Olivocochlear innervation in the mouse: Immunocytochemical maps, crossed versus uncrossed contributions, and transmitter colocalization

Journal of Comparative Neurology

Volumn 455, Issue 3, 2003, Pages 406-416

  Maison, Stéphane F ^a   Adams, Joe C ^a   Liberman, M Charles ^a  

^a MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

Author keywords

aminobutyric acid; Acetylcholine; Calcitonin gene related peptide; Cochlea; Efferents; Hair cells

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; CALCITONIN GENE RELATED PEPTIDE; GLUTAMATE DECARBOXYLASE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; AUDITORY NERVOUS SYSTEM; BRAIN STEM; COCHLEA; CONTROLLED STUDY; EFFERENT NERVE; FEMALE; HAIR CELL; IMMUNOCYTOCHEMISTRY; INNERVATION; MALE; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL;

ACETYLCHOLINE; ANIMALS; AUDITORY PATHWAYS; AXOTOMY; CALCITONIN GENE-RELATED PEPTIDE; CARRIER PROTEINS; COCHLEA; COCHLEAR NERVE; EFFERENT PATHWAYS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HAIR CELLS; HAIR CELLS, INNER; HAIR CELLS, OUTER; IMMUNOHISTOCHEMISTRY; MALE; MEMBRANE TRANSPORT PROTEINS; MICE; MICE, INBRED CBA; OLIVARY NUCLEUS; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS; VESICULAR TRANSPORT PROTEINS;

EID: 0037434073     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10490     Document Type: Article

References (50)

1. Adams JC. 1995. Sound stimulation induces Fos-related antigens cells with common morphological properties throughout the auditory brainstem. J Comp Neurol 361:645-668.
2. Altschuler RA, Neises GR, Harmison GG, Wenthold RJ, Fex J. 1981. Immunocytochemical localization of aspartate aminotransferase immunoreactivity in the cochlear nucleus of the guinea pig. Proc Natl Acad Sci USA 78:6553-6557.
3. Altschuler RA, Parakkal MH, Fex J. 1983. Localization of enkephalin-like immunoreactivity in acetylcholinesterase-positive cells in the guinea pig lateral superior olivary complex that project to the cochlea. Neuroscience 9:621-630.
4. Altschuler RA, Parakkal MH, Rubio JA, Hoffman DW, Fex J. 1984. Enkephalin-like immunoreactivity in the guinea pig organ of Corti: Ultrastructural and lesion studies. Hear Res 16:17-32.
5. Bailey GP, Sewell WF. 2000. Calcitonin gene-related peptide suppresses hair cell responses to mechanical stimulation in the Xenopus lateral line organ. J Neurosci 20:5163-5169.
6. Brown MC 1987. Morphology of labelled efferent fibers in the guinea pig cochlea. J Comp Neurol 260:591-604
7. Brown MC. 1989. Morphology and response properties of single olivocochlear fibers in the guinea pig. Hear Res 40:93-109.
8. Brown MC. 1993. Fiber pathways and branching patterns of biocytin-labeled olivocochlear neurons in the mouse brainstem. J Comp Neurol 337:600-613.
9. Campbell JP, Henson MM. 1988. Olivocochlear neurons in the brainstem of the mouse. Hear Res 35:271-274.
10. Dannhof BJ, Roth B, Bruns V. 1991. Anatomical mapping of choline acetyltransferase (ChAT)-like and glutamate decarboxylase (GAD)-like immunoreactivity in outer hair cell efferents in adult rats. Cell Tissue Res 266:89-95.
11. Dezaki K, Kimura I, Tsuneki H, Kimura M. 1996. Enhancement by calcitonin gene-related peptide of non-contractile Ca2(+)-induced nicotinic receptor desensitization at the mouse neuromuscular junction. Br J Pharmacol 118:1971-1976.
12. Ehret G. 1983. Peripheral anatomy and physiology II. In: Willott JF, editor. The auditory psychobiology of the mouse. Springfield, IL: Charles C Thomas. pp 169-200.
13. Eybalin M. 1993. Neurotransmitters and neuromodulators of the mammalian cochlea. Physiol Rev 73:309-373.
14. Eybalin M, Altschuler RA. 1990. Immunoelectron microscopic localization of neurotransmitters in the cochlea. J Electron Microsc 15:209-224.
15. Eybalin M, Parnaud M, Geffard M, Pujol R. 1988. Immunoelectron microscopy identifies several types of GABA-containing efferent synapses in the guinea-pig organ of Corti. Neuroscience 24:29-38.
16. Fex J, Altschuler RA. 1984. Glutamic acid decarboxylase immunoreactivity of olivocochlear neurons in the organ of Corti of guinea pig and rat. Hear Res 15:123-131.
17. Fex J, Altschuler RA. 1986. Neurotransmitter-related immunochemistry of the organ of Corti. Hear Res 22:249-263.
18. Fex J, Altschuler RA, Kachar B, Wenthold RJ, Zempel JM. 1986. GABA visualized by immunocytochemistry in the guinea pig cochlea in axons and endings of efferent neurons. Brain Res 366:106-117.
19. Gifford ML, Guinan JJ Jr. 1987. Effects of electrical stimulation of medial olivocochlear neurons on ipsilateral and contralateral cochlear responses. Hear Res 29:179-194.
20. Gitter AH, Zenner HP. 1992. γ-aminobutyric acid receptor activation of outer hair cells in the guinea pig cochlea. Eur Arch Otorhinolaryngol 249:62-65.
21. Guinan JJ Jr, Warr WB, Norris BE. 1983. Differential olivocochlear projections from lateral versus medial zones of the superior olivary complex. J Comp Neurol 221:358-370.
22. Iwasa K, Oomori Y, Tanaka H. 1999. Colocalization of gammaaminobutyric acid immunoreactivity and acetylcholinesterase activity in nerve fibers of the mouse adrenal gland. J Vet Med Sci 61:631-635.
23. A-receptor messenger ribonucleic acid (alpha-1 sub-unit) detection by in situ hybridization. Eur Arch Otorhinolaryngol 251:61-64.
24. Kirk DL, Johnstone BM. 1993. Modulation of f2-f1: Evidence for a GABAergic efferent system in apical cochlea of the guinea pig. Hear Res 67:20-34.
25. Kitajiri M, Yamashita T, Tohyama Y, Kumazawa T, Takeda N, Kawasaki Y, Matsunaha T, Girgis S, Hillyard CJ, MacIntyre I, Emson PC, Shiosaka S, Tohyama M. 1985. Localization of calcitonin gene-related peptide in the organ of Corti of the rat: An immunohistochemical study. Brain Res 358:394-397.
26. Kosaka T, Tauchi M, Dahl JL. 1988. Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Exp Brain Res 70:605-617.
27. Kujawa SG, Fallon M, Bobbin RP. 1995. Time-varying alterations in the f2-f1 DPOAE response to continuous primary stimulation. I: Response characterization and contribution of the olivocochlear efferents. Hear Res 85:142-154.
28. Liberman MC, Brown MC. 1986. Physiology and anatomy of single olivocochlear neurons in the cat. Hear Res 24:17-36.
29. 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.
30. Merchan-Perez A, Gil-Loyzaga P, Eybalin M. 1990. Ontogeny and GADand GABA immunoreactivities in the rat cochlea. Eur Arch Otorhinolaryngol 248:4-7.
31. N'Guyen LT, Grzywacz NM. 2000. Colocalization of choline acetyltransferase and γ-acid in the developing and adult turtle retinas. J Comp Neurol 420:527-538.
32. Oertel WH, Schmechel DE, Tappaz ML, Kopin IJ. 1981. Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6:2689-2700.
33. Robertson D, Gummer M. 1985. Physiological and morphological characterization of efferent neurones in the guinea pig cochlea. Hear Res 20:63-77.
34. Ryan AF, Schwartz IR. 1986. Nipecotic acid: Preferential accumulation in the cochlea by GABA uptake systems and selective retrograde transport to brainstem. Brain Res 399:399-403.
35. Ryan AF, Schwartz IR, Keithley EM, Wang ZX. 1992. Selective retrograde transport of nipecotic acid, a GABA analog, labels a subpopulation of gerbil olivocochlear neurons. J Comp Neurol 326:337-346.
36. Saffiedine S, Eybalin M. 1992a. Triple immunofluorescence evidence for a coexistence of acetylcholine, enkephalins and calcitonin gene-related peptide within efferent (olivocochlear) neurons of rats and guinea pigs. Eur J Neurosci 4:981-992.
37. Saffiedine S, Eybalin M. 1992b. Coexistence of efferent neurotransmitters. Immunocytochemical and in situ hybridization studies. In: Proceedings of the Symposium on Molecular and Biological Hearing and Deafness. La Jolla, CA. p 107.
38. Safieddine S, Prior AM, Eybalin M. 1997. Choline acetyltransferase decarboxylase, tyrosine hydroxylase, calcitonin gene-related peptide and opioid peptides coexist in lateral efferent neurons of rat and guinea-pig. Eur J Neurosci 9:356-367.
39. Scholtz AW, Kanonier G, Schrott-Fischer A. 1998. Immunohistochemical investigation of enkephalins in the human inner ear. Hear Res 118:123-128.
40. Sewell WF. 1996. Neurotransmitters and synaptic transmission. In: Dallos PJ, Popper AN, Fay RR, editors. The cochlea. New York: Springer-Verlag. pp 503-534.
41. 2+ concentration in chick cochlear hair cells. J Physiol Lond 420:127-148.
42. Thompson GC, Cortez AM, Igarashi M. 1986. GABA-like immunoreactivity in the squirrel organ of Corti. Brain Res 372:72-79.
43. Vetter DE, Adams JC, Mugnaini E. 1991. Chemically distinct rat olivocochlear neurons. Synapse 7:21-43.
44. Vetter DE, Liberman MC, Mann J, Barhanin J, Boulter J, Brown MC, Saffiote-Kolman J, Heinemann SF, Elgoyhen AB. 1999. Role of α9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 23:93-103.
45. Warr BW. 1992. Organization of olivocochlear efferent systems in mammals. In: Webster DB, Popper AN, Fay RR, editors. Mammalian auditory pathway: Neuroanatomy. New York: Springer-Verlag. pp 410-228.
46. Warr BW, Guinan JJ Jr. 1979. Efferent innervation of the organ of Corti: Two separate systems. Brain Res 173:152-155.
47. Whitlon DS, Sobkowicz HM. 1989. GABA-like immunoreactivity in the cochlea of the developing mouse. J Neurocytol 18:505-518.
48. Wilson JL, Henson MM, Henson OW. 1991. Course and distribution of efferent fibers in the cochlea of the mouse. Hear Res 55:98-108.
49. Yoshida N, Liberman MC. 1999. Stereociliary anomaly in the guinea pig: Effects of hair bundle rotation on cochlear sensitivity. Hear Res 131:29-38.
50. Zuo J, Treadaway J, Buckner TW, Fritzsch B. 1999. Visualization of α9 acetylcholine receptor expression in hair cells of transgenic mice containing a modified artificial chromosome. Proc Natl Acad Sci USA 96:14100-14105.