Effect of changes in action potential shape on calcium currents and transmitter release in a calyx-type synapse of the rat auditory brainstem

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 354, Issue 1381, 1999, Pages 347-355

  Borst, J G G ^a   Sakmann, B ^a  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

Action potential; Calcium current; Calcium domain; Calyx of Held; Presynaptic terminal; Voltage clamp

Indexed keywords

ANIMALIA; CALYX;

EID: 0033611704     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.1999.0386     Document Type: Conference Paper

References (60)

1. 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. J. Neurosci. 11, 1496-1507.
2. Augustine, G. J. 1990 Regulation of transmitter release at the squid giant synapse by presynaptic delayed rectifier potassium current. J. Physiol. 431, 343-364.
3. Augustine, G. J. & Charlton, M. P. 1986 Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J. Physiol. 381, 619-640.
4. Augustine, G. J. & Eckert, R. 1984 Divalent cations differentially support transmitter release at the squid giant synapse. J. Physiol. 346, 257-271.
5. Augustine, G. J., Charlton, M. P. & Smith, S. J. 1985 Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J. Physiol. 369, 163-181.
6. Augustine, G. J., Adler, E. M. & Charlton, M. P. 1991 The calcium signal For transmitter secretion from presynaptic nerve terminals. Ann. NY Acad. Sci. 635, 365-381.
7. Banks, M. I. & Smith, P. H. 1992 Intracellular recordings from neurobiotin-labeled cells in brain slices of the rat medial nucleus of the trapezoid body. J. Neurosci. 12, 2819-2837.
8. Barnes-Davies, M. & Forsythe, I. D. 1995 Pre- and postsynaptic glutamate receptors at a giant excitatory synapse in rat auditory brainstem slices. J. Physiol. 488, 387-406.
9. Bennett, M. K., Calakos, N. & Scheller, R. H. 1992 Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255-259.
10. Bennett, M. R. & Brain, K. 1997 Autonomic synaptic transmission at single boutons and calyces. J. Neurocytol. 26, 577-603.
11. Bezprozvanny, I., Scheller, R. H. & Tsien, R. W. 1995 Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 378, 623-626.
12. Borst, J. G. G. & Helmchen, F. 1998 Calcium influx during an action potential. In Methods in enzymology (ed. P. M. Conn), pp. 352-371. New York: Academic Press.
13. Borst, J. G. G. & Sakmann, B. 1996 Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431-434.
14. Borst, J. G. G. & Sakmann, B. 1998 Calcium current during a single action potential in a large presynaptic terminal of the rat brainstem. J. Physiol. 506, 143-157.
15. Borst, J. G. G., Helmchen, F. & Sakmann, B. 1995 Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J. Physiol. 489, 825-840.
16. Chad, J. E. & Eckert, R. 1984 Calcium domains associated with individual channels can account for anomalous voltage relations of Ca-dependent responses. Biophys. J. 45, 993-999.
17. Dodge, F. A. Jr & Rahamimoff, R. 1967 Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193, 419-432.
18. Forsythe, I. D. & Barnes-Davies, M. 1993 The binaural auditory pathway: excitatory amino acid receptors mediate dual time-course excitatory postsynaptic currents in the rat medial nucleus of the trapezoid body. Proc. R. Soc. Lond. B 251, 151-157.
19. 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, 1275-1280.
20. Helmchen, F., Borst, J. G. G. & Sakmann, B. 1997 Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys. J. 72, 1458-1471.
21. Herrington, J. & Bookman, R. J. 1994 Pulse Control V4.0: IGOR XOPs for patch clamp data acquisition and capacitance measurements. Miami, FL: University of Miami.
22. Heuser, J. E., Reese, T. S. & Landis, D. M. D. 1974 Functional changes in frog neuromuscular junctions studied with freeze-fracture. J. Neurocytol. 3, 109-131.
23. Katz, B. 1969 The release of neural transmitter substances. Springfield, IL: Thomas.
24. 2+ channel blockers on transmitter release and presynaptic currents at the frog neuromuscular junction. J. Physiol. 486, 695-706.
25. Llinás, R., Sugimori, M. & Simon, S. M. 1982 Transmission by presynaptic spike-like depolarisation in the squid giant synapse. Proc. Natl Acad. Sci. USA 79, 2415-2419.
26. Luebke, J. I., Dunlap, K. & Turner, T. J. 1993 Multiple calcium channel types control glutamatergic synaptic transmission in the hippocampus. Neuron 11, 895-902.
27. Mintz, I. M., Sabatini, B. L. & Regehr, W. G. 1995 Calcium control of transmitter release at a cerebellar synapse. Neuron 15, 675-688.
28. Neher, E. 1986 Concentration profiles of intracellular calcium in the presence of a diffusible chelator. Expl Brain Res. 14, 80-96.
29. Neher, E. 1995 The use of fura-2 for estimating Ca buffers and Ca fluxes. Neuropharmacology 34, 1423-1442.
30. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399.
31. Oertel, D. 1997 Encoding of timing in the brain stem auditory nuclei of vertebrates. Neuron 19, 959-962.
32. Ohana, O. & Sakmann, B. 1998 Transmitter release modulation in nerve terminals of rat neocortical pyramidal cells by intracellular calcium buffers. J. Physiol. 513, 135-148.
33. Olivera, B. M. (and 10 others) 1987 Neuronal calcium channel antagonists. Discrimination between calcium channel subtypes using ω-conotoxin from Conus magus venom. Biochemistry 26, 2086-2090.
34. Pape, P. C., Jong, D.-S. & Chandler, W. K. 1995 Calcium release and its voltage dependence in frog cut muscle fibers equilibrated with 20 mM EGTA. J. Gen. Physiol. 106, 259-336.
35. Pattillo, J. M., Simples, J. E. Jr, Artim, D. E. & Meriney, S. D. 1998 Alteration in timing of action potential broadening results in opposite effects on peak calcium current. Biophys. J. 74, A245.
36. Pumplin, D. W., Reese, T. S. & Llinás, R. 1981 Are the presynaptic membrane particles the calcium channels? Proc. Natn. Acad. Sci. USA 78, 7210-7213.
37. Roberts, W. M., Jacobs, R. A. & Hudspeth, A. J. 1990 Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J. Neurosci. 10, 3664-3684.
38. Robitaille, R., Adler, E. M. & Charlton, M. P. 1990 Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 5, 773-779.
39. Robitaille, R., Garcia, M. L., Kaczorowski, G. J. & Charlton, M. P. 1993 Functional colocalization of calcium and calciumgated potassium channels in control of transmitter release. Neuron 11, 645-655.
40. Sabatini, B. L. & Regehr, W. G. 1997 Control of neurotransmitter release by presynaptic waveform at the granule cell to Purkinje cell synapse. J. Neurosci. 17, 3425-3435.
41. Schweizer, F. E., Betz, H. & Augustine, G. J. 1995 From vesicle docking to endocytosis: intermediate reactions of exocytosis. Neuron 14, 689-696.
42. Spencer, A. N., Przysiezniak, J., Acosta-Urquidi, J. & Basarsky, T. A. 1989 Presynaptic spike broadening reduces junctional potential amplitude. Nature 340, 636-638.
43. Stanley, E. F. 1991 Single calcium channels on a cholinergic presynaptic nerve terminal. Neuron 7, 585-591.
44. Stanley, E. F. 1993 Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 11, 1007-1011.
45. Stanley, E. F. & Mirotznik, R. R. 1997 Cleavage of syntaxin prevents G-protein regulation of presynaptic calcium channels. Nature 385, 340-343.
46. Takahashi, T. & Momiyama, A. 1993 Different types of calcium channels mediate central synaptic transmission. Nature 366, 156-158.
47. Takahashi, T., Forsythe, I. D., Tsujimoto, T., Barnes-Davies, M. & Onodera, K. 1996 Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274, 594-597.
48. 2+ channels. EMBO J. 15, 4100-4110.
49. Wu, L.-G. & Saggau, P. 1994 Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J. Neurosci. 14, 5613-5622.
50. Wu, L.-G. & Saggau, P. 1997 Presynaptic inhibition of elicited neurotransmitter release. Trends Neurosci. 20, 204-212.
51. 2+ currents evoke transmitter release at a rat central synapse. Proc. Natn. Acad. Sci. USA 95, 4720-4725.
52. Wu, L.-G., Westenbroek, R. E., Borst, J. G. G., Catterall, W. A. & Sakmann, B. 1999 Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J. Neurosci. 19, 726-736.
53. Yamada, W. M. & Zucker, R. S. 1992 Time course of transmitter release calculated from simulations of a calcium diffusion model. Biophys. J. 61, 671-682.
54. Yawo, H. & Momiyama, A. 1993 Re-evaluation of calcium currents in pre- and postsynaptic neurones of the chick ciliary ganglion. J. Physiol. 460, 153-172.
55. Yoshida, A., Oho, C., Omori, A., Kuwahara, R., Ito, T. & Takahashi, M. 1992 HPC-1 is associated with synaptotagmin and ω-conotoxin receptor. J. Biol. Chem. 267, 24 925-24 928.
56. Yoshikami, D., Bagabaldo, Z. & Olivera, B. M. 1989 The inhibitory effects of omega-conotoxins on Ca channels and synapses. Ann. NY Acad. Sci. 560, 230-248.
57. Zengel, J. E., Sosa, M. A. & Poage, R. E. 1993 ω-conotoxin reduces facilitation of transmitter release at the frog neuromuscular junction. Brain Res. 611, 25-30.
58. Zhang, Z.-W., Coggan, J. S. & Berg, D. K. 1996 Synaptic currents generated by neuronal acetylcholine receptors sensitive to α-bungarotoxin. Neuron 17, 1231-1240.
59. Zucker, R. S. 1996 Exocytosis: a molecular and physiological perspective. Neuron 17, 1049-1055.
60. Zucker, R. S., Delaney, K. R., Mulkey, R. & Tank, D. W. 1991 Presynaptic calcium in transmitter release and posttetanic potentiation. Ann. NY Acad. Sci. 635, 191-207.