Activity-related features of synapse morphology: A study of endbulbs of Held

Journal of Comparative Neurology

Volumn 365, Issue 1, 1996, Pages 141-158

  Ryugo, David K ^a   Wu, Melissa M ^a   Pongstaporn, Tan ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

active zones; electron microscopy; hearing; spontaneous discharge rate; synaptic vesicles

Indexed keywords

ANIMAL TISSUE; ARTICLE; CAT; COCHLEAR NERVE; COCHLEAR NUCLEUS; ELECTRON MICROSCOPY; INTRACELLULAR RECORDING; MALE; MICROSCOPY; MITOCHONDRION; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

ANIMALS; CATS; EVOKED POTENTIALS; HORSERADISH PEROXIDASE; MALE; MICROSCOPY, ELECTRON; MITOCHONDRIA; NERVE FIBERS; NEUROGLIA; NEURONS, AFFERENT; SYNAPSES; SYNAPTIC VESICLES; VESTIBULOCOCHLEAR NERVE;

EID: 0030070083     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960129)365:1<141::AID-CNE11>3.0.CO;2-T     Document Type: Article

References (108)

1. Bakin, J.S., and N.M. Weinberger (1990) Classical conditioning induces CS-specific receptive field plasticity in the auditory cortex of the guinea pig. Brain Res. 536:271-286.
2. Bakkum, B.W., L.A. Benevento, and R.S. Cohen (1991) Effects of light/darkand dark-rearing on synaptic morphology in the superior colliculus and visual cortex of the postnatal and adult rat. J. Neurosci. Res. 28:65-80.
3. Baude, A., Z. Nusser, J.D.B. Roberts, E. Mulvihill, R.A.J. McIlhinney, and P. Somogyi (1993) The metabotropic glutamate receptor (mGluR1α) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron 11:771-781.
4. Benson, T.W., D.K. Ryugo, and J.W. Hinds (1984) Effects of sensory deprivation on the developing mouse olfactory system: A light and electron microscopic, morphometric analysis. J. Neurosci. 4:638-653.
5. Born, D.E., and E.W. Rubel (1985) Afferent influences on brain stem auditory nuclei of the chicken: Neuron number and size following cochlea removal. J. Comp. Neurol. 231:435-445.
6. Born, D.E., D. Durham, and E.W. Rubel (1991) Afferent influences on brainstem auditory nuclei of the chick: Nucleus magnocellularis neuronal activity following cochlea removal. Brain Res. 557:37-47.
7. Bourk, T.R., J.P. Mielcarz, and B.E. Norris (1981) Tonotopic organization of the anteroventral cochlear nucleus of the cat. Hear. Res. 4:215-241.
8. Boyne, A.F., T.P. Bohan, and T.H. Williams (1975) Changes in cholinergic synaptic vesicle populations and the ultrastructure of the nerve terminal membranes of Narcine brasiliensis electric organ stimulated to fatigue in vivo. J. Cell Biol. 67:814-825.
9. Burwen, S.J., and B.H. Satir (1977) Plasma membrane folds on the mast cell surface and their relationship to secretory activity. J. Cell Biol. 74:690-697.
10. Cant, N.B., and D.K. Morest ( 1979) Bushy cells in the anteroventral cochlear nucleus of the cat: A study with the electron microscope. Neuroscience 4:1925-1945.
11. Carlin, R.K., and P. Siekevitz (1983) Plasticity in the nervous system: Do synapses divide? Proc. Natl. Acad. Sci. USA 80:3517-3521.
12. Cooke, C.K., T.M. Nolan, S.E. Dyson, and D.G. Jones (1974) Pentobarbital-induced configurational changes at the synapse. Brain Res. 76:330-335.
13. Devon, R.M., and D.G. Jones (1981) Synaptic parameters in developing rat cerebral cortex: Comparison of anaesthetized and unanaesthetized states. Dev. Neurosci. 4:351-362.
14. Diamond, M.E., M. Armstrong-James, and F.F. Ebner (1993) Experiencedependent plasticity in adult rat barrel cortex. Proc. Natl. Acad. Sci. USA 90:2082-2086.
15. Dickinson-Nelson, A., and T.S. Reese (1983) Structural changes during transmitter release at synapses in the frog sympathetic ganglion. J. Neurosci. 3:42-52.
16. Dyson, S.E., and D.G. Jones (1984) Synaptic remodelling during development and maturation: Junction differentiation and splitting as a mechanism for modifying connectivity. Dev. Brain Res. 13:125-137.
17. Edwards, F.A. (1995) LTP - A structural model to explain the inconsistencies. Trends Neurosci. 18:250-255.
18. Evans, E.F., and A.R. Palmer (1980) Relationship between the dynamic range of cochlear nerve fibers and their spontaneous activity. Exp. Brain Res. 40:115-118.
19. Fekete, D.M., E.M. Rouiller, M.C. Liberman, and D.K. Ryugo (1984) The central projections of intracellularly labeled auditory nerve fibers in cats. J. Comp. Neurol. 229:432-450.
20. Fifková, E., and M. Morales (1992) Actin matrix of dendritic spines, synaptic plasticity, and long-term potentiation. Int. Rev. Cytol. 139:267-301.
21. Fifková, E., and A. van Harreveld (1977) Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J. Neurocytol. 6:211-230.
22. Flucher, B.E., and M.P. Daniels (1989) Distribution of Na+ channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43 KD protein. Neuron 3:163-175.
23. Gil-Loyzaga, P., and R. Pujol (1990) Neurotoxieity of kainic acid in the rat cochlea during early developmental stages. Eur. Arch. Otorhinolaryngol. 248:40-48.
24. Gilbert, C.D., and T.N. Wiesel (1990) Receptive field dynamics in adult primary visual cortex. Nature 356:150-152.
25. Goodman, C.S., and C.J. Shatz (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Neuron 72(10):77-98.
26. Gray, E. (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscopic study. J. Anat. (Lond.) 93:420-433.
27. Gray, E. (1961) The granule cells, mossy synapses and Purkinje spine synapses of the cerebellum: Light and electron microscopic observations. J. Anat. (Lond.) 95:345-356.
28. Güldner, F.-H., and C.A. Ingram (1980) Increase in postsynaptic density material in optic target neurons of the rat suprachiasmatic nucleus after bilateral enucleation. Neurosci. Lett. 17:27-31.
29. Güldner, F.-H., and S.C. Phillips (1985) Structural plasticity of developing optic synapses under different lighting conditions. Neurosci. Lett. 55:225-228.
30. Gulley, R.L., D.M.D. Landis, and T.S. Reese (1978) Internal organization of membranes at end bulbs of Held in the anteroventral cochlear nucleus. J. Comp. Neurol. 180:707-142.
31. Hashisaki, G.T., and E.W. Rubel (1989) Effects of unilateral cochlea removal on anteroventral cochlear nucleus neurons in developing gerbil. J. Comp. Neurol. 283:465-473.
32. Held, H. (1893) Die centrale Gehorleitung. Arch. Anat. Physiol. Anat. Abt. 201-248.
33. Heuser, J.E., and T.S. Reese (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57:315-344.
34. Hirokawa, N. (1991) Molecular architecture and dynamics of the neuronal cytoskeleton. In R.D. Burgoyne (ed): The Neuronal Cytoskeleton. New York: Wiley-Liss, pp. 5-74.
35. Huchton, D.M., T. Pongstaporn, J.K. Niparko, and D.K. Ryugo (1995) Ultrastructural features of endbulbs of Held in deaf white cats: Changes in structure related to age of deafness. Otol. Head Neck Surg., Abstr, 113:100.
36. Hunter, C., R.S. Petralia, T. Vu, and R.J. Wenthold (1993) Expression of AMPA-selective glutamate receptor subunits in morphologically defined neurons of the mammalian cochlear nucleus. J. Neurosci. 13:1932-1946.
37. Ibata, Y., and G.D. Pappas (1976) The fine structure of synapses in relation to the large spherical neurons in the anterior ventral cochlear (sic) of the cat. J. Neurocytol. 5:395-406.
38. Kaas, J.H. (1991) Plasticity of sensory and motor maps in adult mammals. Ann. Rev. Neurosci. 14:137-167.
39. Katz, B. (1966) Nerve, Muscle, and Synapse, New York: McGraw-Hill.
40. Kennedy, M.B. (1989) Regulation of neuronal function by calcium. Trends Neurosci. 12:417-420.
41. Kiang, N.Y.-S., T. Watanabe, B.C. Thomas, and L.F. Clark (1965) Discharge Patterns of Single Fibers in the Cat's Auditory Nerve. Cambridge: MIT Press.
42. Kiang, N.Y.-S., J.M. Rho, C.C. Northrop, M.C. Liberman, D.K. Ryugo (1982) Hair-cell innervation by spiral ganglion cells in adult cats. Science 217(4555):175-177.
43. Kim. D.O., and C.E. Molnar (1979) A population study of cochlear nerve fibres: Comparison of spatial distributions of average rate and phaselocking measures of responses to single tones. J. Neurophysiol. 42:16-30.
44. Koenig, J.H., T. Kosaka, and K. Ikeda (1989) The relationship between the number of synaptic vesicles and the amount of transmitter released. J. Neurosci. 9(6):1937-1942.
45. Leake, P.A., and G.T. Hradek (1988) Cochlear pathology of long term neomycin induced deafness in cats. Hear. Res. 33:11-34.
46. Lenn, N.Y., and T.S. Reese (1966) The fine structure of nerve endings in the nucleus of the trapezoid body and the ventral cochlear nucleus. Am. J. Anat. 118:375-389.
47. LeVay, S., T.N. Wiesel, and D.H. Hubel (1980) The development of ocular dominance columns in normal and visually deprived monkeys. J. Comp. Neurol. 191:1-51.
48. Liberman, M.C. (1978) Auditory-nerve responses from cats raised in a low-noise chamber. J. Acoust. Soc. Am. 63:442-455.
49. Liberman, M.C. (1982a) Single-neuron labeling in the cat auditory nerve. Science 216:1239-1241.
50. Liberman, M.C. (1982b) The cochlear frequency map for the cat: Labeling auditory-nerve fibers of known characteristic frequency. J. Acoust. Soc. Am. 75:1441-1449.
51. Liberman, M.C. (1991) Central projections of auditory-nerve fibers of differing spontaneous rate. I. Anteroventral cochlear nucleus. J. Comp. Neurol. 313:240-258.
52. Lorente de No, R. (1981) The Primary Acoustic Nuclei. New York: Raven Press.
53. Markus, E.J., and T.L. Petit (1989) Synaptic structural plasticity: Role of synaptic shape. Synapse 3:1-11.
54. Melloni, E., and S. Pontremoli (1989) The calpains. Trends Neurosci. 12:438-443.
55. Mennerick, S., and C.F. Zorumski (1994) Glial contributions to excitatory neurotransmission in cultured hippocampal cells. Nature 368:59-62.
56. Molnar, C.E., and R.R. Pfeiffer (1968) Interpretation of spontaneous spike discharge patterns of neurons in the cochlear nucleus. Proceed. IEEE 56:993-1004.
57. Moore, D.R. (1985) Postnatal development of the mammalian central auditory system and the neural consequences of auditory deprivation. Acta Otolaryngol. (Stochk) 421 (Suppl.):19-30.
58. Moore, D.R., and N.B. Kowakhuk (1988) Auditory brainstem of the ferret: Effects of unilateral cochlear lesions on cochlear nucleus volume and projections to the inferior colliculus. J. Comp. Neurol. 272:503-515.
59. Nieto-Sampetro, M., S.F. Hoff, and C.W. Cotman (1982) Perforated postsynaptic densities: Probably intermediates in the synapse turnover. Proc. Natl. Acad. Sci. USA 79:7518-7522.
60. Nordeen, K.W., H.P. Killackey, and L.M. Kitzes (1983) Ascending projections to the inferior colliculus following unilateral cochlear ablation in the neonatal gerbil, Meriones unguiculatus. J. Comp. NeuroL 514:144-153.
61. Nusser, Z., E. Mulvihill, P. Streit, and P. Somogyi (1994) Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience 61:421-427.
62. Ösen, K.K. (1969) Cytoarchitecture of the cochlear nuclei in the cat. J. Comp. Neurol. 136:453-484.
63. Parks, T.N. (1979) Afferent influences on the development of the brain stem auditory nuclei of the chicken: Otocyst ablation. J. Comp. Neurol. 183:665-678.
64. Pasik, T.R., D.R. Moore, and E.W. Rubel (1994) Effect of altered neuronal activity on cell size in the medial nucleus of the trapezoid body and ventral cochlear nucleus of the gerbil. J. Comp. Neurol. 345:111-120.
65. Peters, A., and I.R. Kaiserman-Abramof (1969) The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Z. Zellforsch. Mikorsk. Anat. 100:487-506.
66. 1 of the dorsal nucleus of the lateral geniculate body of the cat. J. Anat. (Lond.) 100:451-486.
67. Pfeiffer, R.R. (1966) Anteroventral cochlear nucleus: Wave forms of extracellularly recorded spike potentials. Science 154:667-668.
68. Powell, T.P.S., and S.D. Erulkar (1962) Transneuronal cell degeneration in the auditory relay nuclei of the cat. J. Anat. (Lond.) 96:249-268.
69. Pysh, J.J. (1972) Morphological alterations of synapses in electrically stimulated superior cervical ganglia of the cat. Science 176:191-193.
70. Raman, I.M., and L.O. Trussell (1992) The kinetics of the response to glutamate and kainate in neurons of the avian cochlear nucleus. Neuron 9:173-186.
71. Ramón y Cajal, S. (1909) Histologie du Système Nerveux de l'Homme et des Vertébrés, vol. I. Madrid: Instituto Ramón y Cajal (1952 reprint).
72. Recanzone, G.H., C.E. Schreiner, and M.M. Merzenich (1993) Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J. Neurosci. 13:87-103.
73. Rees, S., F.-H. Güldner. and L. Aitkin (1985) Activity dependent plasticity of postsynaptic density structure in the ventral cochlear nucleus of the rat. Brain Res. 325:370-374.
74. Robertson, D., and D. R. Irvine (1989) Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J. Comp. Neurol. 282:456-471.
75. Rostas, J.A.P., J.M. Kavanaugh, P.R. Dodd, J.W. Heath, and D.A. Powis (1992) Mechanisms of synaptic plasticity: Changes in postsynaptic densities and glutamate receptors in chicken forebrain during maturation. Mol. Neurobiol. 5(2-4):203-216.
76. Rothstein, J.D., L. Martin, A.I. Levey, M. Dykes-Hoberg, L. Jin, D. Wu, N. Nash, and R.W. Kuncl (1994) Localization of neuronal and glial glutamate transporters. Neuron 23:713-725.
77. Rouiller, E.M., R. Cronin-Schreiber, D.M. Fekete. and D.K. Ryugo (1986) The central projections of intracellularly labeled auditory nerve fibers: An analysis of terminal morphology. J. Comp. Neurol. 549:261-278.
78. Ryugo, D.K. (1992) The auditory nerve: Peripheral innervation, cell body morphology, and central projections. In D.B. Webster (ed): Mammalian Auditory Pathway: Neuroanatomy. New York: Springer-Verlag, pp. 23-65.
79. Ryugo, D.K., and D.M. Fekete (1982) Morphology of primary axosomatic endings in the anteroventral cochlear nucleus of the cat: A study of the endbulbs of Held. J. Comp. Neurol. 210:239-257.
80. Ryugo, D.K., and S.K. May (1993) The projections of intracellularly labeled auditory nerve fibers to the dorsal cochlear nucleus of cats. J. Comp. Neurol. 329:20-35.
81. Ryugo, D.K., and E.M. Rouiller (1988) The central projections of intracellularly labeled auditory nerve fibers in cats: Morphometric correlations with physiological properties. J. Comp. Neurol. 271:130-142.
82. Ryugo, D.K., and S. Sento (1991) Synaptic connections of the auditory nerve in cats: Relationship between endbulbs of Held and spherical bushy cells. J. Comp. Neurol. 305:35-48.
83. Sachs. M.B., and P.J. Abbas (1974) Rate versus level functions for auditorynerve fibers in cats: Tone-burst stimulation. J. Acoust. Soc. Am. 56:1835-1847.
84. Schwaber, M.K., P.E. Garraghty, and J.H. Kaas (1993) Neuroplasticity of the adult primary auditory cortex following cochlear hearing loss. Am. J. Otol. 14:252-258.
85. Seitanidou, T., A. Triller, and H. Korn (1988) Distribution of glycine receptors on the membrane of a central neuron: An immunoelectron microscopy study. J. Neurosci. 5:4319-4333.
86. Sento, S., and D.K. Ryugo (1989) Endbulbs of Held and spherical bushy cells in cats: Morphological correlates with physiological properties. J. Comp. Neurol. 280:553-562.
87. Shatz, C.J. (1990) Impulse activity and the patterning of connections during CNS development. Neuron 5:745-756.
88. Shatz, C.J., and M.P. Stryker (1978) Ocular dominance in layer IV of the cat's visual cortex and the effects of monocular deprivation. J. Physiol. 281:267-283.
89. Shatz, C.J., and M.P. Stryker (1988) Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. Science 242:87-89.
90. Sie, K.C.Y., and E.W. Rubel (1992) Rapid changes in protein synthesis and cell size in the cochlear nucleus following eighth nerve activity blockade or cochlea ablation. J. Comp. Neurol. 320:501-508.
91. Siekevitz, P. (1985) The postsynaptic density: A possible role in the long-lasting effects in the central nervous system. Proc. Natl. Acad. Sci. USA 82:3494-3498.
92. Sokolich. W.G. (1977) Improved acoustic system for auditory research. J. Acoust. Soc. Am. 62(Suppl.):512.
93. Spoendlin, H. (1978) The afferent innervation of the cochlea. In R.F. Naunton and C. Fernandez (eds): Evoked Electrical Activity in the Auditory Nervous System. New York: Academic Press, pp. 21-41.
94. Storck, T., S. Schulte, K. Hofmann, and W. Stoffel (1992) Structure, expression, and functional analysis of a Na(+)-dependent glutamate/ aspartate transporter from rat brain. Proc. Natl. Acad. Sci. USA 89:10955-10909.
95. Szentágothai, J. (1963) The structure of the synapse in the lateral geniculate body. Acta Anat. 55:166-185.
96. Trune, D.R. (1982) Influence of neonatal cochlear removal on the development of mouse cochlear nucleus: I. Number, size, and density of its neurons. J. Comp. Neurol. 209:409-424.
97. Trussell, L.O., and G.D. Fischbach (1989) Glutamate receptor desensitization and its role in synaptic transmission. Neuron 3:209-218.
98. Tucci, D.L., D.E. Born, and E.W. Rubel (1987) Changes in spontaneous activity and CNS morphology associated with conductive and sensorineural hearing loss in chickens. Ann. Otol. Rhinol. Laryngol. 96:343-350.
99. Van der Loos, H., and T.A. Woolsey (1973) Somatosensory cortex: Structural alterations following early injury to sense organs. Science 179:395-398.
100. Van Huizen. F., H.J. Romijn, and M.A. Corner (1987) Indications for a critical period for synapse elimination in developing rat cerebral cortex cultures. Brain Res. 428:1-6.
101. Vrensen, G., and J.N. Cardozo (1981) Changes in size and shape of synaptic connections after visual training: An ultrastructural approach of synaptic plasticity. Brain Res. 218:19-97.
102. Weinberger, N.M. (1995) Dynamic regulation of receptive fields and maps in the adult sensory cortex. Ann. Rev. Neurosci. 18:129-158.
103. Weinberger, N.M., R. Javid, and B. Lepan (1993) Long-term retention of learning-induced receptive-field plasticity in the auditory cortex. Proc. Natl. Acad. Sci. USA 90:2394-2398.
104. Weisel, T.N., and D.H. Hubel (1963) Effects of visual deprivation on morphology and physiology of cells in the cat's lateral geniculate body. J. Neurophysiol. 26:973-993.
105. Wenthold, R.J. (1985) Glutamate and aspartate as neurotransmitters of the auditory nerve. In D.G. Drescher (ed): Auditory Biochemistry. Springfield: Thomas, pp. 125-140.
106. Wesa, J.M., F.-L.F. Chang, W.T. Greenough, and R.W. West (1982) Synaptic contact curvature: Effects of differential rearing on rat occipital cortex. Dev. Brain Res. 4:253-257.
107. Zhang, S., and L.O. Trussell (1994) A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J. Neurophysiol. 72:705-718.
108. Zhou, N., and T.N. Parks (1992) γ-D-glutamylaminomethyl sulfonic acid (GAMS) distinguishes subtypes of glutamate receptor in the chick cochlear nucleus (nuc. magnocellularis). Hear. Res. 60:20-26.