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Presynaptic fibres of spiral neurons and reciprocal synapses in the organ of Corti in culture

  • Published:
Journal of Neurocytology

Summary

Isolated segments of the newborn mouse organ of Corti were explanted together with the spiral ganglion components. Within the innervation provided by the spiral neurons, we observed presynaptic vesiculated nerve endings that form reciprocal ribbon-afferent/efferent synapses with inner hair cells. These intracochlear presynaptic fibres are characteristically located between adjoining inner hair cells, on the modiolar side, low and close to the supporting cells. The presynaptic fibres display different modes of synaptic connectivity, forming repetitive reciprocal synapses on single inner hair cells or on adjoining hair cells, or connecting adjoining inner hair cells through simultaneous efferent synapses. Many presynaptic fibres exhibit a distinctive ultrastructure: defined clusters of synaptic vesicles, dense core vesicles, coated vesicles, and mitochondria. These organelles occur focally at the synaptic sites; beyond the efferent synaptic specializations, the endings appear quite nondescript and afferent-like.

We believe that the reciprocal synapses, although observed in cultures of the organ of Corti, represent real intracochlear synaptic arrangements providing a feedback mechanism between the primary sensory receptors and a special class of spiral ganglion cells that have yet to be recognized in the organin situ.

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References

  • Allerand, C. D. (1971) Patterns of neuronal differentiation in developing cultures of neonatal mouse cerebellum: a living and silver impregnation study.Journal of Comparative Neurology 142, 167–204.

    PubMed  Google Scholar 

  • Andres, K. H. (1965) Der Feinbau des bulbus olfactorius der Ratte unter besonderer Berücksichtigung der synaptischen Verbindungen.Zeitschrift für Zellforschung und mikroskopische Anatomie 65, 530–61.

    Google Scholar 

  • Blank, N. K. &Seil, F. J. (1982) Mature Purkinje cells in cerebellar tissue cultures: An ultrastructural study.Journal of Comparative Neurology 208, 169–76.

    PubMed  Google Scholar 

  • Borg, E., Densert, O. &Flock, A. (1974) Synaptic vesicles in the cochlea.Acta Otolaryngologica 78, 321–32.

    Google Scholar 

  • Calvet, M.-C., Calvet, J., Teilhac, J.-R. &Drian, M.-J. (1992) Networks formed by dorsal root ganglion neurites within spinal cord explants: a computer-aided analysis of HRP intracellularly labeled neurons.Brain Research 584, 1–10.

    PubMed  Google Scholar 

  • De Robertis, E. &Pellegrino De Iraldi, A. (1961) Plurivesicular secretory processes and nerve endings in the pineal gland of the rat.Journal of Biophysical & Biochemical Cytology 10, 361–72.

    Google Scholar 

  • Dowling, J. E. (1968) Synaptic organization of the frog retina: an electron microscopic analysis comparing the retinas of frogs and primates.Proceedings of the Royal Society of London (B) 170, 205–28.

    Google Scholar 

  • Dowling, J. E. &Boycott, B. B. (1966) Organization of the primate retina: electron microscopy.Proceedings of the Royal Society of London (B) 166, 80–111.

    Google Scholar 

  • Dunn, R. F. (1976) Reciprocal synapses in the crista ampullaris: a possible mechanism for hair cell interaction.Transactions of the American Academy of Ophthalmology and Otolaryngology 82, 188–9.

    Google Scholar 

  • Dunn, R. F. (1980) Reciprocal synapses between hair cells and first order afferent dendrites in the crista ampullaris of the bullfrog.Journal of Comparative Neurology 193, 255–64.

    PubMed  Google Scholar 

  • Ellis, L. C., Jr. &Rustioni, A. (1981) A correlative HRP, Golgi, and EM study of the intrinsic organization of the feline dorsal column nuclei.Journal of Comparative Neurology 197, 341–67.

    PubMed  Google Scholar 

  • Emmerling, M. R., Sobkowicz, H. M., Levenick, C. V., Scott, G. L., Slapnick, S. M. &Rose, J. E. (1990) Biochemical and morphological differentiation of acetyl-cholinesterase-positive efferent fibres in the mouse cochlea.Journal of Electron Microscopy Technique 15, 123–43.

    PubMed  Google Scholar 

  • Engström, H., Bergström, B. &Ades, H. W. (1972) Macula utriculi and macula sacculi in the squirrel monkey.Acta Otolaryngologica Supplement 301, 75–126.

    Google Scholar 

  • Famiglietti, E. V., Jr. (1970) Dendro-dendritic synapses in the lateral geniculate nucleus of the cat.Brain Research 20, 181–91.

    PubMed  Google Scholar 

  • Fex, J. &Altschuler, R. A. (1986) Neurotransmitter related immunocytochemistry of the organ of Corti.Hearing Research 22, 249–63.

    PubMed  Google Scholar 

  • Gähwiler, B. H. (1984) Development of the hippocampusin vitro: Cell types, synapses and receptors.Neuroscience 11, 751–60.

    PubMed  Google Scholar 

  • Gianessi, F. (1989) On the presence of reciprocal synapses in the paratympanic organ of the chicken.Anatomy and Embryology 180, 175–8.

    PubMed  Google Scholar 

  • Gil-Loyzaga, P. &Parés-Herbute, N. (1989) HPLC detection of dopamine and noradrenaline in the cochlea of adult and developing rats.Developmental Brain Research 48, 157–60.

    PubMed  Google Scholar 

  • Gobel, S., Falls, W. M., Bennett, G. J., Abdelmoumene, M., Hayashi, H. &Humphrey, E. (1980) An EM analysis of the synaptic connections of horseradish peroxidasefilled stalked cells and islet cells in the substantia gelatinosa of adult cat spinal cord.Journal of Comparative Neurology 194, 781–807.

    PubMed  Google Scholar 

  • Guillery, R. W., Sobkowicz, H. M. &Scott, G. L. (1968) Light and electron microscopical observations of the ventral horn and ventral root in long term cultures of the spinal cord of the fetal mouse.Journal of Comparative Neurology 134, 433–76.

    PubMed  Google Scholar 

  • Guillery, R. W., Sobkowicz, H. M. &Scott, G. L. (1970) Relationships between glial and neuronal elements in the development of long term cultures of the spinal cord of the fetal mouse.Journal of Comparative Neurology 140, 1–34.

    PubMed  Google Scholar 

  • Gummer, A. W. (1991) Postsynaptic inhibition can explain the concentration of short inter-spike-intervals in avian auditory nerve fibers.Hearing Research 55, 231–43.

    PubMed  Google Scholar 

  • Hager, H. &Tafuri, W. L. (1959) Elektronenoptischer Nachweis sog. neurosekretorischer Elementargranula in marklosen Nervenfasern des Plexus myentericus (Auerbach) des Meerschweinchens.Die Naturwissenschaften 46, 332–3.

    Google Scholar 

  • Hámori, J. &Silakov, L. (1980) Plasticity of relay neurons in dorsal lateral geniculate nucleus of the adult cat: Morphological evidence.Neuroscience 5, 2073–7.

    PubMed  Google Scholar 

  • Harding, B. N. (1971) Dendro-dendritic synapses, including reciprocal synapses, in the ventrolateral nucleus of the monkey thalamus.Brain Research 34, 181–5.

    PubMed  Google Scholar 

  • Herndon, R. M., Seil, F. J. &Seidman, C. (1981) Synaptogenesis in mouse cerebellum: A comparativein vivo and tissue culture study.Neuroscience 6, 2587–98.

    PubMed  Google Scholar 

  • Hild, W. (1954) Das morphologische, kinetische und endocrinologische Verhalten von hypothalamischem und neurohypophysärem Gewebe in vitro.Zeitschrift für Zellforschung und mikroskopische Anatomie 40, 257–312.

    Google Scholar 

  • Hinds, J. W. (1970) Reciprocal and serial dendrodendritic synapses in the glomerular layer of the rat olfactory bulb.Brain Research 17, 530–4.

    PubMed  Google Scholar 

  • Hirata, Y. (1964) Some observations on the fine structure of the synapses in the olfactory bulb of the mouse, with particular reference to the atypical synaptic configuration.Archives of Histology Okayama [Saibo Kaku Byorigaku Zasshi]24, 293–302.

    Google Scholar 

  • Jackowski, A., Parnavelas, J. G. &Lieberman, A. R. (1978) The reciprocal synapse in the external plexiform layer of the mammalian olfactory bulb.Brain Research 159, 17–28.

    PubMed  Google Scholar 

  • Jones, N., Fex, J. &Altschuler, R. A. (1987) Tyrosine hydroxylase immunoreactivity identifies possible catecholaminergic fibres in the organ of Corti.Hearing Research 30, 33–8.

    PubMed  Google Scholar 

  • Kim, S. U. (1974) Granule cell with somatodendritic synapse in organotypic cultures of mouse cerebellum.Experimental Neurology 45, 659–62.

    PubMed  Google Scholar 

  • King, A. S., King, D. Z., Hodges, R. D. &Henry, J. (1975) Synaptic morphology of the carotid body of the domestic fowl.Cell & Tissue Research 162, 459–73.

    Google Scholar 

  • Landis, D. M. D., Reese, T. S. &Raviola, E. (1974) Differences in membrane structure between excitatory and inhibitory components of the reciprocal synapse in the olfactory bulb.Journal of Comparative Neurology 155, 67–92.

    PubMed  Google Scholar 

  • Lavail, M. M. &Hild, W. (1971) Histotypic organization of the rat retinain vitro.Zeitschrift für Zellforschung und mikroskopische Anatomie 114, 557–79.

    Google Scholar 

  • Liberman, M. C. (1980) Morphological differences among radial afferent fibres in the cat cochlea: An electron-microscopic study of serial sections.Hearing Research 3, 45–63.

    PubMed  Google Scholar 

  • Lieberman, A. R. (1973) Neurons with presynaptic perikarya and presynaptic dendrites in the rat lateral geniculate nucleus.Brain Research 59, 35–59.

    PubMed  Google Scholar 

  • Lieberman, A. R. &Webster, K. E. (1972) Presynaptic dendrites and a distinctive class of synaptic vesicle in the rat dorsal lateral geniculate nucleus.Brain Research 42, 196–200.

    PubMed  Google Scholar 

  • Massey, S. C., Mills, S. L. &Marc, R. E. (1992) All indoleamine-accumulating cells in the rabbit retina contain GABA.Journal of Comparative Neurology 322, 275–91.

    PubMed  Google Scholar 

  • Mcdonald, D. M. (1976) Structure and function of reciprocal synapses interconnecting glomus cells and sensory nerve terminals in the rat carotid body. InChromaffin, Enterochromaffin and Related Cells (edited byCoupland, R. E. &Fujita, T.) pp. 375–94. Amsterdam: Elsevier.

    Google Scholar 

  • Mcdonald, D. M. &Mitchell, R. A. (1975) The innervation of glomus cells, ganglion cells and blood vessels in the rat carotid body: a quantitative ultrastructural analysis.Journal of Neurocytology 4, 177–230.

    Google Scholar 

  • Nadol, J. B., Jr. (1981) Reciprocal synapses at the base of outer hair cells in the organ of Corti of man.Annals of Otology, Rhinology and Laryngology 90, 12–17.

    Google Scholar 

  • Nadol, J. B., Jr. (1983) Serial section reconstruction of the neural poles of hair cells in the human organ of Corti. II. Outer hair cells.Laryngoscope 93, 780–91.

    PubMed  Google Scholar 

  • Nadol, J. B., Jr. (1984) Incidence of reciprocal synapses on outer hair cells of the human organ of Corti.Annals of Otology, Rhinology and Laryngology 93, 247–50.

    Google Scholar 

  • Nadol, J. B., Jr. (1988) Comparative anatomy of the cochlea and auditory nerve in mammals.Hearing Research 34, 253–66.

    PubMed  Google Scholar 

  • Nadol, J. B., Jr. (1990) Synaptic morphology of inner and outer hair cells of the human organ of Corti.Journal of Electron Microscopy Technique 15, 187–96.

    PubMed  Google Scholar 

  • Pasik, P., Pasik, T. &HÁmori, J. (1986) A newly recognized element in the monkey dorsal lateral geniculate nucleus exhibiting both presynaptic and postsynaptic sites.Journal of Neurocytology 15, 177–86.

    PubMed  Google Scholar 

  • Price, J. L. (1968) The termination of centrifugal fibres in the olfactory bulb.Brain Research 7, 483–6.

    PubMed  Google Scholar 

  • Pujol, R., Carlier, E. &Lenoir, M. (1980) OntOgenetic approach to inner and outer hair cell function.Hearing Research 2, 423–30.

    PubMed  Google Scholar 

  • Pujol, R., Lenoir, M. &Eybalin, M. (1986) Synaptology of the cochlea: Different types of synapse, putative neurotransmitters and physiopathological implications. InBasic and Applied Aspects of Noise-Induced Hearing Loss (edited bySalvi, R. J., Henderson, D., Hamernik, R. P. &Colletti, V.) pp. 43–53. New York: Plenum Press.

    Google Scholar 

  • Rall, W., Shepherd, G. M., Reese, T. S. &Brightman, M. W. (1966) Dendrodendritic synaptic pathway for inhibition in the olfactory bulb.Experimental Neurology 14, 44–56.

    PubMed  Google Scholar 

  • Raviola, G. &Raviola, E. (1967) Light and electron microscopic observations on the inner plexiform layer of the rabbit retina.American Journal of Anatomy 120, 403–26.

    PubMed  Google Scholar 

  • Rebière, A. &Dainat, J. (1981) Quantitative study of synapse formation in the duck olfactory bulb.Journal of Comparative Neurology 203, 103–20.

    PubMed  Google Scholar 

  • Reese, T. S. &Brightman, M. W. (1965) Electron microscopic studies on the rat olfactory bulb.Anatomical Record 151, 492.

    Google Scholar 

  • Reese, T. S. &Shepherd, G. M. (1972) Dendro-dendritic synapses in the central nervous system. InStructure and Function of Synapses (edited byPappas, G. D. &Purpura, O. P.) pp. 121–36. New York: Raven Press.

    Google Scholar 

  • Richardson, K. C. (1962) The fine structure of autonomie nerve endings in smooth muscle of the rat vas deferens.Journal of Anatomy 96, 427–42.

    PubMed  Google Scholar 

  • Richardson, K. C. (1966) Electron microscopic identification of autonomie nerve endings.Nature 210, 756.

    Google Scholar 

  • Ross, M. D. (1985) Anatomic evidence for peripheral neural processing in mammalian graviceptors.Aviation, Space and Environmental Medicine 56, 338–43.

    Google Scholar 

  • Ross, M. D. &Donovan, K. (1984) Gravity receptors: An ultrastructural basis for peripheral sensory processing.The Physiologist (Supplement) 27, S85-S86.

    Google Scholar 

  • Ross, M. D., Rogers, C. M. &Donovan, K. M. (1986) Innervation patterns in rat saccular macula.Acta Otolaryngologica 102, 75–86.

    Google Scholar 

  • Ross, M. D., Cutler, L., Meyer, G., Lam, T. &Vaziri, P. (1990) 3-D components of a biological neural network visualized in computer generated imagery.Acta Otolaryngologica 109, 83–92.

    Google Scholar 

  • Saito, K. (1990) Freeze-fracture organization of hair cell synapses in the sensory epithelium of guinea pig organ of Corti.Journal of Electron Microscopy Technique 15, 173–86.

    PubMed  Google Scholar 

  • Seil, F. J. (1979) Cerebellum in tissue culture. InReviews of Neuroscience (edited bySchneider, D. M.) pp. 105–77. New York: Raven Press.

    Google Scholar 

  • Seil, F. J. (1993) Organotypic neural cultures. InIn Vitro Biological Systems, Methods in Toxicology (edited byTyson, C. A. &Frazier, J. M.) pp. 7–26. Orlando: Academic Press.

    Google Scholar 

  • Seil, F. J., Drake-Baumann, R., Herndon, R. M. &Leiman, A. L. (1992) Cytosine arabinoside effects in mouse cerebellar cultures in the presence of astrocytes.Neuroscience 51, 149–58.

    PubMed  Google Scholar 

  • Smith, C. A. &Sjöstrand, F. S. (1961) Structure of the nerve endings on the external hair cells of the guinea pig cochlea as studied by serial sections.Journal of Ultrastructure Research 5, 523–56.

    PubMed  Google Scholar 

  • Sobkowicz, H. M. (1992) The development of innervation in the organ of Corti. InDevelopment of Auditory and Vestibular Systems II (edited byRomand, R.) pp. 59–100. Amsterdam: Elsevier.

    Google Scholar 

  • Sobkowicz, H. M. &Rose, J. E. (1983) Innervation of the organ of Corti of the fetal mouse in culture. InDevelopment of Auditory and Vestibular Systems (edited byRomand, R.) pp. 27–45. New York: Academic Press.

    Google Scholar 

  • Sobkowicz, H. M. &Slapnick, S. M. (1992) Neuronal sprouting and synapse formation in response to injury in the mouse organ of Corti in culture.International Journal of Developmental Neuroscience 10, 545–66.

    PubMed  Google Scholar 

  • Sobkowicz, H. M., Guillery, R. W. &Bornstein, M. B. (1968) Neuronal organization in long term cultures of the spinal cord of the fetal mouse.Journal of Comparative Neurology 132, 365–96.

    PubMed  Google Scholar 

  • Sobkowicz, H. M., Hartmann, H. A., Monzain, R. &Desnoyers, P. (1973) Growth, differentiation and ribonucleic acid content of the fetal rat spinal ganglion cells in culture.Journal of Comparative Neurology 148, 249–84.

    PubMed  Google Scholar 

  • Sobkowicz, H. M., Bleier, R., Bereman, B. &Monzain, R. (1974a) Axonal growth and organization of the mamillary nuclei of the newborn mouse in culture.Journal of Neurocytology 3, 431–47.

    PubMed  Google Scholar 

  • Sobkowicz, H. M., Bleier, R. &Monzain, R. (1974b) Cell survival and architectonic differentiation of the hypothalamic mamillary region of the newborn mouse in culture.Journal of Comparative Neurology 155, 355–76.

    PubMed  Google Scholar 

  • Sobkowicz, H. M., Bereman, B. &Rose, J. E. (1975) Organotypic development of the organ of Corti in culture.Journal of Neurocytology 4, 543–72.

    PubMed  Google Scholar 

  • Sobkowicz, H. M., Rose, J. E., Scott, G. L., Kuwada, S., Hind, J. E., Oertel, D. &Slapnick, S. M. (1980) Neuronal growth in the organ of Corti in culture. InTissue Culture in Neurobiology (edited byGiacobini, E., Verna-Dakis, A. &Shahar, A.) pp. 253–75. New York: Raven Press.

    Google Scholar 

  • Sobkowicz, H. M., Rose, J. E., Scott, G. L. &Slapnick, S. M. (1982) Ribbon synapses in the developing intact and cultured organ of Corti in the mouse.Journal of Neuroscience 2, 942–57.

    Google Scholar 

  • Sobkowicz, H. M., Rose, J. E., Scott, G. L. &Holy, J. M. (1984) The ultrastructure of the developing organ of Corti of the mouse in culture. InUltrastructural Atlas of the Inner Ear (edited byFriedmann, I. &Ballantyne, J.)pp. 61–97. London: Butterworths.

    Google Scholar 

  • Sobkowicz, H. M., Rose, J. E., Scott, G. L. &Levenick, C. V. (1986) Distribution of synaptic ribbons in the developing organ of Corti.Journal of Neurocytology 15, 693–714.

    Google Scholar 

  • Sobkowicz, H. M., August, B. K. &Slapnick, S. M. (1992) Epithelial repair following mechanical injury of the developing organ of Corti in culture: An electron microscopic and autoradiographic study.Experimental Neurology 115, 44–9.

    PubMed  Google Scholar 

  • Sobkowicz, H. M., Loftus, J. M. &Slapnick, S. M. (1993) Tissue culture of the organ of Corti.Acta Otolaryngologica Supplement 502, 3–36.

    Google Scholar 

  • Sotelo, C. (1977) Formation of presynaptic dendrites in the rat cerebellum following neonatal X-irradiation.Neuroscience 2, 275–83.

    PubMed  Google Scholar 

  • Sotello, C. (1982) Synaptic remodeling in agranular cerebella.Experimental Brain Research Supplement 6, 50–68.

    Google Scholar 

  • ŠpaČek, J., PaŘizek, J. &Lieberman, A. R. (1973) Golgi cells, granule cells and synaptic glomeruli in the molecular layer of the rabbit cerebellar cortex.Journal of Neurocytology 2, 407–28.

    PubMed  Google Scholar 

  • Strettoi, E., Dacheux, R. F. &Raviola, E. (1990) Synaptic connections of rod bipolar cells in the inner plexiform layer of the rabbit retina.Journal of Comparative Neurology 295, 449–66.

    PubMed  Google Scholar 

  • Tachibana, M. &Kaneko, A. (1988) Retinal bipolar cells receive negative feedback input from GABAergic amacrine cells.Visual Neuroscience 1, 297–305.

    PubMed  Google Scholar 

  • Tanaka, K. &Smith, C. A. (1978) Structure of the chicken's inner ear: SEM and TEM study.American Journal of Anatomy 153, 251–72.

    PubMed  Google Scholar 

  • Thorn, L., Schinko, I. &Wetzstein, R. (1972) Synaptic bar in the efferent part of a synapse in the organ of Corti.Experientia 28, 835.

    PubMed  Google Scholar 

  • Toran-Allerand, C. D. (1978) Culture of hypothalamic neurons: Organotypic culture.Colloques Internationaux du C.N.R.S. 280, 759–76.

    Google Scholar 

  • Usami, S.-I., Hozawa, J., Tazawa, M., Yoshihara, T., Igarashi, M. &Thompson, G. C. (1988) Immunocytochemical study of catecholaminergic innervation in the guinea pig cochlea.Acta Otolaryngologica 447, 36–45.

    Google Scholar 

  • Vaughn, J. E., Famiglietti, E. V., Jr., Barber, R. P., Saito, K., Roberts, E. &Ribak, C. E. (1981) GABAergic amacrine cells in rat retina: immunocytochemical identification and synaptic connectivity.Journal of Comparative Neurology 197, 113–27.

    PubMed  Google Scholar 

  • Whitlon, D. S. &Sobkowicz, H. M. (1989) GABA-like immunoreactivity in the cochlea of the developing mouse.Journal of Neurocytology 18, 505–18.

    PubMed  Google Scholar 

  • Wilson, D. A.&Leon, M. (1988) Noradrenergic modulation of olfactory bulb excitability in the postnatal rat.Developmental Brain Research 42, 69–75.

    Google Scholar 

  • Wolf, M. K. (1970) Anatomy of cultured mouse cerebellum. II. Organotypic migration of granule cells demonstrated by silver impregnation of normal and mutant cultures.Journal of Comparative Neurology 140, 281–98.

    PubMed  Google Scholar 

  • Wolf, M. K. &Dubois-Dalcq, M. (1970) Anatomy of cultured mouse cerebellum. I. Golgi and electron microscopic demonstrations of granule cells, their afferent and efferent synapses.Journal of Comparative Neurology 140, 261–80.

    PubMed  Google Scholar 

  • Zimmer, J. &GÄhwiler, B. H. (1984) Cellular and connective organization of slice cultures of the rat hippocampus and fascia dentata.Journal of Comparative Neurology 228, 432–46.

    PubMed  Google Scholar 

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  1. Department of Neurology, University of Wisconsin, 1300 University Avenue, W153706, Madison, USA

    H. M. Sobkowicz, S. M. Slapnick & B. K. August

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Sobkowicz, H.M., Slapnick, S.M. & August, B.K. Presynaptic fibres of spiral neurons and reciprocal synapses in the organ of Corti in culture. J Neurocytol 22, 979–993 (1993). https://doi.org/10.1007/BF01218355

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