Abstract
The distribution of enkephalin-like immunoreactivity in the cochlea of the guinea pig and cat was studied. Indirect immunofluorescence immunohistochemistry using antisera generated against a methionine enkephalin-bovine thyroglobulin conjugate was applied to surface preparations of the organ of Corti and cryostat sections of the whole of the cochlea. In the cochlear osseous spiral lamina, immunofluorescence was localized to unmyelinated fibers of the intraganglionic spiral bundle. In the organ of Corti, immunofluorescence was localized to a small number of fibers at inner hair cells, the inner spiral bundle, and tunnel spiral bundle, to tunnel crossing fibers at the level of the tunnel floor, to an occasional spiral outer fiber, and to the synaptic region of outer hair cells in the three rows of the basal turn of the cochlea. Less immunofluorescence was found in this region as one progressed towards the apex, with none seen at the apex. At the most apical region the inner spiral bundle became patchy and the tunnel spiral bundle developed arcades. There was no immunofluorescence found in spiral ganglion cells, in auditory nerve fibers, or in the hair cells of the organ of Corti. The findings were the same in cat as in guinea pig, the latter being studied in more detail. It was concluded that efferent, olivocochlear neurons of the cochlea, synapsing predominantly with primary auditory nerve fibers from the inner sensory cells or with the sensory cells, contain enkephalin-like immunoreactivity. Also, the findings indicate that endings of olivocochlear neurons that synapse predominantly with outer hair cells contain enkephalin-like immunoreactivity. It has previously been shown that olivocochlear neurons are likely to be cholinergic.
Keywords: opioid, cholinergic neurons, organ of Corti, immunofluorescence, efferent synapses
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- CHURCHILL J. A., SCHUKNECHT H. F., DORAN R. Acetylcholinesterase activity in the cochlea. Laryngoscope. 1956 Jan;66(1):1–15. doi: 10.1288/00005537-195601000-00001. [DOI] [PubMed] [Google Scholar]
- COONS A. H. Fluorescent antibody methods. Gen Cytochem Methods. 1958;1:399–422. [PubMed] [Google Scholar]
- DESMEDT J. E., LAGRUTTA V. FUNCTION OF THE UNCROSSED EFFERENT OLIVOCOCHLEAR FIBRES IN THE CAT. Nature. 1963 Nov 2;200:472–474. doi: 10.1038/200472b0. [DOI] [PubMed] [Google Scholar]
- DESMEDT J. E., MONACO P. Mode of action of the efferent olivo-cochlear bundle on the inner ear. Nature. 1961 Dec 30;192:1263–1265. doi: 10.1038/1921263a0. [DOI] [PubMed] [Google Scholar]
- Elde R., Hökfelt T., Johansson O., Terenius L. Immunohistochemical studies using antibodies to leucine-enkephalin: initial observations on the nervous system of the rat. Neuroscience. 1976 Aug;1(4):349–351. doi: 10.1016/0306-4522(76)90063-4. [DOI] [PubMed] [Google Scholar]
- FEX J. AUDITORY ACTIVITY IN UNCROSSED CENTRIFUGAL COCHLEAR FIBRES IN CAT. A STUDY OF A FEEDBACK SYSTEM. II. Acta Physiol Scand. 1965 May-Jun;64:43–57. doi: 10.1111/j.1748-1716.1965.tb04152.x. [DOI] [PubMed] [Google Scholar]
- FEX J. Auditory activity in centrifugal and centripetal cochlear fibres in cat. A study of a feedback system. Acta Physiol Scand Suppl. 1962;189:1–68. [PubMed] [Google Scholar]
- Fex J., Adams J. C. alpha-Bungarotoxin blocks reversibly cholinergic inhibition in the cochlea. Brain Res. 1978 Dec 29;159(2):440–444. doi: 10.1016/0006-8993(78)90555-3. [DOI] [PubMed] [Google Scholar]
- Fex J., Wenthold R. J. Choline acetyltransferase, glutamate decarboxylase and tyrosine hydroxylase in the cochlea and cochlear nucleus of the guinea pig. Brain Res. 1976 Jun 18;109(3):575–585. doi: 10.1016/0006-8993(76)90036-6. [DOI] [PubMed] [Google Scholar]
- GALAMBOS R. Suppression of auditory nerve activity by stimulation of efferent fibers to cochlea. J Neurophysiol. 1956 Sep;19(5):424–437. doi: 10.1152/jn.1956.19.5.424. [DOI] [PubMed] [Google Scholar]
- Glazer E. J., Basbaum A. I. Leucine enkephalin: localization in and axoplasmic transport by sacral parasympathetic preganglionic neurons. Science. 1980 Jun 27;208(4451):1479–1481. doi: 10.1126/science.6155697. [DOI] [PubMed] [Google Scholar]
- Godfrey D. A., Krzanowski J. J., Jr, Matschinsky F. M. Activities of enzymes of the cholinergic systems in the guinea pig cochlea. J Histochem Cytochem. 1976 Feb;24(2):470–472. doi: 10.1177/24.2.1254944. [DOI] [PubMed] [Google Scholar]
- Gulley R. L., Reese T. S. Freeze-fracture studies on the synapses in the organ of Corti. J Comp Neurol. 1977 Feb 15;171(4):517–543. doi: 10.1002/cne.901710407. [DOI] [PubMed] [Google Scholar]
- HILDING D., WERSALL J. Cholinesterase and its relation to the nerve endings in the inner ear. Acta Otolaryngol. 1962 Sep;55:205–217. doi: 10.3109/00016486209127354. [DOI] [PubMed] [Google Scholar]
- Hughes J., Smith T. W., Kosterlitz H. W., Fothergill L. A., Morgan B. A., Morris H. R. Identification of two related pentapeptides from the brain with potent opiate agonist activity. Nature. 1975 Dec 18;258(5536):577–580. doi: 10.1038/258577a0. [DOI] [PubMed] [Google Scholar]
- Hökfelt T., Johansson O., Ljungdahl A., Lundberg J. M., Schultzberg M. Peptidergic neurones. Nature. 1980 Apr 10;284(5756):515–521. doi: 10.1038/284515a0. [DOI] [PubMed] [Google Scholar]
- Ishii D., Balogh K., Jr Distribution of efferent nerve endings in the organ of Corti. Their graphic reconstruction in cochleae by localization of acetylcholinesterase activity. Acta Otolaryngol. 1968 Oct;66(4):282–288. doi: 10.3109/00016486809126295. [DOI] [PubMed] [Google Scholar]
- Jasser A., Guth P. S. The synthesis of acetylcholine by the olivo-cochlear bundle. J Neurochem. 1973 Jan;20(1):45–53. doi: 10.1111/j.1471-4159.1973.tb12103.x. [DOI] [PubMed] [Google Scholar]
- Julliard J. H., Shibasaki T., Ling N., Guillemin R. High-molecular-weight immunoreactive beta-endorphin in extracts of human placenta is a fragment of immunoglobulin G. Science. 1980 Apr 11;208(4440):183–185. doi: 10.1126/science.6244620. [DOI] [PubMed] [Google Scholar]
- KIMURA R., WERSALL J. Termination of the olivo-cochlear bundle in relation to the outer hair cells of the organ of Corti in guinea pig. Acta Otolaryngol. 1962 Jul-Aug;55:11–32. doi: 10.3109/00016486209127336. [DOI] [PubMed] [Google Scholar]
- Micevych P., Elde R. Relationship between enkephalinergic neurons and the vasopressin-oxytocin neuroendocrine system of the cat: an immunohistochemical study. J Comp Neurol. 1980 Mar 1;190(1):135–146. doi: 10.1002/cne.901900109. [DOI] [PubMed] [Google Scholar]
- Morrison D., Schindler R. A., Wersäll J. A quantitative analysis of the afferent innervation of the organ of corti in guinea pig. Acta Otolaryngol. 1975 Jan-Feb;79(1-2):11–23. doi: 10.3109/00016487509124649. [DOI] [PubMed] [Google Scholar]
- Paradiesgarten A., Spoendlin H. The unmyelinated nerve fibres of the cochlea. Acta Otolaryngol. 1976 Sep-Oct;82(3-4):157–164. doi: 10.3109/00016487609120876. [DOI] [PubMed] [Google Scholar]
- RASMUSSEN G. L. Further observations of the efferent cochlear bundle. J Comp Neurol. 1953 Aug;99(1):61–74. doi: 10.1002/cne.900990105. [DOI] [PubMed] [Google Scholar]
- SCHUKNECHT H. F., CHURCHILL J. A., DORAN R. The localization of acetylcholinesterase in the cochlea. AMA Arch Otolaryngol. 1959 May;69(5):549–559. doi: 10.1001/archotol.1959.00730030561005. [DOI] [PubMed] [Google Scholar]
- SMITH C. A., SJOSTRAND F. S. Structure of the nerve endings on the external hair cells of the guinea pig cochlea as studied by serial sections. J Ultrastruct Res. 1961 Dec;5:523–556. doi: 10.1016/s0022-5320(61)80025-7. [DOI] [PubMed] [Google Scholar]
- Schultzberg M., Hökfelt T., Terenius L., Elfvin L. G., Lundberg J. M., Brandt J., Elde R. P., Goldstein M. Enkephalin immunoreactive nerve fibres and cell bodies in sympathetic ganglia of the guinea-pig and rat. Neuroscience. 1979;4(2):249–270. doi: 10.1016/0306-4522(79)90087-3. [DOI] [PubMed] [Google Scholar]
- Simantov R., Kuhar M. J., Uhl G. R., Snyder S. H. Opioid peptide enkephalin: immunohistochemical mapping in rat central nervous system. Proc Natl Acad Sci U S A. 1977 May;74(5):2167–2171. doi: 10.1073/pnas.74.5.2167. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simantov R., Snyder S. H. Morphine-like peptides in mammalian brain: isolation, structure elucidation, and interactions with the opiate receptor. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2515–2519. doi: 10.1073/pnas.73.7.2515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skowsky W. R., Fisher D. A. The use of thyroglobulin to induce antigenicity to small molecules. J Lab Clin Med. 1972 Jul;80(1):134–144. [PubMed] [Google Scholar]
- Spoendlin H. Innervation patterns in the organ of corti of the cat. Acta Otolaryngol. 1969 Feb-Mar;67(2):239–254. doi: 10.3109/00016486909125448. [DOI] [PubMed] [Google Scholar]
- Spoendlin H. Neural connections of the outer haircell system. Acta Otolaryngol. 1979 Mar-Apr;87(3-4):381–387. doi: 10.3109/00016487909126437. [DOI] [PubMed] [Google Scholar]
- Stopp P. E., Comis S. D. Afferent and efferent innervation of the guinea-pig cochlea: a light microscopic and histochemical study. Neuroscience. 1978;3(12):1197–1206. doi: 10.1016/0306-4522(78)90139-2. [DOI] [PubMed] [Google Scholar]
- Terayama Y., Yamamoto K. Olivo-cochlear bundle in the guinea pig cochlea after central transsection of the crossed bundle. Electron microscopic study on origin and distribution of unmyelinated efferent fibers by axonal degeneration. Acta Otolaryngol. 1971 Dec;72(6):385–396. doi: 10.3109/00016487109122498. [DOI] [PubMed] [Google Scholar]
- Warr W. B., Guinan J. J., Jr Efferent innervation of the organ of corti: two separate systems. Brain Res. 1979 Sep 7;173(1):152–155. doi: 10.1016/0006-8993(79)91104-1. [DOI] [PubMed] [Google Scholar]
- Warr W. B. Olivocochlear and vestibular efferent neurons of the feline brain stem: their location, morphology and number determined by retrograde axonal transport and acetylcholinesterase histochemistry. J Comp Neurol. 1975 May 15;161(2):159–181. doi: 10.1002/cne.901610203. [DOI] [PubMed] [Google Scholar]
- Wright C. G. Cochlear innervation in the guinea pig. I. The inner spiral bundle region. Acta Otolaryngol. 1975 Sep-Oct;80(3-4):220–229. doi: 10.3109/00016487509121322. [DOI] [PubMed] [Google Scholar]
- Wright C. G., Preston R. E. Cochlear innervation in the guinea pig. II. The spiral tunnel bundle. Acta Otolaryngol. 1975 Nov-Dec;80(5-6):335–342. doi: 10.3109/00016487509121335. [DOI] [PubMed] [Google Scholar]
- Wright C. G., Preston R. E. Degeneration and distribution of efferent nerve fibers in the guinea pig organ of Corti. A light and scanning electron microscopic study. Brain Res. 1973 Aug 17;58(1):37–59. doi: 10.1016/0006-8993(73)90822-6. [DOI] [PubMed] [Google Scholar]