Presynaptic calcium dynamics and transmitter release evoked by single action potentials at mammalian central synapses

Biophysical Journal

Volumn 72, Issue 2 I, 1997, Pages 637-651

  Sinha, Saurabh R ^a   Wu, Ling Gang ^b   Saggau, Peter ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL EXPERIMENT; ARTICLE; CALCIUM TRANSPORT; HIPPOCAMPUS; HUMAN CELL; KINETICS; MODEL; NEUROTRANSMITTER RELEASE; NONHUMAN; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION;

EID: 0031030834     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(97)78702-2     Document Type: Article

References (57)

1. Adler, E. M., G. J. Augustine, S. N. Duffy and M. P. Charlton. 1991. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11:1496-1507.
2. Al-Baldawi, N. F., and R. F. Abercrombie. 1995. Cytoplasmic calcium buffer capacity determined with Nitr-5 and DM-nitrophen. Cell Calcium. 17:409-421.
3. Andersen, P. 1975. Organization of hippocampal neurons and their interconnections. In The Hippocampus. Vol. 1: Structure and Development. R. L. Isaacson and K. H. Pribram, editors. New York: Plenum Press. 155-175.
4. Augustine, G. J., E. M. Adler, and M. P. Charlton. 1991. The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann. N.Y. Acad. Sci. 635:365-381.
5. Augustine, G. J., and M. P. Charlton. 1986. Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J. Physiol. (Lond.). 381:619-640.
6. Augustine, G. J., M. P. Charlton, and S. J. Smith. 1985. Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J. Physiol. (Lond.). 369:163-181.
7. Baylor, S. M., and S. Hollingworth. 1988. Fura-2 calcium transients in frog skeletal muscle fibers. J. Physiol. (Lond.). 403:151-192.
8. Berlin, J. R., J. W. M. Bassani, and D. M. Bers. 1994. Intrinsic cytosolic calcium buffering properties of single rat cardiac myocytes. Biophys. J. 67:1775-1787.
9. 2+ indicators. Biophys. J. 65: 1632-1647.
10. Borst, J. G. G., F. Helmchen, and B. Sakmann. 1995. Pre- and postsynaptic whole-cell recording in the medial nucleus of the trapezoid body of the rat. J. Physiol. (Lond.). 489:825-840.
11. Borst, J. G. G., and B. Sakmann. 1996. Calcium influx and transmitter release in a fast CNS synapse. Nature. 383:431-434.
12. Charlton, M. P., S. J. Smith, and R. S. Zucker. 1982. Role of presynaptic calcium ions and channels in synaptic facilitation and depression at the squid giant synapse. J. Physiol. (Lond.). 323:173-193.
13. Clements, J. D., R. A. J. Lester, G. Tong, C. E. Jahr, and G. L. Westbrook. 1992. The time course of glutamate in the synaptic cleft. Science. 258:1498-1501.
14. 2+ channels on frog motor nerve terminals revealed by fluorescent ω-conotoxin. J. Neurosci. 11:1032-1039.
15. Crank, J. 1978. The Mathematics of Diffussion, 2nd ed. Clarendon Press, Oxford.
16. Dittman, J. S., and W. G. Regehr. 1996. Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J. Neurosci. 16:1623-1633.
17. Dodge, F. A., and R. Rahamimoff. 1967. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. (Lond.). 193:419-432.
18. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260:3440-3450.
19. Heidelberger, R., C. Heinemann, E. Neher, and G. Matthews. 1994. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature. 371:513-515.
20. 2+ binding kinetics of fura-2 and azo-1 from temperature-jump relaxation measurements. Biophys. J. 53: 635-639.
21. Katz, B., and R. Miledi. 1970. Further study of the role of calcium in synaptic transmission. J. Physiol. (Lond.). 207:789-801.
22. Konishi, M., and J. R. Berlin. 1993. Ca transients in cardiac myocytes measured with a low affinity fluorescent indicator, furaptra. Biophys. J. 64:1331-1343.
23. Lagnado, L., L. Cervetto, and P. A. McNaughton. 1992. Calcium homeostasis in the outer segments of retinal rods from the tiger salamander. J. Physiol, (Lond.). 455:111-142.
24. 2+ chelators. J. Neurophysiol. 72: 825-830.
25. Llinás, R. R., M. Sugimori, and R. B. Silver. 1992. Microdomains of high calcium concentration in a presynaptic terminal. Science. 256:677-679.
26. 2+ imaging of CNS axons in culture indicates reliable coupling between single action potentials and distal functional release sites. Neuron. 16:783-795.
27. Miller, A., and B. Hu. 1995. A molecular model of low-voltage-activated calcium conductance. J. Neurophysiol. 73:2349-2356.
28. Mintz, I. M., B. L. Sabatini, and W. G. Regehr. 1995. Calcium control of transmitter release at a cerebellar synapse. Neuron. 15:675-688.
29. Neher, E. 1995. The use of fura-2 for estimating Ca buffers and Ca fluxes. Neuropharmacology. 34:1423-1442.
30. Neher, E., and G. J. Augustine. 1992. Calcium gradients and buffers in bovine chromaffin cells. J. Physiol. (Lond.). 450:273-301.
31. Peters, A., S. L. Palay, and H. deF. Webster. 1991. The Fine Structure of the Nervous System: Neurons and Their Supporting Cells, 3rd Ed. Oxford University Press, New York.
32. Qian, J., L.-G. Wu, and P. Saggau. 1995. Presynaptic calcium influx is modulated during muscarinic receptor-induced presynaptic inhibition and LTP at CA3-CA1 synapses in guinea pig hippocampus. Soc. Neurosci. Abstr. 21:432.19.
33. Raju, B., E. Murphy, L. A. Levy, R. D. Hall, and R. E. London. 1989. A fluorescent indicator for measuring cytosolic free magnesium. Am. J. Physiol. 256:C540-C548.
34. Regehr, W. G., and P. P. Alturi. 1995. Calcium transients in cerebellar granule cell presynaptic terminals. Biophys. J. 68:2156-2170.
35. Regehr, W. G., K. R. Delaney, and D. W. Tank. 1994. The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J. Neurosci. 14:523-537.
36. Regehr, W. G., and D. W. Tank. 1991. Selective fura-2 loading of presynaptic terminals and nerve cell processes by local perfusion in brain slice. J. Neurosci. Methods. 37:111-119.
37. Roberts, W. M. 1993. Spatial calcium buffering in saccular hair cells. Nature. 363:74-76.
38. Roberts, W. M., R. A. Jacobs, and A. J. Hudspeth. 1990. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cell. J. Neurosci. 10:3664-3684.
39. Robitaille, R., E. M. Adler, and M. P. Charlton. 1990. Strategic location of calcium channels at transmitter release sites of frog neuromuscular junction. Neuron. 5:773-779.
40. Saggau, P., L.-G. Wu, and I. Yehezkely. 1992. Optical recording of transients of cytosolic free calcium in synaptic structures of hippocampal CA1 pyramidal cells employing a novel selective loading technique in brain slices. Biophys. J. 61:2941.
41. Sala, F., and A. Hernandez-Cruz. 1990. Calcium diffusion modeling in a spherical neuron: relevance of buffering properties. Biophys. J. 57: 313-324.
42. Sinha, S. R., L.-G. Wu, and P. Saggau. 1996. A model of presynaptic calcium transients and neurotransmitter release from terminals in the mammalian central nervous system. Biophys. J. 70:A197.
43. Smith, S. J., J. Buchanan, L. R. Osses, M. P. Charlton, and G. J. Augustine. 1993. The spatial distribution of calcium signals in squid presynaptic terminals. J. Physiol. (Lond.). 472:573-593.
44. Stanley, E. F. 1993. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron. 11:1007-1011.
45. Svoboda, K., D. W. Tank, and W. Denk. 1996. Action potential evoked calcium transients in individual neocortical presynaptic terminals measured using two photon fluorescence scanning microscopy. Biophys. J. 70:A371.
46. 2+, exocytosis, endocytosis in single melanotrophs of the rat pituitary. Neuron. 5:723-733.
47. Westrum, L. E., and T. W. Blackstad. 1962. An electron microscopic study of the stratum radiatum of the rat hippocampus (regio superior, CA1) with particular emphasis on synaptology. J. Comp. Neurol. 119: 281-309.
48. 2+ channels in rat hippocampus. J. Neurosci. 16: 2226-2237.
49. Wu, L.-G., and P. Saggau. 1994a. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J. Neurosci. 14: 645-654.
50. Wu, L.-G., and P. Saggau. 1994b. Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J. Neurosci. 14:5613-5622.
51. Wu, L.-G., and P. Saggau. 1994c. Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron. 12:1139-1148.
52. Wu, L.-G., and P. Saggau. 1995a. Block of multiple presynaptic calcium channel types by ω-conotoxin-MVIIC at hippocampal CA3 to CA1 synapses. J. Neurophysiol. 73:1965-1972.
53. 2+ influx. J. Physiol. (Lond.). 485:649-657.
54. Yawo, H., and N. Chuhma. 1994. ω-Conotoxin-sensitive and -resistant transmitter release from the chick ciliary presynaptic terminal. J. Physiol. (Lond.). 477:437-448.
55. Zhou, Z., and E. Neher. 1993. Mobile and immobile calcium buffers in bovine adrenal chromaffin cells. J. Physiol. (Lond.). 469:245-273.
56. Zucker, R. S., K. R. Delaney, R. Mulkey, and D. W. Tank. 1991. Presynaptic calcium in transmitter release and posttetanic potentiation. Ann. N.Y. Acad. Sci. 635:191-207.
57. Zucker, R. S., and A. L. Fogelson. 1986. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc. Natl. Acad. Sci. USA. 83:3032-3036.