer channels in mammalian cochlear hair cells. Nat Neurosci 6:832-836.
49. Vollrath MA,, Eatock RA (2003) Time course and extent of mechanotransducer adaptation in mouse utricular hair cells: Comparison with frog saccular hair cells. J Neurophysiol 90:2676-89.
50. Fettiplace R, Ricci AJ, Hackney CM (2001) Clues to the cochlear amplifier from the turtle ear. Trends Neurosci 24:169-175.
51. Flock A, Russell I (1976) Inhibition by efferent nerve fibres: Action on hair cells and afferent synaptic transmission in the lateral line canal organ of the burbot Lota lota. J Physiol 257:45-62.
52. Assad JA, Corey DP (1992) An active motor model for adaptation by vertebrate hair cells. J Neurosci 12 (9):3291-3309.
53. Holt JR, et al. (2002) A chemical-genetic strategy implicates myosin-1c in adaptation by hair cells. Cell 108:371-381.
54. Howard J, Hudspeth AJ (1988) Compliance of the hair bundle associated with gating of mechanoelectrical transduction channels in the bullfrog's saccular hair cell. Neuron 1:189-199.
55. Crawford AC, Evans MG, Fettiplace R (1991) The actions of calcium on the mechanoelectrical transducer current of turtle hair cells. J Physiol 434:369-398.
56. 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 USA 95:15321-15326.
57. Beurg M, Nam JH, Crawford A, Fettiplace R (2008) The actions of calcium on hair bundle mechanics in mammalian cochlear hair cells. Biophys J 94:2639-2653.
58. Assad JA, Shepherd GM, Corey DP (1991) Tip-link integrity and mechanical transduction in vertebrate hair cells. Neuron 7:985-994.
59. Ricci AJ, Crawford AC, Fettiplace R (2000) Active hair bundle motion linked to fast transducer adaptation in auditory hair cells. J Neurosci 20:7131-7142.
60. Breneman KD, Brownell WE, Rabbitt RD (2009) Hair cell bundles: Flexoelectric motors of the inner ear. PLoS One 4:e5201.
61. Cheung EL, Corey DP (2006) Ca2+ changes the force sensitivity of the hair-cell transduction channel. Biophys J 90:124-139.
62. Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I. Resting discharge and response to constant angular accelerations. J Neurophysiol 34:635-660.
63. Ifediba MA, Rajguru SM, Hullar TE, Rabbitt RD (2007) The role of 3-canal biomechanics in angular motion transduction by the human vestibular labyrinth. Ann Biomed Eng 35(7):1247-1263.
64. Dickman JD, Correia MJ (1989) Responses of pigeon horizontal semicircular canal afferent fibers. I. Step, trapezoid, and low-frequency sinusoid mechanical and rotational stimulation. J Neurophysiol 62:1090-1101.
65. Rajguru SM, Rabbitt RD (2007) Afferent responses during experimentally induced semicircular canalithiasis. J Neurophysiol 97:2355-2363.
66. Thévenaz P, Ruttimann UE, Unser M (1998) A pyramid approach to subpixel registration based on intensity. IEEE Trans Image Process 7:27-41.