Ca2+ imaging of CNS axons in culture indicates reliable coupling between single action potentials and distal functional release sites

Neuron

Volumn 16, Issue 4, 1996, Pages 783-795

  Mackenzie, Paul J ^a   Umemiya, Masashi ^a,b   Murphy, Timothy H ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; FETUS; IMAGING; NERVE CONDUCTION; NERVE FIBER; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN CORTEX; CELL CULTURE; ELECTRON MICROSCOPY; IMAGE PROCESSING; METABOLISM; NERVE CELL; PHYSIOLOGY; PRENATAL DEVELOPMENT; SYNAPSE; ULTRASTRUCTURE;

CALCIUM; CALCIUM CHANNEL; FLUORESCENT DYE;

ACTION POTENTIALS; ANIMALS; AXONS; CALCIUM; CALCIUM CHANNELS; CELLS, CULTURED; CEREBRAL CORTEX; FLUORESCENT DYES; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, ELECTRON; NEURONS; RATS; SYNAPSES;

EID: 0029664972     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80098-7     Document Type: Article

References (67)

1. Adler, E.M., Augustine, G.J., Duffy, S.N., and Charlton, M.P. (1991). Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11, 1496-1507.
2. Allen, C., and Stevens, C.F. (1994). An evaluation of causes for unreliability of synaptic transmission. Proc. Natl. Acad. Sci. USA 91, 10380-10383.
3. Augustine, G.J., and Charlton, M.P. (1986). Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J. Physiol. (Lond.) 381, 619-640.
4. Augustine, G.J., Adler, E.M., and Charlton, M.P. (1990). The calcium signal for neurotransmitter secretion from presynaptic nerve terminals. In Calcium Entry and Action at the Presynaptic Nerve Terminal, E.F. Stanley, M.C. Nowycky, and D.J. Triggle, eds. (New York: New York Academy of Sciences), pp. 365-381.
5. Bekkers, J.M., and Stevens, C.F. (1990). Presynaptic mechanism for long term potentiation in the hippocampus. Nature 346, 724-729.
6. Betz, W.J., and Bewick, G.S. (1992). Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255, 200-203.
7. Betz, W.J., and Bewick, G.S. (1993). Optical monitoring of transmitter release and synaptic vesicle recycling at the frog neuromuscular junction. J. Physiol. (Lond.) 460, 287-309.
8. Cajal, R. (1911). Histology of the Nervous System, N. Swanson and L.W. Swanson, trans. (New York: Oxford University Press).
9. 2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron 12, 261-269.
10. Cooper, R.L., Martin, L., and Atwood, H.L. (1995). Synaptic differentiation of a single motor neuron: conjoint definition of transmitter release, presynaptic calcium signals, and ultrastructure. J. Neurosci. 15, 4209-4222.
11. Delaney, K., Tank, D.W., and Zucker, R.S. (1991). Presynaptic and serotonin-mediated enhancement of transmitter release at crayfish neuromuscular junction. J. Neurosci. 11, 2631-2643.
12. del Castillo, J., and Katz, B. (1954). Quantal components of the endplate potential. J. Physiol. (Lond.) 124, 560-573.
13. Dodge, F.A.J., and Rahamimoff, R. (1967). Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. (Lond.) 193, 419-432.
14. 2+ channels in mammalian central neurons. Trends Neurosci. 18, 89-98.
15. Fields, R.D., Yu, C., and Nelson, P.G. (1991). Calcium, network activity, and the role of NMDA channels in synaptic plasticity. J. Neurosci. 11, 134-146.
16. Frerking, M., Borges, S., and Wilson, M. (1995). Variation in GABA mini amplitude is the consequence of variation in transmitter concentration. Neuron 15, 885-895.
17. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
18. Hamill, O.P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. (1981). Improved patch-clamp techniques for high resolution current recordings from cells and cell-free membrane patches. Pflügers Arch. 391, 85-100.
19. Harris, K.M. (1995). How multiple-synapse boutons could preserve input specificity during an interneuronal spread of LTP. Trends Neurosci. 18, 365-369.
20. Heidelberger, R., Heinemann, C., Neher, E., and Matthews, G. (1994). Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513-515.
21. Hessler, N.A., Shirke, A.M., and Malinow, R. (1993). The probability of transmitter release at a mammalian central synapse. Nature 366, 569-572.
22. Hille, B. (1992). Ionic Channels of Excitable Membranes, Second Edition (Sunderland, Massachusetts: Sinauer Associates, Incorporated), pp. 321-326.
23. Jonas, P., Major, G., and Sakmann, B. (1993). Quantal components of unitary EPSPs at mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. (Lond.) 472, 615-663.
24. Liao, D., Hessler, N.A., and Malinow, R. (1995). Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404.
25. Liu, G., and Tsien, R.W. (1995). Properties of synaptic transmission and single hippocampal synaptic boutons. Nature 375, 404-408.
26. Lüscher, C., Streit, J., Lipp, P., and Lüscher, H.-R. (1994) Action potential conduction through embryonic dorsal root ganglion cells in culture. II. Decrease of conduction reliability during repetitive stimulation. J. Neurophysiol. 72, 634-643.
27. Magee, J.C., and Johnston, D. (1995). Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268, 301-304.
28. Malgaroli, A., Ting, A.E., Wendland, B., Bergamaschi, A., Villa, A., Tsien, R.W., and Scheller, R.H. (1995). Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268, 1624-1628.
29. Malinow, R. (1994). LTP: desperately seeking resolution. Science 266, 1195-1196.
30. Malinow, R., and Tsien, R.W. (1990). Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346, 177-180.
31. 2+ entry through the N-methyl-D-aspartate channel. Proc. Natl. Acad. Sci. USA 91, 8170-8174.
32. Minta, A., Kao, J., and Tsien, R.Y. (1989). Fluorescent indicators for cytosolic calcium based on rhodamine and fluorescein chromophores. J. Biol. Chem. 264, 8171-8178.
33. Mintz, I.M., Sabatini, B.L., and Regehr, W.G. (1995). Calcium control of transmitter release at a cerebellar synapse. Neuron 15, 675-688.
34. Murphy, T.H., and Baraban, J.M. (1990). Glutamate toxicity in immature cortical neurons precedes development of glutamate receptor currents. Dev. Brain Res. 57, 146-150.
35. Murphy, T.H., Baraban, J.M., Wier, W.G., and Blatter, L.A. (1994). Visualization of quantal synaptic transmission by dendritic calcium imaging. Science 263, 529-532.
36. Murphy, T.H., Baraban, J.M., and Wier, W.G. (1995). Mapping miniature synaptic currents to single synapses using calcium imaging reveals heterogeneity in postsynaptic output. Neuron 15, 159-168.
37. Peters, A., Palay, S.L., and Webster, H.D. (1976). The Fine Structure of the Nervous System: The Neurons and Their Supporting Cells (Philadelphia: W.B. Saunders Company), pp. 90-117.
38. Pumplin, D.W., Reese, T.S., and Llinás, R. (1981). Are the presynaptic membrane particles the calcium channels? Proc. Natl. Acad. Sci. USA 78, 7210-7213.
39. Raastad, M., Storm, J.F., and Andersen, P. (1992). Putative single quantum and single fibre excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur. J. Neurosci. 4, 113-117.
40. Ragu, B., Murphy, E., Levy, L.A., Hall, R.D., and London, R.E. (1989). A fluorescent indicator for measuring cytosolic free magnesium. Am. J. Physiol. 256, C540-C548.
41. Regehr, W.G., and Atluri, P.P. (1995). Calcium transients in cerebellar granule cell presynaptic terminals. Biophys. J. 68, 2156-2170.
42. Regehr, W.G., Delaney, K.R., and Tank, D.W. (1994). The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J. Neurosci. 14, 523-537.
43. 2+ channel blockers. Neuron 14, 773-779.
44. Reynolds, E.S. (1963). The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
45. Robitaille, R., Adler, E.M., and Charlton, M.P. (1990). Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 5, 773-779.
46. Rosenmund, C., Clements, J.D., and Westbrook, G.L. (1993). Non-uniform probability of glutamate release at a hippocampal synapse. Science 262, 754-757.
47. Ryan, T.A., and Smith, S.J. (1995). Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14, 983-989.
48. Ryan, T.A., Reuter, H., Wendlan, B., Schweizer, F.E., Tsien, R.W., and Smith, S.J. (1993). The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11, 713-724.
49. Sheng, Z.-H., Rettig, J., Takahashi, M., and Catterall, W.A. (1994). Identification of a syntaxin-binding site on N-type calcium channels. Neuron 13, 1303-1313.
50. Smith, S.J., and Augustine, G.J. (1988). Calcium ions, active zones and synaptic transmitter release. Trends Neurosci. 11, 458-464.
51. Smith, S.J., Buchanan, J., Osses, L.R., Charlton, M.P., and Augustine, G.J. (1993). The spatial distribution of calcium signals in squid presynaptic terminals. J. Physiol. (Lond.) 472, 573-593.
52. Sorra, K.E., and Harris, K.M. (1993). Occurrence and three-dimensional structure of multiple synapses between individual radium axons and their target pyramidal cells in hippocampal area CA1. J. Neurosci. 13, 3736-3748.
53. Spruston, N., Schiller, Y., Stuart, G., and Sakmann, B. (1995). Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268, 297-300.
54. Stevens, C.F., and Wang, Y. (1994). Changes in reliability of synaptic function as a mechanism for plasticity. Nature 371, 704-707.
55. Stevens, C.F., and Wang, Y. (1995). Facilitation and depression at single central synapses. Neuron 14, 795-802.
56. Stuart, G.J., and Sakmann, B. (1994). Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367, 69-72.
57. Takahashi, T., and Momiyama, A. (1993). Different types of calcium channels mediate central synaptic transmission. Nature 366, 156-158.
58. Toth, P.T., Bindokas, V., Bleakman, D., Colmers, W.F., and Miller, R.J. (1993). Mechanism of presynaptic inhibition by neuropeptide Y at sympathetic nerve terminals. Nature 364, 635-639.
59. Volgushev, M., Voronin, L.L., Chistiakova, M., Artola, A., and Singer, W. (1995). All-or-none excitatory postsynaptic potentials in the rat visual cortex. Eur. J. Neurosci. 7, 1751-1760.
60. Wall, P.D. (1995). Do nerve impulses penetrate terminal arborizations? A pre-presynaptic control mechanism. Trends Neurosci. 18, 99-103.
61. 2+ channels in supporting hippocampal synaptic transmission. Science 264, 107-111.
62. Wu, L.-G., and Saggau, P. (1994a). Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J. Neurosci. 14, 5613-5622.
63. Wu, L.-G., and Saggau, P. (1994b). Adenosine inhibits evoked synaptic transmission primarily by reducing presynaptic calcium influx in area CA1 of hippocampus. Neuron 12, 1139-1148.
64. Wu, L.-G., and Saggau, P. (1994c). 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.
65. Yuste, R., and Denk, W. (1995). Dendritic spines as basic functional units of neuronal integration. Nature 375, 682-684.
66. Zar, J.H. (1984). Biostatistical Analysis (Englewood Cliffs, New Jersey: Prentice Hall).
67. Zucker, R.S. (1993). Calcium and transmitter release. J. Physiol. (Paris) 87, 25-36.