Calcium sensitivity of neurotransmitter release differs at phasic and tonic synapses

Journal of Neuroscience

Volumn 25, Issue 12, 2005, Pages 3113-3125

  Millar, Andrew G ^a   Zucker, Robert S ^b   Ellis Davies, Graham C R ^c   Charlton, Milton P ^a   Atwood, Harold L ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Ca2+ sensitivity; Crayfish; Neuromuscular junction; Priming; Synapse; Synaptic strength

Indexed keywords

CALCIUM;

ACTION POTENTIAL; ARTICLE; CALCIUM BINDING; CALCIUM CELL LEVEL; CRAYFISH; CRUSTACEA; EXTRACELLULAR CALCIUM; LEARNING; MEMORY; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NEUROTRANSMITTER RELEASE; PHOTOLYSIS; PRIORITY JOURNAL; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; ASTACOIDEA; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; EGTAZIC ACID; ELECTRIC STIMULATION; MODELS, BIOLOGICAL; NEUROMUSCULAR JUNCTION; NEUROTRANSMITTER AGENTS; PHOTOLYSIS; SYNAPSES; SYNAPTIC TRANSMISSION; TIME FACTORS; ULTRAVIOLET RAYS;

EID: 16244421360     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4717-04.2005     Document Type: Article

References (75)

1. 2+ channels mediate excitatory and inhibitory synaptic transmitter release in crayfish muscle. Proc Natl Acad Sci USA 91:4224-4228.
2. Atwood HL (1967) Variation in physiological properties of crustacean motor synapses. Nature 215:57-58.
3. Atwood HL, Bittner GD (1971) Matching of excitatory and inhibitory inputs to crustacean muscle fibers. J Neurophysiol 34:157-170.
4. Atwood HL, Karunanithi S (2002) Diversification of synaptic strength: presynaptic elements. Nat Rev Neurosci 3:497-516.
5. Augustine GI, Santamaria F, Tanaka K (2003) Local calcium signaling in neurons. Neuron 40:331-346.
6. Bai J, Chapman ER (2004) The C2 domains of synaptotagmin: partners in exocytosis. Trends Biochem Sci 29:143-151.
7. Beutner D, Voets T, Neher E, Moser T (2001) Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29:681-690.
8. Bittner GD (1968) Differentiation of nerve terminals in the crayfish opener muscle and its functional significance. J Gen Physiol 51:731-758.
9. 2+ buffer saturation underlies paired pulse facilitation in calbindin-D28k- containing terminals. Neuron 38:79-88.
10. Blundon JA, Wright SN, Brodwick MS, Bittner GD (1995) Presynaptic calcium-activated potassium channels and calcium channels at a crayfish neuromuscular junction. J Neurophysiol 73:178-189.
11. Bollmann JH, Sakmann B, Borst JG (2000) Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289:953-957.
12. Bradacs H, Cooper RL, Msghina M, Atwood HL (1997) Differential physiology and morphology of phasic and tonic motor axons in a crayfish limb extensor muscle. J Exp Biol 200:677-691.
13. Cooper RL, Stewart BA, Wojtowicz JM, Wang S, Atwood HL (1995) Quantal measurement and analysis methods compared for crayfish and Drosophila neuromuscular junctions and rat hippocampus. J Neurosci Methods 61:67-78.
14. 2+ and assembly with the core SNARE complex onto membranes. Neuron 24:363-376.
15. Delaney K, Tank DW, Zucker RS (1991) Presynaptic calcium and serotonin-mediated enhancement of transmitter release at crayfish neuromuscular junction. J Neurosci 11:2631-2643.
16. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995-1008.
17. Dudel J (1981) The effect of reduced calcium on quantal unit current and release at the crayfish neuromuscular junction. Pflügers Arch 391:35-40.
18. Duncan RR, Shipston MJ, Chow RH (2000) Double C2 protein: a review. Biochimie 82:421-426.
19. Ellis-Davies GC (2003) Development and application of caged calcium. Methods Enzymol 360:226-238.
20. Ellis-Davies GC, Kaplan JH, Barsotti RJ (1996) Laser photolysis of caged calcium: rates of calcium release by nitrophenyl-EGTA and DM-nitrophen. Biophys J 70:1006-1016.
21. Felmy F, Neher E, Schneggenburger R (2003) Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37:801-811.
22. Geppert M, Südhof TC (1998) RAB3 and synaptotagmin: the yin and yang of synaptic membrane fusion. Annu Rev Neurosci 21:75-95.
23. Grimes JH, Huggard AJ, Wilford SP (1963) The stabilities of the alkaline earth chelate of some polyaminopolycarboxylic acids. J Inororg Nucl Chem 25:1225-1238.
24. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260:3440-3450.
25. Heidelberger R, Matthews G (2004) Vesicle priming and depriming: a SNAP decision. Neuron 41:311-313.
26. Heidelberger R, Heinemann C, Neher E, Matthews G (1994) Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371:513-515.
27. Hilfiker S, Pieribone VA, Czernik AJ, Kao HT, Augustine GI, Greengard P (1999) Synapsins as regulators of neurotransmitter release. Philos Trans R Soc Lond B Biol Sci 354:269-279.
28. 2+ buffers on evoked release and on facilitation in the crayfish neuromuscular junction. Neurosci Lett 125:215-218.
29. Hua Y, Scheller RH (2001) Three SNARE complexes cooperate to mediate membrane fusion. Proc Natl Acad Sci USA 98:8065-8070.
30. 2+ and short-term synaptic plasticity. Nature 371:603-606.
31. 2+ binding kinetics of fura-2 and azo-1 from temperature-jump relaxation measurements. Biophys J 53:635-639.
32. Kennedy D, Takeda K (1965a) Reflex control of abdominal flexor muscles in the crayfish. I. The twitch system. J Exp Biol 43:211-227.
33. Kennedy D, Takeda K (1965b) Reflex control of abdominal flexor muscles in the crayfish. II. The tonic system. J Exp Biol 43:229-246.
34. King MJ, Atwood HL, Govind CK (1996) Structural features of crayfish phasic and tonic neuromuscular terminals. J Comp Neurol 372:618-626.
35. Llinás R, Steinberg IZ, Walton K (1981) Presynaptic calcium currents in squid giant synapse. Biophys J 33:289-321.
36. Llinas R, Sugimori M, Simon SM (1982) Transmission by presynaptic spike-like depolarization in the squid giant synapse. Proc Natl Acad Sci USA 79:2415-2419.
37. Lonart G (2002) RIM1: an edge for presynaptic plasticity. Trends Neurosci 25:329-332.
38. Markram H, Wang Y, Tsodyks M (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci USA 95:5323-5328.
39. Martin TF (2002) Prime movers of synaptic vesicle exocytosis. Neuron 34:9-12.
40. Matveev V, Sherman A, Zucker RS (2002) New and corrected simulations of synaptic facilitation. Biophys J 83:1368-1373.
41. Matveev V, Zucker RS, Sherman A (2004) Facilitation through buffer saturation: constraints on endogenous buffering properties. Biophys J 86:2691-2709.
42. Millar AG, Bradacs H, Charlton MP, Atwood HL (2002) Inverse relationship between release probability and readily releasable vesicles in depressing and facilitating synapses. J Neurosci 22:9661-9667.
43. 2A domain. FEBS Lett 516:93-96.
44. Msghina M, Govind CK, Atwood HL (1998) Synaptic structure and transmitter release in crustacean phasic and tonic motor neurons. J Neurosci 18:1374-1382.
45. Msghina M, Millar AG, Charlton MP, Govind CK, Atwood HL (1999) Calcium entry related to active zones and differences in transmitter release at phasic and tonic synapses. J Neurosci 19:8419-8434.
46. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20:389-399.
47. Neher E, Zucker RS (1993) Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10:21-30.
48. Oheim M, Naraghi M, Muller TH, Neher E ( 1998) Two dye two wavelength excitation calcium imaging: results from bovine adrenal chromaffin cells. Cell Calcium 24:71-84.
49. 2+ action on neuropeptide and acetylcholine release in Aplysia californica. J Physiol (Lond) 535:647-662.
50. 2+ and asynchronous transmitter release from the same crayfish bouton. J Physiol (Lond) 501:251-262.
51. ++-triggered exocytosis. Science 298:781-785.
52. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1:279-285.
53. Roberts WM (1994) Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci 14:3246-3262.
54. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J Physiol (Lond) 531:807-826.
55. Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. I Neurosci 17:5858-5867.
56. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889-893.
57. Stevens CF (2003) Neurotransmitter release at central synapses. Neuron 40:381-388.
58. Stevens CF, Sullivan JM (2003) The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39:299-308.
59. Tang Y, Schlumpberger T, Kim T, Lueker M, Zucker RS (2000) Effects of mobile buffers on facilitation: experimental and computational studies. Biophys J 78:2735-2751.
60. Tank DW, Regehr WG, Delaney KR (1995) A quantitative analysis of presynaptic calcium dynamics that contribute to short-term enhancement. J Neurosci 15:7940-7952.
61. Trommershäuser J, Schneggenburger R, Zippelius A, Neher E (2003) Heterogeneous presynaptic release probabilities: functional relevance for short-term plasticity. Biophys J 84:1563-1579.
62. Van der Kloot W (1988) Estimating the timing of quantal releases during end-plate currents at the frog neuromuscular junction. J Physiol (Lond) 402:595-603.
63. Wojtowicz JM, Atwood HL (1983) Maintained depolarization of synaptic terminals facilitates nerve-evoked transmitter release at a crayfish neuromuscular junction. J Neurobiol 14:385-390.
64. Wojtowicz JM, Atwood HL (1984) Presynaptic membrane potential and transmitter release at the crayfish neuromuscular junction. J Neurophysiol 52:99-113.
65. Wojtowicz JM, Marin L, Atwood HL (1994) Activity-induced changes in synaptic release sites at the crayfish neuromuscular junction. J Neurosci 14:3688-3703.
66. Worden MK, Bykhovskaia M, Hackett JT (1997) Facilitation at the lobster neuromuscular junction: a stimulus-dependent mobilization model. J Neurophysiol 78:417-428.
67. Wright SN, Brodwick MS, Bittner GD (1996) Presynaptic calcium currents at voltage-clamped excitor and inhibitor nerve terminals of crayfish. J Physiol (Lond) 496:347-361.
68. 2+ clearance in the cytosol of adrenal chromaffin cells. Biophys J 73:532-545.
69. Yamada WM, Zucker RS (1992) Time course of transmitter release calculated from simulations of a calcium diffusion model. Biophys J 61:671-682.
70. 2+ ATPase in post-tetanic potentiation at crayfish neuromuscular junctions. J Neurosci 21:9598-9607.
71. 2+. Methods Cell Biol 40:31-63.
72. Zucker RS (1992) Effects of photolabile calcium chelators on fluorescent calcium indicators. Cell Calcium 13:29-40.
73. Zucker RS (2003) NCS-1 stirs somnolent synapses. Nat Neurosci 6:1006-1008.
74. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.
75. Zucker RS, Kullmann DM, Bennett M (1999) Release of neurotransmitters. In: Fundamental neuroscience (Zigmond MJ, Bloom FL, Landis SC, Roberts JL, Squire LR, eds), pp 155-192. San Diego: Academic.