Inverse relationship between release probability and readily releasable vesicles in depressing and facilitating synapses

Journal of Neuroscience

Volumn 22, Issue 22, 2002, Pages 9661-9667

  Millar, Andrew G ^a   Bradacs, Haymo ^a   Charlton, Milton P ^a   Atwood, Harold L ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Crustacean; Exocytosis; Glutamatergic; Phasic; Presynaptic; Quantal content; Rapid depletion; Release probability; Synaptic differentiation; Tonic

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; EXCITATION; EXOCYTOSIS; MEASUREMENT; MOTONEURON; NERVE CELL; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; STIMULATION; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION; TISSUE CULTURE;

EID: 0037112065     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-22-09661.2002     Document Type: Article

References (46)

1. Atwood HL, Lang F (1973) Differential responses of crab neuromuscular synapses to cesium ion. J Gen Physiol 61:747-766.
2. Atwood HL, Wojtowicz JM (1986) Short-term and long-term plasticity and physiological differentiation of crustacean motor synapses. Int Rev Neurobiol 28:275-362.
3. Atwood HL, Wojtowicz JM (1999) Silent synapses in neural plasticity: Current evidence. Learn Mem 6:542-571.
4. Atwood HL, Karunanithi S, Wong K, Marin L, Stewart BA (1999) Determinants of quantal size at Drosophila synapses: Bouton type, vesicle size, and the size of the postsynaptic receptor patch. Soc Neurosci Abstr 25:475.
5. Bollmann JH, Sakmann B, Borst JGG (2000) Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289:953-957.
6. 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.
7. Cooper RL, Marin L, Atwood HL (1995a) Synaptic differentiation of a single motor neuron: Conjoint definition of transmitter release, presynaptic calcium signals, and ultrastructure. J Neurosci 15:4209-4222.
8. Cooper RL, Stewart BA, Wojtowicz JM, Wang S, Atwood HL (1995b) Quantal measurement and analysis methods compared for crayfish and Drosophila neuromuscular junctions, and rat hippocampus. J Neurosci Methods 61:67-78.
9. del Castillo J, Katz B (1954) Statistical factors involved in neuromuscular facilitation and depression. J Physiol (Lond) 124:574-585.
10. Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147-6162.
11. Dittman JS, Kreitzer AC, Regehr WG (2000) Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J Neurosci 20:1374-1385.
12. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995-1008.
13. Dudel J (1981) The effect of reduced calcium on quantal unit current and release at the crayfish neuromuscular junction. Pflügers Arch 391:35-40.
14. Dudel J, Franke CH, Hatt H (1990) Rapid activation, desensitization, and resensitization of synaptic channels of crayfish muscle after glutamate pulses. Biophys J 57:533-545.
15. Eccles JC, Llinás R, Sasaki K (1966) The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum. J Physiol (Lond) 182:268-296.
16. Elmquist D, Quastel DMJ (1965) A quantitative study of end-plate potentials in isolated human muscle. J Physiol (Lond) 178:505-529.
17. Hanse E, Gustafsson B (2001) Factors explaining heterogeneity in short-term synaptic dynamics of hippocampal glutamatergic synapses in the neonatal rat. J Physiol (Lond) 5371:141-149.
18. Heidelberger R, Heinemann C, Neher E, Matthews G (1994) Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371:513-515.
19. Hubbard JI, Llinas R, Quastel DMJ (1969) Electrophysiological Analysis of Synaptic Transmission. London: Edward Arnold.
20. Jahromi SS, Atwood HL (1974) Three-dimensional ultrastructure of the crayfish neuromuscular apparatus. J Cell Biol 63:599-613.
21. Kennedy D, Takeda K (1965a) Reflex control of abdominal flexor muscles in the crayfish. I. The twitch system. J Exp Biol 43:211-227.
22. Kennedy D, Takeda K (1965b) Reflex control of abdominal flexor muscles in crayfish. II. The tonic system. J Exp Biol 43:229-246.
23. King MJR, Atwood HL, Govind CK (1996) Structural features of crayfish phasic and tonic neuromuscular junctions. J Comp Neurol 372:618-626.
24. Klenchin VA, Martin TF (2000) Priming in exocytosis: Attaining fusion-competence after vesicle docking. Biochimie 82:399-407.
25. Konnerth A, Llano I, Armstrong CM (1990) Synaptic currents in cerebellar Purkinje cells. Proc Natl Acad Sci USA 87:2662-2665.
26. Lnenicka GA, Atwood HL (1985) Age-dependent long-term adaptation of crayfish phasic motor axon synapses to altered activity. J Neurosci 5:459-467.
27. Lnenicka GA, Hong SJ (1997) Activity-dependent changes in voltage-dependent calcium currents and transmitter release. Mol Neurobiol 14:1-31.
28. Lnenicka GA, Atwood HL, Marin L (1986) Morphological transformation of synaptic terminals of a phasic motoneuron by long-term tonic stimulation. J Neurosci 6:2252-2258.
29. McNaughton BL (1980) Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res 199:1-19.
30. Msghina M, Atwood HL (1997) Distribution and morphology of inhibitory innervation in crayfish limb and abdominal muscles. Cell Tissue Res 290:111-118.
31. Msghina M, Govind CK, Atwood HL (1998) Synaptic structure and transmitter release in crustacean phasic and tonic motor neurons. J Neurosci 18:1374-1382.
32. 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.
33. Parsegian VA (1977) Considerations in determining the mode of influence of calcium on vesicle-membrane interaction. In: Society for Neuroscience Symposia, Vol II, Approaches to the Cell Biology of Neurons (Cowan WW, Ferrendelli JA, eds), pp 161-171. Bethesda, MD: Society for Neuroscience.
34. Quigley PA, Msghina M, Govind CK, Atwood HL (1999) Visible evidence for differences in synaptic effectiveness with activity-dependent vesicular uptake and release of FM1-43. J Neurophysiol 81:356-370.
35. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207.
36. Schikorski T, Stevens CF (1997) Quantitative ultrastructural analysis of hippocampal excitatory synapses. J Neurosci 17:5858-5867.
37. Schikorski T, Stevens CF (1999) Quantitative fine-structural analysis of olfactory cortical synapses. Proc Natl Acad Sci USA 96:4107-4112.
38. Schikorski T, Stevens CF (2001a) Morphological correlates of functionally defined synaptic vesicle pools. Soc Neurosci Abstr 27:1009.
39. Schikorski T, Stevens CF (2001b) Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4:391-395.
40. Schneggenburger R, Neher E (2000) Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889-983.
41. Schneggenburger R, Meyer AC, Neher E (1999) Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23:399-409.
42. Stevens CF, Tsujimoto T (1995) Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci USA 92:846-849.
43. Von Gersdorff H, Schneggenburger R, Weis S, Neher E (1997) Presynaptic depression at a calyx synapse: The small contribution of metabotropic glutamate receptors. J Neurosci 17:8137-8146.
44. Wang L-Y, Kaczmarek LK (1998) High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394:384-388.
45. Wojtowicz JM, Marin L, Atwood HL (1994) Activity-induced changes in synaptic release sites at the crayfish neuromuscular junction. J Neurosci 14:3688-3702.
46. Xu-Friedman MA, Harris KM, Regehr WG (2001) Three-dimensional comparison of ultrastructural characteristics at depressing and facilitating synapses onto cerebellar Purkinje cells. J Neurosci 21:6666-6672.