Postnatal development of efferent synapses in the rat cochlea

Journal of Comparative Neurology

Volumn 423, Issue 3, 2000, Pages 532-548

  Bruce, Laura L ^a   Christensen, Maria A ^a   Warr, W Bruce ^a,b  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BOYS TOWN NATIONAL RESEARCH HOSPITAL   (United States)

Author keywords

Cochlear development; Deiters' cell; DiI; Efferent development; Hair cell; Synaptogenesis

Indexed keywords

ANIMAL TISSUE; ARTICLE; CELL SUBPOPULATION; CELL ULTRASTRUCTURE; COCHLEA; CONTROLLED STUDY; EFFERENT NERVE; HAIR CELL; MAGNOCELLULAR NUCLEUS; NERVE FIBER GROWTH; NEUROANATOMY; NEWBORN; NONHUMAN; ONTOGENY; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RAT; SYNAPSE VESICLE; SYNAPTOGENESIS;

ANIMALS; AUDITORY PATHWAYS; CARBOCYANINES; FLUORESCENT DYES; HAIR CELLS; MICROSCOPY, ELECTRON; NEURONS, EFFERENT; RATS; RATS, LONG-EVANS; SYNAPSES;

EID: 0034738705     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/1096-9861(20000731)423:3<532::AID-CNE14>3.0.CO;2-T     Document Type: Article

References (77)

1. Bianchi LM, Liu H, Krug EL, Capehart AA. 1999. Selective and transient expression of a native chondroitin sulfate epitope in Deiters' cells, pillar cells, and the developing tectorial membrane. Anat Rec 256:64-71.
2. Bohnke F, Arnold W. 1998. Nonlinear mechanics of the organ of Corti caused by Deiters cells. IEEE Trans Biomed Eng 45:1227-1233.
3. Bruce LL, Christensen MA, Warr WB. 1995. Synaptogenesis in the rat cochlea at birth. Assoc Res Otolaryngol Abstr 354.
4. Bruce LL, Christensen MA, Warr WB. 1996. Postnatal synaptogenesis of efferents with hair cells and Deiters' cells in the rat cochlea. Assoc Res Otolaryngol Abstr 439.
5. Bruce LL, Christensen MA, Fritzsch B. 1997a. Electron microscopic differentiation of directly and transneuronally diffused DiI and applications for studies of synaptogenesis. J Neurosci Methods 73:107-112.
6. Bruce LL, Kingsley J, Nichols DH, Fritzsch B. 1997b. The development of vestibulocochlear efferents and cochlear afferents in mice. Int J Dev Neurosci 15:671-692.
7. Burda H. 1985. Qualitative assessment of postnatal maturation of the organ of Corti in two rat strains. Hearing Res 17:201-208.
8. Burda H, Ballast L, Bruns V. 1988. Cochlea in old world mice and rats (Muridae). J Morphol 198:169-285.
9. Cole KS, Robertson D. 1992. Early efferent innervation of the developing rat cochlea studied with a carbocyanine dye. Brain Res 575:223-230.
10. Engstrom H, Ades HW, Andersson A. 1966. Structural pattern of the organ of Corti. Baltimore: Williams and Wilkins.
11. Ernfors P, van de Water T, Loring J, Jaenisch R. 1995. Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 14:1153-1164.
12. Fechner FP, Burgess BJ, Adams JC, Liberman MC, Nadol JB Jr. 1998. Dense innervation of Deiters' and Hensen's cells persists after chronic deefferentation of guinea pig cochleas. J Comp Neurol 400:299-309.
13. Fitzsimonds RM, Poo MM. 1998. Retrograde signaling in the development and modification of synapses. Physiol Rev 78:143-170.
14. Flock A, Flock B, Fridberger A, Scarfone E, Ulfendahl M. 1999. Supporting cells contribute to control of hearing sensitivity. J Neurosci 19:4498-4507.
15. Fritzsch B, Nichols DH. 1993. DiI reveals a prenatal arrival of efferents at the differentiating otocyst of mice. Hearing Res 65:51-60.
16. Fritzsch B, Wilm C. 1990. Dextran amines in neuronal tracing. Trends Neurosci 13:14.
17. Fritzsch B, Silos-Santiago I, Smeyne R, Fagan AM, Barbacid M. 1995. Reduction and loss of inner ear innervation in trkB and trkC receptor knockout mice: a whole mount DiI and scanning electron microscopic analysis. Aud Neurosci 1:401-417.
18. Fritzsch B, Farinas I, Reichardt L. 1997. The development of NT-3 expression as revealed with a lac-Z reporter and of innervation deficits in NT-3 mutant mice. Soc Neurosci Abstr 23:881.
19. Fritzsch B, Pirvola U, Ylikoski J. 1999. Making and breaking the innervation of the ear: neurotrophic support during ear development and its clinical implications. Cell Tissue Res 295:369-382.
20. Gil-Loyzaga P, Pujol R. 1988. Synaptophysin in the developing cochlea. Int J Dev Neurosci 6:1150-1160.
21. Godement P, Vanselow J, Thanos S, Bonhoeffer F. 1987. A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101:697-713.
22. Hafidi A, Depres G, Romand R. 1990. Cochlear innervation in the developing rat: an immunocytochemical study of neurofilament and spectrin proteins. J Comp Neurol 300:153-161.
23. Heffner HE, Heffner RS, Contos C, Ott T. 1994. Audiogram of the hooded Norway rat. Hearing Res 73:244-247.
24. Hinojosa R. 1977. A note on development of Corti's organ. Acta Otolaryngol 84:238-251.
25. Hallböök F, Fritzsch B. 1997. Distribution of BDNF and trkB mRNA in the otic region of 3.5 and 4.5 day chick embryos as revealed with a combination of in situ hybridization and tract tracing. Int J Dev Biol 41:725-732.
26. Honig MG, Hume RI. 1989. DiI and DiO: versatile fluorescent dyes for neuronal labelling and pathway tracing. Trends Neurosci 12:333-341.
27. Kachar B, Brownell WE, Altschuler R, Fex J. 1986. Electrokinetic shape changes of cochlear outer hair cells. Nature 322:365-368.
28. Kaltenbach JA, Falzarano PR. 1994. Postnatal development of the hamster cochlea. I. Growth of hair cells and the organ of Corti. J Comp Neurol 340:87-97.
29. Kelly JB, Masterton B. 1977. Auditory sensitivity of the albino rat. J Comp Physiol Psychol 91:930-936.
30. Knipper M, Zimmermann U, Rohbock K, Köpschall I, Zenner H-P. 1995. Synaptophysin and GAP-43 proteins in efferent fibers of the inner ear during postnatal development. Brain Res Dev Brain Res 89:73-86.
31. Knipper M, Zimmermann U, Rohbock K, Köpschall I, Zenner H-P. 1996. Expression of neurotrophin receptor trkB in rat cochlear hair cells at time of rearrangement of innervation. Cell Tissue Res 283:339-353.
32. Lenoir M, Shnerson A, Pujol R. 1980. Cochlear receptor development in the rat with emphasis on synaptogenesis. Anat Embryol 160:253-262.
33. Liberman MC, Dodds LW, Pierce S. 1990. Afferent and efferent innervation of the cat cochlea: quantitative analysis with light and electron microscopy. J Comp Neurol 301:443-460.
34. Lim DJ. 1987. Development of the tectorial membrane. Hearing Res 28: 9-21.
35. Lim DJ, Rueda J. 1992. Structural development of the cochlea. In: Romand R, editor. Development of auditory and vestibular systems 2. Amsterdam: Elsevier, p 33-58.
36. Ma Q, Anderson DJ, Fritzsch B. 1999. ngnl Mutants have no afferent, efferent and autonomic innervation of the ear but develop normal hair cells in smaller sensory epithelia. ARO Abstr 22:176.
37. Merchán-Pérez A, Gil-Loyzaga P, López-Sánchez J, Eybalin M, Valderrama FJ. 1993. Ontogeny of γ-aminobutyric acid in efferent fibers to the rat cochlea. Brain Res Dev Brain Res 76:33-41.
38. Merchán-Pérez A, Gil-Loyzaga P, Eybalin M, Fernández Mateos P, Bartolomé MV. 1994. Choline-acetyltransferase-like immunoreactivity in the organ of Corti of the rat during postnatal development. Brain Res Dev Brain Res 82:29-34.
39. Muller M. 1991. Frequency representation in the rat cochlea. Hearing Res 51:247-254.
40. Nadol JB Jr, Burgess BJ. 1994. Supranuclear efferent synapses on outer hair cells and Deiters' cells in the human organ of Corti. Hearing Res 81:49-56.
41. Nenov AP, Chen C, Bobbin RP. 1998. Outward rectifying potassium currents are the dominant voltage activated currents present in Deiters' cells. Hearing Res 123:168-182.
42. Nomura Y, Schuknecht HF. 1965. The efferent fibers in the cochlea. Ann Otol Rhinol Laryngol 74:289-302.
43. Pirvola U, Lehtonen E, Ylikoski J. 1991. Spatiotemporal development of cochlear innervation and hair cell differentiation in the rat. Hearing Res 52:345-355.
44. Pirvola U, Ylikoski J, Palgi J, Lehtonen E, Arumae U, Saarma M. 1992. Brain-derived neurotrophic factor and neurotrophin 3 mRNAs in the peripheral target fields of developing inner ear ganglion. Proc Natl Acad Sci USA 89:9915-9919.
45. Pirvola U, Arumae U, Moshnyakov M, Palgi J, Saarma M, Ylikoski J. 1994. Coordinated expression and function of neurotrophins and their receptors in the rat inner ear during target innervation. Hearing Res 75: 131-144.
46. Puel J, Uziel A. 1987. Correlative development of cochlear action potential sensitivity, latency, and frequency selectivity. Brain Res Dev Brain Res 37:179-188.
47. Pujol R. 1986. Synaptic plasticity in the developing cochlea. In: Ruben RJ, Van de Water TR, Rubel EW, editors. The biology of change in otolaryngology. Amsterdam: Elsevier. p 47-54.
48. Pujol R, Carlier E, Devigne C. 1978. Differential patterns of cochlear innervation during the development of the kittens. J Comp Neurol 117:529-536.
49. Rasmussen GL. 1953. Further observations of the efferent cochlear bundle. J Comp Neurol 99:61-74.
50. Robertson D, Harvey AR, Cole KS. 1989. Postnatal development of the efferent innervation of the rat cochlea. Brain Res Dev Brain Res 47: 197-207.
51. Schecterson LC, Bothwell M. 1992. Novel roles for neurotrophins are suggested by BDNF and NT-3 expression in developing neurons. Neuron 9:449-463.
52. Schecterson LC, Bothwell M. 1994. Neurotrophin and neurotrophin mRNA expression in developing inner ear. Hearing Res 73:92-100.
53. Shnerson A, Devigne D, Pujol R. 1982. Age-related changes in the C57BL/6J mouse cochlea. II. Ultrastructural findings. Brain Res Dev Brain Res 2:77-88.
54. Silos-Santiago I, Fagan AM, Garber M, Fritzsch B, Barbacid M. 1997. Severe sensory deficits but normal CNS development in newborn mice lacking TrkB and TrkC tyrosine protein kinase receptors. Eur J Neurosci 9:2045-2056.
55. Simmons DD, Liberman MC. 1988a. Afferent innervation of outer hair cells in adult cats: I. Light microscopic analysis of fibers labeled with horseradish peroxidase. J Comp Neurol 270:132-144.
56. Simmons DD, Liberman MC. 1988b. Afferent innervation of outer hair cells in adult cats: II. Electron microscopic analysis of fibers labeled with horseradish peroxidase. J Comp Neurol 270:145-154.
57. Simmons DD, Morley BJ. 1998. Differential expression of the α9 nicotinic acetylcholine receptor subunit in neonatal and adult cochlear hair cells. Brain Res Mol Brain Res 56:287-292.
58. Simmons DD, Manson-Gieseke L, Hendrix TW, McCarter S. 1990. Reconstructions of efferent fibers in the postnatal hamster. Hearing Res 49:127-140.
59. Simmons DD, Mansdorf MB, Kim JH. 1996a. Olivocochlear innervation of inner and outer hair cells during postnatal maturation: evidence for a waiting period. J Comp Neurol 370:551-562.
60. Simmons DD, Moulding HD, Zee D. 1996b. Olivocochlear innervation of inner and outer hair cells during postnatal maturation: an immunocy-tochemical study. Brain Res Dev Brain Res 95:213-226.
61. Smith CA, Rasmussen GL. 1963. Recent observation of the olivocochlear bundle. Ann Otol Rhinol Laryngol 72:489-505.
62. Sobkowicz HM. 1992. The development of innervation in the organ of Corti. In: Romand R, editor. Development of auditory and vestibular systems 2. Amsterdam: Elsevier. p 59-100.
63. Sobkowicz HM, Emmerling MR. 1989. Development of acetylcholine-sterase-positive neuronal pathways in the cochlea of the mouse. J Neurocytol 18:209-224.
64. Sobkowicz HM, Slapnick SM. 1994. The efferents interconnecting auditory inner hair cells. Hearing Res 75:81-92.
65. Sobkowicz HM, Rose JE, Scott GL, Levenick CV. 1986. Distribution of synaptic ribbons in the developing organ of Corti. J Neurocytol 15:693-714.
66. Song HJ, Ming GL, Poo MM. 1997. cAMP-induced switching in turning direction of nerve growth cones. Nature 388:275-279.
67. Uziel A, Romand R, Marot M. 1981. Development of cochlear potentials in rats. Audiology 20:89-100.
68. von Bartheld CS, Cunningham DE, Rubel EW. 1990. Neuronal tracing with DiI: decalcification, cryosectioning, and photoconversion for light and electron microscopic analysis. J Histochem Cytochem 38:725-733.
69. Walsh EJ, McGee J, McFadden SL, Liberman MC. 1998. Long-term effects of sectioning the olivocochlear bundle in neonatal cats. J Neurosci 18:3859-3869.
70. Warr WB. 1992. Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR, editors. The mammalian auditory pathway: neuroanatomy. Springer handbook of auditory research, vol 1. New York: Springer-Verlag, p 410-448.
71. Wheeler EF, Bothwell M, Schecterson LC, von Bartheld CS. 1994. Expression of BDNF and NT-3 mRNA in hair cells of the organ of Corti, quantitative analysis in developing rats. Hearing Res 73:46-56.
72. White JS, Warr WB. 1983. The dual origins of the olivocochlear bundle in the albino rat. J Comp Neurol 219:203-214.
73. Whitlon DS, Sobkowicz HM. 1989. GABA-like immunoreactivity in the cochlea of the developing mouse. J Neurocytol 18:505-518.
74. Whitlon DS, Zhang X., Kusakabe M. 1999. Tenascin-C in the cochlea of the developing mouse. J Comp Neurol 406:361-374.
75. Wiechers B, Gestwa G, Mack A, Carroll P, Zenner H-P, Knipper M. 1999. A changing pattern of brain-derived neurotrophic factor expression correlates with the rearrangement of fibers during cochlear development of rats and mice. J Neurosci 19:3033-3042.
76. Ylikoski J, Pirvola U, Moshnyakov M, Palgi J, Arumae U, Saarma M. 1993. Expression patterns of neurotrophin and their receptor mRNAs in the rat inner ear. Hearing Res 65:69-78.
77. Zuo J, Treadaway J, Buckner TW, Fritzsch B. 1999. Visualization of α9 acetylcholine receptor expression in hair cells of transgenic mice containing a modified bacterial artificial chromosome. Proc Natl Acad Sci USA 96:14100-14105.