Development of the organ of corti in horseshoe bats: Scanning and transmission electron microscopy

Journal of Comparative Neurology

Volumn 377, Issue 4, 1997, Pages 520-534

  Vater, Marianne ^a   Lenoir, Marc ^b   Pujol, Remy ^b  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b Hopital Saint Charles   (France)

Author keywords

audition; cochlea; postnatal ontogeny

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BAT; COCHLEA; COCHLEA DUCT; CORTI ORGAN; EARDRUM; FETUS; HAIR CELL; HEARING; MAGNOCELLULAR NUCLEUS; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; STEREOCILIUM; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; ANIMALS, NEWBORN; AUDITORY PATHWAYS; CHIROPTERA; HAIR CELLS; MICROSCOPY, ELECTRON; MICROSCOPY, ELECTRON, SCANNING; ORGAN OF CORTI; RECEPTORS, SENSORY; TECTORIAL MEMBRANE; ULTRASONICS;

EID: 0031036665     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19970127)377:4<520::AID-CNE4>3.0.CO;2-4     Document Type: Article

References (85)

1. Anniko, M. (1983) Postnatal maturation of cochlear sensory hairs in the mouse. Anat. Embryol. 166:355-368.
2. Arjmand, E., D. Harris, and P. Dallos (1988) Developmental changes in frequency mapping of the gerbil cochlea: Comparison of two cochlear locations. Hear. Res. 32:93-96.
3. Bannister, L.H., H.C. Dodson, A.R. Astbury, and E.E. Douek (1988) The cortical lattice: A highly ordered system of subsurface filaments in guinea pig cochlear outer hair cells. In W. Hamman and A. Iggo (eds): Biomedical Division, Vol. 74. New York: Elsevier Science Publishers, pp. 213-219.
4. Bishop, A.L., and M.M. Henson (1988) The efferent auditory system in Doppler-shift compensating bats. In P.E. Nachtigall and P.W.B. Moore (eds): Animal Sonar. New York: Plenum Press, pp. 307-311.
5. Bosher, S.K., and R.L. Warren (1971) Study of the electrochemistry and osmotic relationship of the cochlear fluids in the neonatal rat at the time of development of the endocochlear potential. J. Physiol. 212:739-761.
6. Brownell, W.E., C.R. Bader, D. Bertrand, and Y. de Ribeaupierre (1985) Evoked mechanical respones of isolated outer hair cells. Science 227:194-196.
7. Bruns, V. (1976a) Peripheral auditory tuning for fine frequency analysis by the CF-FM bat, Rhinolophus ferrumeqinnum. I. Mechanical specializations of the cochlea. J. Comp. Physiol. 106:77-86.
8. Bruns, V. (1976b) Peripheral auditory tuning for fine frequency analysis by the CF-FM bat, Rhinolophus ferrumequinum. II. Frequency mapping of the cochlea. J. Comp. Physiol. 106:87-97.
9. Bruns, V., and E. Schmieszek (1980) Cochlear innervation in the greater horseshoe bat: Demonstration of an acoustic fovea. Hear. Res. 3:27-43.
10. Burda, H., and M. Branis (1988) Postnatal development of the organ of Corti in the wild house mouse, laboratory mouse, and their hybrid. Hear. Res. 36:97-106.
11. Crowley, D.E., and M.C Hepp-Reymond (1966) Development of cochlear function in the ear of the infant cat. J. Comp. Physiol. Psychol. 62:427-432.
12. Dallos, P. (1992) The active cochlea. J. Neurosci. 12:4575-4585.
13. Davis, H. (1983) An active process in cochlear mechanics. Hear. Res. 9:79-90.
14. Echteler, S. M., E. Armand, and P. Dallos (1989) Developmental alterations in the frequency map of the mammalian cochlea. Nature 341:147-149.
15. Furness, D.N., and C.M. Hackney (1990) Comparative ultrastructure of subsurface cisternae in inner and outer hair cells of the guinea pig cochlea. Eur. Arch. Otorhinolaryngol. 247:12-15.
16. Gabrion, J., C. Legrand, B. Mercier, M.-C. Harricane, and A. Uziel (1984) Microtubules in the cochlea of the hypothyroid developing rat. Hear. Res. 13:203-214.
17. Harris, D.M., and P. Dallos (1984) Ontogenetic changes in frequency mapping of mammalian ear. Science 225:741-743.
18. He, D.Z.Z., B.N. Evans, and P. Dallos (1994) First appearance and development of electromotility in neonatal gerbil outer hair cells. Hear. Res. 78:77-90.
19. Henson, M.M., and R. Rübsamen (1996) The postnatal development of tension fibroblasts in the spiral ligament of the horseshoe bat, Rhinolophus rouxi. Auditory Neurosci. 2:3-13.
20. Holley, M. (1991) High frequency force generation in outer hair cells from the mammalian ear. BioEssays 13:115-120.
21. Holley, M.C., and J.F. Ashmore (1988) A cytoskeletal spring in cochlear outer hair cells. Nature 335:635-637.
22. Holley, M., and J.F. Ashmore (1990) Spectrin, actin and the structure of the cortical lattice in mammalian cochlear outer hair cells. J. Cell Science 96:283-291.
23. Kaltenbach, J.A., and P.R. Falzarano (1994) Postnatal development of the hamster cochlea. I. Growth of hair cells and the organ of Corti. J. Comp. Neurol. 340:87-97.
24. Khanna, S.M., and D.G.B. Leonard (1986) Relationship between basilar membrane tuning and hair cell condition. Hear. Res. 23:55-70.
25. Kikuchi, K., and D. Hilding (1965) The development of the organ of Corti in the mouse. Acta Otolaryngol. 60:207-222
26. Kraus, H.-J., and K. Aulbach-Kraus (1981) Morphological changes in the cochlea of the mouse after the onset of hearing. Hear. Res. 4:89-102.
27. Kuhn, B., and M. Vater (1995) The arrangements of F-actin, tubulin and fodrin in the organ of Corti of the horseshoe bat (Rhinolophus rouxi) and the gerbil (Meriones unguiculatus). Hear. Res. 84:139-156.
28. Lavigne-Rebillard, M., and R. Pujol (1988) Hair cell innervation in the fetal human cochlea. Acta Otolaryngol. 105:398-402.
29. Lavigne-Rebillard, M., and R. Pujol (1990) Auditory hair cells in human fetuses: Synaptogenesis and ciliogenesis. J. Electr. Mikrosc. Technol. 15:115-122.
30. Lenoir, M., A. Shnerson, and R. Pujol (1980) Cochlear receptor development in the rat with emphasis on synaptogenesis. Anat. Embryol. 160:253-262.
31. Lenoir, M., J.-L. Puel, and R. Pujol (1987) Stereocilia and tectorial membrane development in the rat cochlea: A SEM study. Anat. Embryol. 175:477-487
32. Liberman, M.C., and L.W. Dodds (1984) Single neuron labelling and chronic cochlear pathology. III. Stereocilia damage and alterations of threshold tuning curves. Hear. Res. 16:55-74.
33. Lim, D. (1987) Development of the tectorial membrane. Hear. Res. 28:9-21.
34. Lindeman, H.H., H.W. Ades, G. Bredberg, and H. Engström (1971) The sensory hairs and the tectorial membrane in the developing cat's organ of Corti. A scanning electron microscopic study. Acta Otolaryngol. 72:229-242.
35. McGuirt, J.P., R.A. Schmiedt, and B.A. Schulte (1995) Development of cochlear potentials in the neonatal gerbil. Hear. Res. 84:52-60.
36. Mikaelian, D., and R.J. Ruben (1964) Development of hearing in the normal CBA-J mouse. Acta Otolaryngol. 59:451-461.
37. Mills, D.M., S.J. Norton, and E.W. Rubel (1994) Development of active and passive mechanics in the mammalian cochlea. Auditory Neurosci. 1: 77-99.
38. Müller, M. (1991) Developmental changes of frequency representation in the rat cochlea. Hear. Res. 56:1-7.
39. Neely, S.T., and D.O. Kim (1983) An active cochlear model showing sharp tuning and high sensitivity. Hear. Res. 9:123-130.
40. Neuweiler, G. (1990) Auditory adaptations for prey capture in echolocating bats. Physiol. Rev. 70:615-641.
41. Norton, S.J., J.Y. Bargones, and E.W. Rubel (1991) Development of otoacoustic emissions in gerbil: Evidence for micromechanical changes underlying development of the place cod. Hear. Res. 51:73-92.
42. Pirvola, U., E. Lehtonen, and J. Ylikovski (1991) Spatiotemporal development of cochlear innervation and hair cell differentiation in the rat. Hear. Res. 52:345-355.
43. Puel, J.L., and A. Uziel (1987) Correlative development of cochlear action potential sensitivity, latency, and frequency selectivity. Dev. Brain Res. 37:179-188.
44. Puel, J.-L., M. Lenoir, and A. Uziel (1987) Dose-dependent changes in the rat cochlea following aminoglycoside intoxication. I. Physiological study. Hear. Res. 26:191-207
45. Pujol, R., and R. Marty (1970) Postnatal maturation in the cochlea of the cat. J. Comp. Neurol. 139:115-126.
46. Pujol, R., and D. Hilding (1973) Anatomy and physiology of the onset of auditory function. Acta Otolaryngol. 76:1-10.
47. Pujol, R., and A. Uziel (1988) Auditory development: Peripheral aspects. In E. Meisami, and P.S. Timiras (eds): Handbook of Human Growth and Developmental Biology, Vol. I. Part B. Boca Raton, Florida: CRC Press, Inc., pp. 109-130.
48. Pujol, R., E. Carlier, and C. Devigne (1978) Different patterns of cochlear innervation during development of the kitten. J. Comp. Neurol. 177:529-536.
49. Pujol, M., E. Carlier, and M. Lenoir (1980) Ontogenetic approach to inner and outer hair cell functions. Hear. Res. 2:423-430.
50. Pujol, R., and M. Lavigne-Rebillard (1985) Early stages of innervation and sensory cell differentiation in the human fetal organ of Corti. Acta Otolaryngol. Suppl. 423:43-50.
51. Pujol, R., G. Zajic, D. Dulon, Y. Raphael, R.A. Altschuler, and J. Schacht (1991) First appearance and development of motile properties in outer hair cells isolated from guinea-pig cochlea. Hear. Res. 57:129-141.
52. Pujol, R., M. Lavigne-Rebillard, and M. Lenoir (1995) Development of sensory and neural structures in the mammalian cochlea. In E.W. Rubel, A.N. Popper, and R.R. Fay (eds): Development of the Auditory System: Handbook of Auditory Research, Vol. 5. New York: Springer-Verlag, in press.
53. Raphael, Y., M. Ohmura, N. Kanoh, N., N. Yagi, and K. Makimoto (1983) Prenatal maturation of endocochlear potential and electrolyte composition of inner ear fluids in guinea pigs. Arch. Otorhinolaryngol. 237:147-152.
54. Romand, R. (1983) Development of the cochlea. In R. Roman (ed): Development of Auditory and Vestibular Systems. New York, London: Academic Press, Inc., pp. 47-88.
55. Romand, R. (1987) Tonotopic evolution during development. Hear. Res. 28:117-123.
56. Romand, R., G. Despres, and N. Giry (1987) Factors affecting the onset of inner function. Hear. Res. 28:1-7.
57. Romand, R., A.E. Zine, and A. Hafidi (1993) Ontogenis of F-Actin in hair cells. Cell Motil. Cytosk. 25:213-222.
58. Roth, B., and V. Bruns (1992a) Postnatal development of the rat organ of Corti. I. General morphology, basilar membrane, tectorial membrane and border cells. Anat. Embryol. 185:559-569.
59. Roth, B., and V. Bruns (1992b) Postnatal development of the rat organ of Corti. II. Hair cell receptors and their supporting elements. Anat. Embryol. 185:571-581.
60. Rubel, E.W., and B.M. Ryals (1983) Development of the place principle: Acoustic trauma. Science 219:512-513.
61. Rubel, E.W., W.R. Lippe, and B.M. Ryals (1984) Development of the place principle. Ann. Otol. Rhinol. Laryngol. 93:609-615.
62. Rübsamen, R. (1987) Ontogenis of the echolocation system in the rufous horseshoe bat, Rhinolophus rouxi. (Audition and vocalization in early postnatal development). J. Comp. Physiol. A 161:899-913.
63. Rübsamen, R. (1992) Postnatal development of central auditory frequency maps. J. Comp. Physiol. A 170:129-143.
64. Rübsamen, R., and M. Schäfer (1990) Ontogenis of auditory fovea representation in the inferior colliculus of the Sri lankan rufous horseshoe bat, Rhinolophus rouxi. J. Comp. Physiol. A 167:757-769.
65. Ruggero, M.A., and N.C. Rich (1991) Furosemide alters organ of Corti mechanics: evidence for feedback of outer hair cells upon the basilar membrane. J. Neurosci. 11:1057-1067.
66. Shnerson, A., and R. Pujol (1983) Development: Anatomy, electrophysiology and behavior. In J.W. Willott (ed): The Auditory Psychobiology of the Mouse. Springfield: Charles C. Thomas, pp. 395-423.
67. Shnerson, A., C. Devigne, and R. Pujol (1982) Age related changes in the C57BL/6J mouse cochlea. II. Ultrastructural findings. Dev. Brain Res. 2:77-88.
68. Sobin, A., and M. Anniko (1984) Early development of cochlear hair cell stereocilia surface morphology. Arch. Otorhinolaryngol. 241:55-64.
69. Spoendlin, H.H., and J.P. Brun (1974) The block surface technique for evaluation of cochlear pathology. Arch. Otorhinolaryngol. 208:137-145.
70. Vater, M. (1988) Light microscopic observations on cochlear development in horseshoe bats. In P. E. Nachtigall and P.W.B. Moore (eds): Animal Sonar Systems. New York, London: Plenum Press, pp. 341-345.
71. Vater, M. (1988) Cochlear anatomy and physiology in bats. In P.E. Nachtigall and P.W.B. Moore (eds): Animal Sonar. New York, London: Plenum Press, pp. 225-243.
72. Vater, M., and R. Rübsamen (1988) Postnatal development of the cochlea in horseshoe bats. In J.P. Wilson and D.T. Kemp (eds): Cochlear mechanisms. Structure, function and models. New York and London: Plenum Press, pp. 217-225.
73. Vater M., and R. Rübsamen (1992) Ontogeny of frequency maps in the peripheral auditory system of horseshoe bats. Proc. Third. Int. Congress Neuroethology, Montreal, pp. 31-32.
74. Vater, M., A.S. Feng, and M. Betz (1985) An HRP-study of the frequency-place map of the horseshoe bat cochlea: Morphological correlates of the sharp tuning to a narrow frequency band. J. Comp. Physiol. A 157:671-686.
75. Vater, M., and M. Lenoir (1992) Ultrastructure of the horseshoe bat's organ of Corti. I. Scanning electron microscopy. J. Comp. Neurol. 318:367-379.
76. Vater, M., M. Lenoir, and R. Pujol (1992) Ultrastructure of the horseshoe bat's organ of Corti. II. transmission electron microscopy. J. Comp. Neurol. 318:380-391.
77. Wada, T. (1923) Anatomical and physiological studies on the growth of the inner ear of the albino rat. Am. Anat. Memoirs 10:1-174.
78. Walsh, E.J., and J. McGee (1986) The development of function in the auditory periphery. In R.A. Altschuler, D.W. Hoffman, and R.P. Bobbin (eds): Neurobiology of Hearing: The Cochlea. New York: Raven Press, pp. 247-269.
79. Weaver, S.P., and L. Schweitzer (1994) Development of gerbil outer hair cells after the onset of cochlear function: An ultrastructural study. Hear. Res. 72:44-52.
80. Weaver, S.P., J. Hoffpauir, and L. Schweitzer (1994) Distribution of actin in developing outer hair cells in the gerbil. Hear. Res. 72:181-188.
81. Woolf, N.K., and A.F. Ryan (1984) The development of auditory function in the cochlea of the mongolian gerbil. Hear. Res. 13:277-283.
82. Woolf, N.K., A.F. Ryan, and J.P. Harris (1986) Development of mammalian endocochlear potential: Normal ontogeny and effects of anoxia. Am. J. Physiol. 250:R493-R498.
83. Woolf, N.K., and A.F. Ryan (1988) Contributions of the middle ear to the development of function in the cochlea of the Mongolian gerbil. Hear. Res. 13:131-142.
84. Ylikoski, J., U. Pirvola, O. Narvanen, and I. Virtanen (1990) Non-erythroid spectrin (fodrin) is a prominent component of cochlear hair cells. Hear. Res. 43:199-204.
85. Zenner, H.P., W. Arnold, and A.H. Gitter (1988) Outer hair cells as fast and slow cochlear amplifiers with a bidirectional transduction cycle. Acta Otolaryngol. 105:457-462.