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Autonomic synaptic transmission at single boutons and calyces

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Journal of Neurocytology

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References

  • Adler, E. M., Augustine, G. J., Duffy, S. N. & Charlton, M. P. (1991) Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. Journal of Neuroscience 11, 1496-507.

    Google Scholar 

  • Araujo, D. M. & Collier, B. (1987) Do presynaptic opiate receptors and alpha-adrenoceptors alter acetylcholine release from a sympathetic ganglion by a similar mechanism? European Journal of Pharmacology 139, 179-86.

    Google Scholar 

  • Arch, J. R. & Newsholme, E. A. (1978) Activities and some properties of 5'-nucleotidase, adenosine kinase and adenosine deaminase in tissues from vertebrates and invertebrates in relation to the control of the concentration and the physiological role of adenosine. Biochemical Journal 174, 965-77.

    Google Scholar 

  • Bartol Jr, T. M., Land, B. P., Salpeter, E. E. & Salpeter, M. M. (1991) Monte Carlo simulation of miniature endplate current generation in the vertebrate neuromuscular junction. Biophysical Journal 59, 1290-307.

    Google Scholar 

  • Bennett, M. R. (1994) Quantal secretion from single visualized synaptic varicosities of sympathetic nerve terminals. Advances in Second Messenger and Phosphoprotein Research 29, 399-423.

    Google Scholar 

  • Bennett, M. R. (1995) The origin of Gaussian distributions of synaptic potentials. Progress in Neurobiology 46, 331-50.

    Google Scholar 

  • Bennett, M. R. (1996) Neuromuscular transmission at an active zone: the secretosome hypothesis. Journal of Neurocytology 25, 869-91.

    Google Scholar 

  • Bennett, M. K., Calakos, N. & Scheller, R. H. (1992a) Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255-9.

    Google Scholar 

  • Bennett, M. R., Farnell, L. & Gibson, W. (1997a) On the origin of skewed distributions of spontaneous synaptic potentials in autonomic ganglia. Proceedings of the Royal Society of London, Series B, in press.

  • Bennett, M. R., Farnell, L., Gibson, W. G. & Lavidis, N. A. (1997b) Synaptic transmission at visualized sympathetic boutons: stochastic interaction between acetylcholine and its receptors. Biophysical Journal, in press.

  • Bennett, M. R., Florin, T. & Pettigrew, A. G. (1976) The effect of calcium ions on the binomial statistic parameters that control acetylcholine release at preganglionic nerve terminals. Journal of Physiology 257, 579-620.

    Google Scholar 

  • Bennett, M. R., Gibson, W. & Robinson, J. (1997c) Probabilistic secretion of quanta and the secretosome hypothesis: evoked release at active zones of varicosities, boutons and endplates. Biophysical Journal, in press.

  • Bennett, M. R., Gibson, W. G. & Robinson, J. (1995) Probabilistic secretion of quanta: spontaneous release at active zones of varicosities, boutons, and endplates. Biophysical Journal 69, 42-56.

    Google Scholar 

  • Bennett, M. R. & Ho, S. (1991) Probabilistic secretion of quanta from nerve terminals in avian ciliary ganglia modulated by adenosine. Journal of Physiology 440, 513-27.

    Google Scholar 

  • Bennett, M. R., Karunanithi, S. & Lavidis, N. A. (1991) Probabilistic secretion of quanta from nerve terminals in toad (Bufo marinus) muscle modulated by adenosine. Journal of Physiology 433, 421-34.

    Google Scholar 

  • Bennett, M. R., Kerr, R. & Khurana, G. (1992b) Adenosine modulation of calcium currents in postganglionic neurons of avian cultured ciliary ganglia. British Journal of Pharmacology 106, 25-32.

    Google Scholar 

  • Bertram, R., Sherman, A. & Stanley, E. F. (1996) Single-domain/bound calcium hypothesis of transmitter release and facilitation. Journal of Neurophysiology 75, 1919-31.

    Google Scholar 

  • Betz, W. J. & Bewick, G. S. (1992) Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255, 200-3.

    Google Scholar 

  • Blackman, J. G., Ginsborg, B. L. & Ray, C. (1963a) Spontaneous synaptic activity in sympathetic ganglion cells of the frog. Journal of Physiology 167, 389-401.

    Google Scholar 

  • Blackman, J. G., Ginsborg, B. L. & Ray, C. (1963b) On the quantal release of the transmitter at a sympathetic synapse. Journal of Physiology 167, 402-15.

    Google Scholar 

  • Blackman, J. G. & Purves, R. D. (1969) Intracellular recordings from ganglia of the thoracic sympathetic chain of the guinea-pig. Journal of Physiology 203, 173-98.

    Google Scholar 

  • Bornstein, J. C. (1978) Spontaneous multiquantal release at synapses in guinea-pig hypogastric ganglia: evidence that release can occur in bursts. Journal of Physiology 282, 375-98.

    Google Scholar 

  • Bornstein, J. C. (1981) Effects of stimulation of the multiquantal spontaneous synaptic potentials in guinea pig hypogastric ganglia. Neuroscience Letters 22, 57-61.

    Google Scholar 

  • Borst, J. G., Helmchen, F. & Sakmann, B. (1995) Pre-and postsynaptic whole-cell recordings in the medical nucleus of the trapezoid body of the rat. Journal of Physiology 489, 825-40.

    Google Scholar 

  • Borst, J. G. G. & Sakmann, B. (1996) Calcium influx and transmitter release is a fast CNS synapse. Nature 383, 431-4.

    Google Scholar 

  • Brain, K. L. & Bennett, M. R. (1995) Calcium in the nerve terminals of chick ciliary ganglia during facilitation, augmentation and potentiation. Journal of Physiology 489, 637-48.

    Google Scholar 

  • Brain, K. L. & Bennett, M. R. (1996) Mechanisms involved in the regulation of intracellular calcium following trains of stimuli in the chick ciliary ganglion. Proceedings of the Australian Neuroscience Society 7, 87.

    Google Scholar 

  • Briggs, C. A., Brown, T. H. & Mcafee, D. A. (1985) Neurophysiology and pharmacology of long-term potentiation in the rat sympathetic ganglion. Journal of Physiology 359, 503-21.

    Google Scholar 

  • Briggs, C. A. & Mcafee, D. A. (1988) Long-term potentiation at nicotinic synapses in the rat superior cervical ganglion. Journal of Physiology 404, 129-44.

    Google Scholar 

  • Delcastillo, J. & Katz, B. (1954) Quantal components of the end-plate potential. Journal of Physiology 124, 560-73.

    Google Scholar 

  • Delaney, K. R. & Tank, D. W. (1994) A quantitative measurement of the dependence of short-term synaptic enhancement on presynaptic residual calcium. Journal of Neuroscience 14, 5885-902.

    Google Scholar 

  • Delaney, K., Tank, D. W. & Zucker, R. S. (1991) Presynaptic calcium and serotonin-mediated enhancement of transmitter release at crayfish neuromuscular junction. Journal of Neuroscience 11, 2631-43.

    Google Scholar 

  • Delaney, K. R., Zucker, R. S. & Tank, D. W. (1989) Calcium in motor nerve terminals associated with posttetanic potentiation. Journal of Neuroscience 9, 3558-67.

    Google Scholar 

  • Dennis, M. J., Harris, A. J. & Kuffler, S. W. (1971) Synaptic transmission and its duplication by focally applied acetylcholine in parasympathetic neurons in the heart of the frog. Proceedings of the Royal Society of London Series B: Biological Sciences 177, 509-39.

    Google Scholar 

  • Derkach, V. A., Selyanko, A. A. & Skok, V. I. (1983) Acetylcholine-induced current fluctuations and fast excitatory post-synaptic currents in rabbit sympathetic neurons. Journal of Physiology 336, 511-26.

    Google Scholar 

  • Dryer, S. E. & Chiappinelli, V. A. (1987) Analysis of quantal content and quantal conductance in two populations of neurons in the avian ciliary ganglion. Neuroscience 20, 905-10.

    Google Scholar 

  • Edwards, F. A., Konnerth, A. & Sakmann, B. (1990) Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch-clamp study. Journal of Physiology 430, 213-49.

    Google Scholar 

  • Elfvin, L. G., Lindh, B. & Hokfelt, T. (1993) The chemical neuroanatomy of sympathetic ganglia. Annual Review of Neuroscience 16, 417-507.

    Google Scholar 

  • Erichsen, J. T., Karten, H. J., Eldred, W. D. & Brecha, N. C. (1982) Localization of substance P-like and enkephalin-like immunoreactivity within preganglionic terminals of the avian ciliary ganglion: light and electron microscopy. Journal of Neuroscience 2, 994-1003.

    Google Scholar 

  • Fletcher, G. H. & Chiappinelli, V. A. (1993) The actions of the kappa 1 opioid agonist U-50,488 on presynaptic nerve terminals of the chick ciliary ganglion. Neuroscience 53, 239-50.

    Google Scholar 

  • Fogelson, A. L. & Zucker, R. S. (1985) Presynaptic calcium diffusion from various arrays of single channels. Implications for transmitter release and synaptic facilitation. Biophysical Journal 48, 1003-17.

    Google Scholar 

  • Hamburger, V. & Hamilton, H. L. A. (1951) A series of normal stages in the development of the chick embryo. Journal of Morphology 88, 49-92.

    Google Scholar 

  • Happola, O., Soinila, S., Paivarinta, H. & Panula, P. (1987) [Met5]enkephalin-Arg6-Phe7-and [Met5]enkephalin-Arg6-Gly7-Leu-8-immunoreactive nerve fibres and neurons in the superior cervical ganglion of the rat. Neuroscience 21, 283-95.

    Google Scholar 

  • Haydon, P. G., Henderson, E. & Stanley, E. F. (1994) Localization of individual calcium channels at the release face of a presynaptic nerve terminal. Neuron 13, 1275-80.

    Google Scholar 

  • Hirst, G. D. & Mclachlan, E. M. (1984) Post-natal development of ganglia in the lower lumbar sympathetic chain of the rat. Journal of Physiology 349, 119-34.

    Google Scholar 

  • Horch, H. L. W. & Sargent, P. B. (1996) Synaptic and extrasynaptic distribution of two distinct populations of nicotinic acetylcholine receptor clusters in the frog cardiac ganglion. Journal of Neurocytology 25, 67-77.

    Google Scholar 

  • Katayama, Y. & Nishi, S. (1984) Sites and mechanisms of actions of enkephalin in the feline parasympathetic ganglion. Journal of Physiology 351, 111-21.

    Google Scholar 

  • Koyano, K., Kuba, K. & Minota, S. (1985) Long-term potentiation of transmitter release induced by repetitive presynaptic activities in bull-frog sympathetic ganglia. Journal of Physiology 359, 219-33.

    Google Scholar 

  • Kuba, K. & Nishi, S. (1979) Characteristics of fast excitatory postsynaptic current in bullfrog sympathetic ganglion cells. Effects of membrane potential, temperature and Ca ions. Pflugers Archiv. European Journal of Physiology 378, 205-12.

    Google Scholar 

  • Lavidis, N. A. & Bennett, M. R. (1992) Probabilistic secretion of quanta from visualized sympathetic nerve varicosities in mouse vas deferens. Journal of Physiology 454, 9-26.

    Google Scholar 

  • Lin, Y. Q., Brain, K. L. & Bennett, M. R. (1997) Calcium in sympathetic boutons of rat superior cervical ganglion during facilitation, augmentation and potentiation. Proceedings of the Australian Neuroscience Society 8, 126.

    Google Scholar 

  • Lin, Y. Q., Brain, K. L., Nichol, K. A., Morgan, J. J. & Bennett, M. R. (1996) Vesicle-associated proteins and calcium in nerve terminals of chick ciliary ganglia during development of facilitation. Journal of Physiology 497, 639-56.

    Google Scholar 

  • Llinas, R., Gruner, J. A., Sugimori, M., Mcguinness, T. L. & Greengard, P. (1991) Regulation by synapsin I and Ca(2 + )-calmodulin-dependent protein kinase II of the transmitter release in squid giant synapse. Journal of Physiology 436, 257-82.

    Google Scholar 

  • Lundberg, J. M. (1996) Pharmacology of cotransmission in the autonomic nervous system: integrative aspects on amines, neuropeptides, adenosine triphosphate, amino acids and nitric oxide. Pharmacological Reviews 48, 113-78.

    Google Scholar 

  • Macdermott, A. B., Connor, E. A., Dionne, V. E. & Parsons, R. L. (1980) Voltage clamp study of fast excitatory synaptic currents in bullfrog sympathetic ganglion cells. Journal of General Physiology 75, 39-60.

    Google Scholar 

  • Margiotta, J. F. & Berg, D. K. (1986) Enkephalin and substance P modulate synaptic properties of chick ciliary ganglion neurons in cell culture. Neuroscience 18, 175-82.

    Google Scholar 

  • Martin, A. R. & Pilar, G. (1964) Quantal components of the synaptic potential in the ciliary ganglion of the chick. Journal of Physiology 175, 1-16.

    Google Scholar 

  • Martin-Moutot, N., Charvin, N., Leveque, C., Sato, K., Nishiki, T., Kozaki, S., Takahashi, M. & Seagar, M. (1996) Interaction of SNARE complexes with P/Q-type calcium channels in rat cerebellar synaptosomes. Journal of Biological Chemistry 271, 6567-70.

    Google Scholar 

  • Mcfadzean, I. (1988) The ionic mechanisms underlying opioid actions. Neuropeptides 11, 173-80.

    Google Scholar 

  • Meriney, S. D. & Grinnell, A. D. (1991) Endogenous adenosine modulates stimulation-induced depression at the frog neuromuscular junction. Journal of Physiology 443, 441-55.

    Google Scholar 

  • Miledi, R., Molenaar, P. & Polak, R. L. (1982) Free and bound acetylcholine in frog muscle. Journal of Physiology 333, 189-99.

    Google Scholar 

  • Motin, L. G., Bennett, M. R. & Christie, M. J. (1995) Opioids acting on delta-receptors modulate Ca2+ currents in cultured postganglionic neurons of avian ciliary ganglia. Neuroscience Letters 193, 21-4.

    Google Scholar 

  • Mynlieff, M. & Beam, K. G. (1994) Adenosine acting at an A1 receptor decreases N-type calcium current in mouse motoneurons. Journal of Neuroscience 14, 3628-34.

    Google Scholar 

  • Perin, M. S., Johnston, P. A., Ozcelik, T., Jahn, R., Francke, U. & Sudhof, T. C. (1991) Structural and functional conservation of synaptotagmin (p65) in Drosophila and humans. Journal of Biological Chemistry 266, 615-22.

    Google Scholar 

  • Pieribone, V. A., Shupliakov, O., Brodin, L., Hilfiker-Rothenfluh, S., Czernik, A. J. & Greengard, P. (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375, 493-7.

    Google Scholar 

  • Poage, R. E. & Zengel, J. E. (1993) Kinetic and pharmacological examination of stimulation-induced increases in synaptic efficacy in the chick ciliary ganglion. Synapse 14, 81-9.

    Google Scholar 

  • Rang, H. P. (1981) The characteristics of synaptic currents and responses to acetylcholine of rat submandibular ganglion cells. Journal of Physiology 311, 23-55.

    Google Scholar 

  • Redman, R. S. & Silinsky, E. M. (1993) A selective adenosine antagonist (8-cyclopentyl-1,3-dipropylxanthine) eliminates both neuromuscular depression and the action of exogenous adenosine by an effect on A1 receptors. Molecular Pharmacology 44, 835-40.

    Google Scholar 

  • Redman, R. S. & Silinsky, E. M. (1994) ATP released together with acetylcholine as the mediator of neuromuscular depression at frog motor nerve endings. Journal of Physiology 477, 117-27.

    Google Scholar 

  • Regehr, W. G., Delaney, K. R. & Tank, D. W. (1994) The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. Journal of Neuroscience 14, 523-37.

    Google Scholar 

  • Regehr, W. G. & Tank, D. W. (1991) The maintenance of LTP at hippocampal mossy fiber synapses is independent of sustained presynaptic calcium. Neuron 7, 451-9.

    Google Scholar 

  • Reiner, A. (1987) A VIP-like peptide co-occurs with substance P and enkephalin in cholinergic preganglionic terminals of the avian ciliary ganglion. Neuroscience Letters 78, 22-8.

    Google Scholar 

  • Rekling, J. C. (1993) Effects of met-enkephalin on GAB-Aergic spontaneous miniature IPSPs in organotypic slice cultures of the rat hippocampus. Journal of Neuroscience 13, 1954-64.

    Google Scholar 

  • Ribeiro, J. A. & Sebastiao, A. M. (1987) On the role, inactivation and origin of endogenous adenosine at the frog neuromuscular junction. Journal of Physiology 384, 571-85.

    Google Scholar 

  • Robinson, J. (1976) Estimation of parameters for a model of transmitter release at synapses. Biometrics 32, 61-8.

    Google Scholar 

  • Robinson, I. M., Yamada, M., Carrion-Vazquez, M., Lennon, V. A. & Fernandez, J. M. (1996) Specialized release zones in chromaffin cells examined with pulsed-laser imaging. Cell Calcium 20, 181-201.

    Google Scholar 

  • Sargent, P. B. & Pang, D. Z. (1989) Acetylcholine receptor-like molecules are found in both synaptic and extrasynaptic clusters on the surface of neurons in the frog cardiac ganglion. Journal of Neuroscience 9, 1062-72.

    Google Scholar 

  • Scott, T. R. & Bennett, M. R. (1993) The effect of ions and second messengers on long-term potentiation of chemical transmission in avian ciliary ganglia. British Journal of Pharmacology 110, 461-9.

    Google Scholar 

  • Shao, X., Davletov, B. A., Sutton, R. B., SÜdhof, T. C. & Rizo, J. (1996) Bipartite Ca2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273, 248-51.

    Google Scholar 

  • Silinsky, E. M. & Redman, R. S. (1996) Synchronous release of ATP and neurotransmitter within milliseconds of a motor nerve impulse in the frog. Journal of Physiology 492, 815-22.

    Google Scholar 

  • Simon, S. M. & Llinas, R. R. (1985) Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophysical Journal 48, 485-98.

    Google Scholar 

  • Simonds, W. F. (1988) The molecular basis of opioid receptor function. Endocrine Reviews 9, 200-12.

    Google Scholar 

  • Smith, P. A. (1993) The autonomic ganglia and the modulation of ganglionic transmission. Advances in Structural Biology 2, 245-316.

    Google Scholar 

  • Stanley, E. F. (1991) Single calcium channels on a cholinergic presynaptic nerve terminal. Neuron 7, 585-91.

    Google Scholar 

  • Stanley, E. F. (1993) Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 11, 1007-11.

    Google Scholar 

  • Streichert, L. C. & Sargent, P. G. (1989) Bouton ultrastructure and synaptic growth in a frog autonomic ganglion. Journal of Comparative Neurology 281, 159-68.

    Google Scholar 

  • SÜdhof, T. C. & Rizo, J. (1996) Synaptotagmins - C2 domain proteins that regulate membrane traffic. Neuron 17, 379-88.

    Google Scholar 

  • Swandulla, D., Hans, M., Zipser, K. & Augustine, G. J. (1991) Role of residual calcium in synaptic depression and posttetanic potentiation: fast and slow calcium signalling in nerve terminals. Neuron 7, 915-26.

    Google Scholar 

  • Tashiro, N., Gallagher, J. P. & Nishi, S. (1976) Facilitation and depression of synaptic transmission in amphibian sympathetic ganglia. Brain Research 118, 45-62.

    Google Scholar 

  • Warren, D., Lavidis, N. A. & Bennett, M. R. (1995) Quantal secretion recorded from visualized boutons. Neuroscience Letters 192, 205-8.

    Google Scholar 

  • Warren, D., Lavidis, N. A. & Bennett, M. R. (1996) Quantal secretion from visualized boutons on rat pelvic ganglion neurons. Journal of the Autonomic Nervous System 56, 175-83.

    Google Scholar 

  • White, J. D., Krause, J. E., Karten, H. J. & Mckelvy, J. F. (1985) Presence and ontogeny of enkephalin and substance P in the chick ciliary ganglion. Journal of Neurochemistry 45, 1319-22.

    Google Scholar 

  • Whittaker, V. P. (1988) Synaptosome preparations. Journal of Neurochemistry 50, 324-5.

    Google Scholar 

  • Yawo, H. & Chuhma, N. (1993) Preferential inhibition of omega-conotoxin-sensitive presynaptic Ca2+-channels by adenosine autoreceptors. Nature 365, 256-8.

    Google Scholar 

  • Zengel, J. E. & Magleby, K. L. (1982) Augmentation and facilitation of transmitter release. A quantitative description at the frog neuromuscular junction. Journal of General Physiology 80, 583-611.

    Google Scholar 

  • Zengel, J. E., Magleby, K. L., Horn, J. P., Mcafee, D. A. & Yarowsky, P. J. (1980) Facilitation, augmentation, and potentiation of synaptic transmission at the superior cervical ganglion of the rabbit. Journal of General Physiology 76, 213-31.

    Google Scholar 

  • Zhang, C., Bachoo, M., Morales, M., Collier, B. & Polosa, C. (1995) The site of the inhibitory action of endogenous opioids in the superior cervical ganglion of the cat. Brain Research 683, 59-64.

    Google Scholar 

  • Zhang, C., Bachoo, M. & Polosa, C. (1993) The receptors activated by exogenous and endogenous opioids in the superior cervical ganglion of the cat. Brain Research 622, 211-4.

    Google Scholar 

  • Zucker, R. S. (1989) Short-term synaptic plasticity. Annual Review of Neuroscience 12, 13-31.

    Google Scholar 

  • Zucker, R. S. & Fogelson, A. L. (1986) Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proceedings of the National Academy of Sciences USA 83, 3032-6.

    Google Scholar 

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  1. The Neurobiology Laboratory, Department of Physiology and Institute for Biomedical Research, University of Sydney F13, NSW 2006, Australia

    M. R Bennett

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Bennett, M.R., Brain, K. Autonomic synaptic transmission at single boutons and calyces. J Neurocytol 26, 577–603 (1997). https://doi.org/10.1023/A:1018537625551

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