Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons

Journal of Neuroscience

Volumn 19, Issue 15, 1999, Pages 6427-6438

  Prange, Oliver ^a   Murphy, Timothy H ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Calcium; Evoked; Miniature; Pool size; Probability; Release; Synapse; Vesicle

Indexed keywords

FLUORESCENT DYE;

ANIMAL CELL; ARTICLE; BRAIN CORTEX; CONTROLLED STUDY; EVOKED RESPONSE; FETUS; MINIATURE ENDPLATE POTENTIAL; NERVE POTENTIAL; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0033179082     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-15-06427.1999     Document Type: Article

References (88)

1. Arancio O, Kandel ER, Hawkins RD (1995) Activity-dependent long-term enhancement of transmitter release by presynaptic 3′,5′-cyclic GMP in cultured hippocampal neurons. Nature 376:74-80.
2. Baba H, Kohno T, Okamoto M, Goldstein PA, Shimoji K, Yoshimura M (1998) Muscarinic facilitation on GABA release in substantia gelatinosa of the rat spinal dorsal horn. J Physiol (Lond) 508:83-93.
3. Bailey CH, Kandel ER (1993) Structural changes accompanying memory storage. Annu Rev Physiol 55:397-426.
4. 2+ channels governing generation of miniature and evoked excitatory synaptic currents in spinal laminae 1 and 2. J Neurosci 18:8740-8750.
5. Betz WJ, Bewick GS (1992) Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255:200-203.
6. Betz WJ, Bewick GS (1993) Optical monitoring of transmitter release and synaptic vesicle recycling at the frog neuromuscular junction. J Physiol (Lond) 460:287-309.
7. Betz WJ, Mao F, Smith CB (1996) Imaging exocytosis and endocytosis, Curr Opin Neurobiol 6:365-371.
8. Buchs PA, Müller D (1996) Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. Proc Natl Acad Sci USA 93:8040-8045.
9. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: state and time dependence. J Neurosci 16:425-435.
10. Calverley RK, Jones DG (1990) Contributions of dendritic spines and perforated synapses to synaptic plasticity. Brain Res Brain Res Rev 15:215-249.
11. Capogna M, Gähwiler BH, Thompson SM (1995) Presynaptic enhancement of inhibitory synaptic transmission by protein kinase A and C in the rat hippocampus. J Neurosci 15:1249-1260.
12. Capogna M, Gähwiler BH, Thompson SM (1996a) Presynaptic inhibition of calcium-dependent and -independent release elicited with ionomycin, gadolinium, and α-latrotoxin in the hippocampus. J Neurophysiol 75:2017-2028.
13. Capogna M, Gähwiler BH, Thompson SM (1996b) Calcium-independent actions of α-latrotoxin on spontaneous and evoked synaptic transmission in the hippocampus. J Neurophysiol 76:3149-3158.
14. 2+ partially rescues synaptic transmission in hippocampal cultures treated with botulinum toxin A and C, but not tetanus toxin. J Neurosci 17:7190-7202.
15. Carroll R, Nicoll RA, Malenka RC (1998) Effect of PKA and PKC on miniature excitatory postsynaptic currents in CA1 pyramidal cells. J Neurophysiol 80:2797-2800.
16. Ceccarelli B, Hurlbut WP, lezzi N (1988) Effect of α-latrotoxin on the frog neuromuscular junction at low temperature. J Physiol (Lond) 402:195-217.
17. Chavez-Noriega LE, Stevens CF (1994) Increased transmitter release at excitatory synapses produced by direct activation of adenylate cyclase in rat hippocampal slices. J Neurosci 14:310-317.
18. Chavis P, Mollard P, Bockaert J, Manzoni O (1998) Visualization of cyclic AMP-regulated presynaptic activity at cerebellar granule cells. Neuron 20:773-781.
19. Chen C, Regehr WG (1997) The mechanism of cAMP-mediated enhancement at a cerebellar synapse. J Neurosci 22:8687-8694.
20. Cormier RJ, Kelly PT (1996) Glutamate-induced long-term potentiation enhances spontaneous EPSC amplitude but not frequency. J Neurophysiol 75:1909-1918.
21. Cummings DD, Wilcox KS, Dichter MA (1996) Calcium-dependent paired-pulse facilitation of miniature EPSC frequency accompanies depression of EPSCs at hippocampal synapse in culture. J Neurosci 16:531-523.
22. Deitcher DL, Ueda A, Stewart BA, Burgess RW, Kidokoro Y, Schwarz TL (1998) Distinct requirements for evoked and spontaneous release of neurotransmitter are revealed by mutations in the Drosophila gene neuronal-synaptobrevin. J Neurosci 18:2028-2039.
23. Dittman JS, Regehr WG (1996) Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J Neurosci 16:1623-1633.
24. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation and depletion at central synapses. Neuron 18:995-1008.
25. Dodge FA, Rahamimoff R (1967) Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J Physiol (Lond) 193:419-432.
26. B receptor-mediated inhibition of GABA release in area CA1 of the rat hippocampus. J Neurophysiol 74:43-53.
27. Edwards FA (1995) Anatomy and electrophysiology of fast central synapses lead to a structural model for long-term potentiation. Physiol Rev 75:759-787.
28. Fisher SA, Fischer TM, Carew TJ (1997) Multiple overlapping processes underlying short-term synaptic enhancement. Trends Neurosci:170-177.
29. Frerking M, Borges S, Wilson M (1997) Are some minis multiquantal? J Neurophysiol 78:1293-1304.
30. 2+-triggered synaptic vesicle exocytosis and clathrinmediated endocytosis at a central synapse. Neuron 21:607-616.
31. Ghiradi M, Braha O, Hochner B, Montarolo PG, Kandel ER, Dale N (1992) Roles of PKA and PKC in facilitation of evoked and spontaneous transmitter release at depressed and nondepressed synapses in Aplysia sensory neurons. Neuron 9:479-489.
32. Gottmann K, Pfrieger FW, Lux HD (1994) The formation of glutamatergic synapses in cultured central neurons: selective increase in miniature synaptic currents. Brain Res Dev Brain Res 81:77-88.
33. 2+ channels types triggering GABA release onto medial preoptic neurons from rat. J Physiol (Lond) 507:77-91.
34. Hamill OP, Marty A, Neher E, Sakmann B, Sigworth F (1981) Improved patch-clamp techniques for high resolution current recordings from cells and cell free membrane patches. Pflügers Arch 391:85-100.
35. Harris KM, Sultan P (1995) Variation in the number, location and size of synaptic vesicles provides an anatomical basis for the nonuniform probability of release at hippocampal CA1 synapses. Neuropharmacology 34:1387-1395.
36. Hell JW, Yokoyama CT, Breeze LJ, Chavkin C, Catterall WA (1995) Phosphorylation of presynaptic and postsynaptic calcium channels by cAMP-dependent protein kinase in hippocampal neurons. EMBO J 14:3036-3044.
37. Henkel AW, Lübke J, Betz WJ (1996) FM1-43 dye ultrastructural localization in and release from frog motor nerve terminals. Proc Natl Acad Sci USA 93:1918-1923.
38. Hua SY, Raciborska DA, Trimble WS, Charlton MP (1998) Different VAMP/Synaptobrevin complexes for spontaneous and evoked transmitter release at the crayfish neuromuscular junction. J Neurophysiol 80:3233-3246.
39. 2+ and short-term synaptic plasticity. Nature 371:603-606.
40. 2+ channel blockers on transmitter release and presynaptic currents at the for neuromuscular junction. J Physiol (Lond) 486:695-706.
41. Kondo S, Marty A (1997) Protein kinase A-mediated enhancement of miniature IPSC frequency by noradrenaline in rat cerebellar stellate cells. J Physiol (Lond) 498:165-176.
42. Kondo S, Marty A (1998) Differential effects of noradrenaline on evoked, spontaneous and miniature IPSCs in rat cerebellar stellate cells. J Physiol (Lond) 509:233-243.
43. Leahy JC, Luo Y, Kent CS, Meiri KF, Vallano ML (1993) Demonstration of presynaptic protein kinase C activation following long-term potentiation in rat hippocampus. Neuroscience 52:563-574.
44. Levenes C, Daniel H, Soubrie P, Crepel F (1998) Cannabinoids decrease excitatory synaptic transmission and impair long-term depression in rat cerebellar Purkinje cells. J Physiol (Lond) 510:867-879.
45. Li YX, Zhang Y, Lester HA, Schuman EM, Davidson N (1998) Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J Neurosci 18:10231-10240.
46. Lisman JE, Harris KM (1993) Quantal analysis and synaptic anatomy-integrating two views of hippocampal plasticity. Trends Neurosci 16:141-147.
47. Liu G, Tsien RW (1995) Properties of synaptic transmission at single hippocampal boutons. Nature 375:404-408.
48. Lonart G, Südhof TC (1998) Region specific phosphorylation of rabphilin in mossy fiber nerve terminals of the hippocampus. J Neurosci 18:634-640.
49. Ma L, Zablow L, Kandel ER, Siegelbaum SA (1999) Cyclic AMP induces functional presynaptic boutons in hippocampal CA3-CA1 cultures. Nature Neurosci 2:24-30.
50. 2+ imaging of CNS axons in culture indicates reliable coupling between single action potentials and distal functional release sites. Neuron 16:783-795.
51. Mackenzie PJ, Kenner GS, Prange O, Shayan H, Umemiya M, Murphy TH (1999) Ultrastructural correlates of quantal synaptic function at single CNS synapses. J Neurosci 19:RC13(1-7).
52. Majewski H, Iannazzo L (1998) Protein kinase C: a physiological mediator of enhanced transmitter output. Prog Neurobiol 55:463-475.
53. Malenka RC, Madison DV, Nicoll RA (1986) Potentiation of synaptic transmission in the hippocampus by phorbol esters. Nature 321:175-177.
54. Malgaroli A, Tsien RW (1992) Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons. Nature 357:134-139.
55. Marcus DS, Kriebel ME, Hanna RB (1992) Effects of calcium on the dynamic process of transmitter release which generates either skew- or bell MEPPS. Brain Res 593:185-196.
56. Matthews G, Wickelgren WO (1977) On the effects of calcium on the frequency of miniature end-plate potentials at the frog neuromuscular junction. J Physiol (Lond) 266:91-101.
57. McKinney RA, Capogna M, Dürr R, Gähwiler BH, Thompson SM (1999) Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci 2:44-49.
58. 2+ in bull frog sympathetic ganglia. J Physiol (Lond) 435:421-438.
59. Mochida S, Fukuda M, Niinobe M, Kobayashi H, Mikoshiba K (1997) Roles of synaptotagmin C2 domains in neurotransmitter secretion and inositol high-polyphosphate binding at mammalian cholinergic synapses. Neuroscience 77:937-943.
60. Momiyama A, Takahashi T (1994) Calcium channels responsible for potassium-induced transmitter release at rat cerebellar synapse. J Physiol (Lond) 476:197-202.
61. Murphy TH, Baraban JM, Wier WG, Blatter LA (1994) Visualization of quantal synaptic transmission by dendritic calcium imaging. Science 263:529-532.
62. Murphy TH, Baraban JM, Wier WG (1995) Mapping miniature synaptic currents to single synapses using calcium imaging reveals heterogeneity in postsynaptic output. Neuron 15:159-168.
63. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18:599-612.
64. O'Brien RJ, Mammen AL, Blackshaw S, Ehlers MD, Rothstein JD, Huganir RL (1997) The development of excitatory synapses in cultured spinal neurons. J Neurosci 19:7339-7350.
65. Parfitt KD, Madison DV (1993) Phorbol esters enhance synaptic transmission by a presynaptic, calcium-dependent mechanisms in rat hippocampus. J Physiol (Lond) 471:245-268.
66. 2+ dependence of spontaneous IPSCs. J Neurosci 16:4835-4845.
67. Prange O, Murphy TM (1997) FM1-43 as an indicator for miniature synaptic activity at single synapses of cortical neurons. Soc Neurosci Abstr 23:2272.
68. Prange O, Murphy TM (1998) Comparison of evoked and miniature release at single CNS synapses in culture. Soc Neurosci Abstr 24:226.
69. Prange O, Murphy TM (1999) An analysis of multiquantal transmitter release from single cultured cortical neuron terminals. J Neurophysiol 81:1810-1817.
70. Ramakers GM, Pasinelli P, Hens JJ, Gispen WH, De Graan PN (1997) Protein kinase C in synaptic plasticity: changes in the in situ phosphorylation state of identified pre- and postsynaptic substrates. Prog Neuropsychopharmacol Biol Psychiatry 21:455-486.
71. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1220.
72. Rouze NC, Schwartz EA (1998) Continuous and transient vesicle cycling at a ribbon synapse. J Neurosci 18:8614-8624.
73. Rusakov DA, Davies HA, Harrison E, Diana G, Richter-Levin G, Bliss TV, Stewart MG (1997) Ultrastructural synaptic correlates of spatial learning in rat hippocampus. Neuroscience 80:69-77.
74. Ryan TA, Smith SJ (1995) Vesicle pool mobilization during action potential firing at hippocampal synapses. Neuron 14:983-989.
75. Ryan TA, Reuter H, Wendland B, Schweizer FE, Tsien RW, Smith SJ (1993) The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11:725-738.
76. Ryan TA, Reuter H, Smith SJ (1997) Optical detection of a quantal presynaptic membrane turnover. Nature 388:478-482.
77. 2+ channels involved? Neuropharmacology 34:1549-1557.
78. Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867.
79. Schoppa NE, Westbrook GL (1997) Modulation of mEPSCs in olfactory bulb mitral cells by metabotropic glutamate receptors. J Neurophysiol 78:1468-1475.
80. Smith CB, Betz WJ (1996) Simultaneous independent measurements of endocytosis and exocytosis. Nature 380:531-534.
81. Stevens CF, Sullivan JM (1998) Regulation of the readily releasable vesicle pool by protein kinase C. Neuron 21:885-893.
82. Tong G, Malenka RC, Nicoll RA (1996) Long-term potentiation in cultures of single hippocampal granule cells: a presynaptic form of plasticity. Neuron 16:1147-1157.
83. Trudeau LE, Doyle RT, Emery DG, Haydon PG (1996) Calcium-independent activation of the secretory apparatus by ruthenium red in hippocampal neurons: a new tool to assess modulation of presynaptic function. J Neurosci 16:46-54.
84. Vautrin J, Barker JL (1995) How can exocytosis account for the actual properties of miniature synaptic signals? Synapse 19:144-149.
85. Villacres EC, Wong ST, Chavkin C, Storm DR (1998) Type 1 adenylyl cyclase mutant mice have impaired mossy fiber long-term potentiation. J Neurosci 19:3186-3194.
86. Wall MJ, Usowicz MM (1998) Development of quantal properties of evoked and spontaneous synaptic currents at a brain synapse. Nat Neurosci 8:675-682.
87. Wang S, Prange O, Murphy TH (1999) Amplification of calcium signals at dendritic spines provides a method for CNS quantal analysis. Can J Physiol Pharmacol, in press.
88. Zucker RS (1996) Exocytosis: a molecular and physiological perspective. Neuron 17:1049-1055.