Persistent, exocytosis-independent silencing of release sites underlies homosynaptic depression at sensory synapses in Aplysia

Journal of Neuroscience

Volumn 22, Issue 5, 2002, Pages 1942-1955

  Gover, Tony D ^a   Jiang, Xue Ying ^a   Abrams, Thomas W ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Computer simulations; Serotonin induced facilitation; Silencing of release sites; Synaptic depression; Univesicular release; Vesicle depletion

Indexed keywords

CALCIUM ION; POTASSIUM CHANNEL; POTASSIUM CHANNEL BLOCKING AGENT; SEROTONIN;

APLYSIA; ARTICLE; CALCIUM TRANSPORT; COMPUTER SIMULATION; EXOCYTOSIS; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SYNAPSE;

EID: 0036522973     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-05-01942.2002     Document Type: Article

References (65)

1. Abbott LF, Varela JA, Sen K, Nelson SB (1997) Synaptic depression and cortical gain control. Science 275:220-224.
2. Adler EM, Augustine GJ, Duffy SN, Charlton MP (1991) Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J Neurosci 11:1496-1507.
3. Armitage BA, Siegelbaum SA (1998) Presynaptic induction and expression of homosynaptic depression at Aplysia sensorimotor neuron synapses. J Neurosci 18:8770-8779.
4. Auger C, Kondo S, Marty A (1998) Multivesicular release at single functional synaptic sites in cerebellar stellate and basket cells. J Neurosci 18:4532-4547.
5. Bailey CH, Chen M (1983) Morphological basis of long-term habituation and sensitization in Aplysia. Science 220:91-93.
6. Bailey CH, Chen M (1988) Morphological basis of short-term habituation in Aplysia, J Neurosci 8:2452-2459.
7. Baxter DA, Byrne JH (1990) Differential effects of cAMP and serotonin on membrane current, action-potential duration, and excitability in somata of pleural sensory neurons of Aplysia. J Neurophysiol 64:978-990.
8. Betz WJ (1970) Depression of transmitter release at the neuromuscular junction of the frog. J Physiol (Lond) 206:629-644.
9. Brody DL, Yue DT (2000) Release-independent short-term synaptic depression in cultured hippocampal neurons. J Neurosci 20:2480-2494.
10. Byrne JH (1982) Analysis of synaptic depression contributing to habituation of gill-withdrawal reflex in Aplysia californica. J Neurophysiol 48:431-438.
11. Byrne JH, Kandel ER (1996) Presynaptic facilitation revisited: State and time dependence. J Neurosci 16:425-435.
12. Canepari M, Cherubini E (1998) Dynamics of excitatory transmitter release: Analysis of synaptic responses in CA3 hippocampal neurons after repetitive stimulation of afferent fibers. J Neurophysiol 79:1977-1988.
13. Carroll RC, Lissin DV, von Zastrow M, Nicoll RA, Malenka RC (1999) Rapid redistribution of glutamate receptors contributes to long-term depression in hippocampal cultures. Nat Neurosci 2:454-460.
14. Castellucci VF, Kandel ER (1974) A quantal analysis of the synaptic depression underlying habituation of the gill-withdrawal reflex in Aplysia, Proc Natl Acad Sci USA 71:5004-5008.
15. Cohen TE, Kaplan SW, Kandel ER, Hawkins RD (1997) A simplified preparation for relating cellular events to behavior: Mechanisms contributing to habituation, dishabituation, and sensitization of the Aplysia gill-withdrawal reflex. J Neurosci 17:2886-2899.
16. Debanne D, Guerineau NC, Gahwiler BH, Thompson SM (1996) Paired-pulse facilitation and depression at unitary synapses in rat hippocampus: Quantal fluctuation affects subsequent release. J Physiol (Lond) 491:163-176.
17. 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.
18. Dobrunz LE, Huang EP, Stevens CF (1997) Very short-term plasticity in hippocampal synapses. Proc Natl Acad Sci USA 94:14843-14847.
19. 2+ influx in presynaptic facilitation. Nature 361:634-637.
20. Eliot LS, Kandel ER, Hawkins RD (1994) Modulation of spontaneous transmitter release during depression and posttetanic potentiation of Aplysia sensory-motor neuron synapses isolated in culture. J Neurosci 14:3280-3292.
21. Elmqvist D, Quastel DM (1965) A quantitative study of end-plate potentials in isolated human muscle. J Physiol (Lond) 178:505-529.
22. Faber DS (1998) Synaptic depression at an identified central synapse: Evidence for different constraints on evoked and spontaneous quanta. In: Central Synapses: Quantal Mechanisms and Plasticity (Faber DS, Korn H, Redman SJ, Thompson SM, Altman JS, eds), pp 158-168. Strasbourg: Human Frontier Science Program.
23. Faber DS, Young WS, Legendre P, Korn H (1992) Intrinsic quantal variability due to stochastic properties of receptor-transmitter interactions. Science 258:1494-1498.
24. Fogelson AL, Zucker RS (1985) Presynaptic calcium diffusion from various arrays of single channels. Implications for transmitter release and synaptic facilitation. Biophys J 48:1003-1017.
25. Geppert M, Goda Y, Stevens CF, Sudhof TC (1997) The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature 387:810-814.
26. Gingrich KJ, Byrne JH (1985) Simulation of synaptic depression, post-tetanic potentiation, and presynaptic facilitation of synaptic potentials from sensory neurons mediating gill-withdrawal reflex in Aplysia. J Neurophysiol 53:652-669.
27. Goldsmith BA, Abrams TW (1991) Reversal of synaptic depression by serotonin at Aplysia sensory neuron synapses involves activation of adenylyl cyclase. Proc Nad Acad Sci USA 88:9021-9025.
28. Goldsmith BA, Abrams TW (1992) cAMP modulates multiple K+ currents, increasing spike duration and excitability in Aplysia sensory neurons. Proc Natl Acad Sci USA 89:11481-11485.
29. Hatt H, Smith DO (1976) Synaptic depression related to presynaptic axon conduction block. J Physiol (Lond) 259:367-393.
30. Heidelberger R, Heinemann C, Neher E, Matthews G (1994) Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371:513-515.
31. Hessler NA, Shirke AM, Malinow R (1993) The probability of transmitter release at a mammalian central synapse. Nature 366:569-572.
32. Hochner B, Klein M, Schacher S, Kandel ER (1986a) Action potential duration and the modulation of transmitter release from the sensory neurons of Aplysia in presynaptic facilitation and behavioral sensitization. Proc Natl Acad Sci USA 83:8410-8414.
33. Hochner B, Klein M, Schacher S, Kandel ER (1986b) Additional component in the cellular mechanism of presynaptic facilitation contributes to behavioral dishabituation in Aplysia. Proc Natl Acad Sci USA 83:8794-8798.
34. Hsu SF, Augustine GJ, Jackson MB (1996) Adaptation of Ca(2+)-triggered exocytosis in presynaptic terminals. Neuron 17:501-512.
35. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: Implications for the expression of LTP. Neuron 15:427-434.
36. Jiang XY, Abrams TW (1998) Use-dependent decline of paired-pulse facilitation atAplysia sensory neuron synapses suggests a distinct vesicle pool or release mechanism. J Neurosci 18:10310-10319.
37. Kandler K, Katz LC, Kauer JA (1998) Focal photolysis of caged glutamate produces long-term depression of hippocampal glutamate receptors. Nat Neurosci 1:119-123.
38. Kim J, Alger BE (2001) Random response fluctuations lead to spurious paired-pulse facilitation. J Neurosci 21:9608-9618.
39. Korn H, Mallet A, Triller A, Faber DS (1982) Transmission at a central inhibitory synapse. II. Quantal description of release, with a physical correlate for binomial n. J Neurophysiol 48:679-707.
40. Korn H, Faber DS, Burnod Y, Triller A (1984) Regulation of efficacy at central synapses. J Neurosci 4:125-130.
41. Korn H, Sur C, Charpier S, Legendre P, Faber DS (1994) The one-vesicle hypothesis and multivesicular release. Adv Second Messenger Phosphoprotein Res 29:301-322.
42. Kruk PJ, Korn H, Faber DS (1997) The effects of geometrical parameters on synaptic transmission: A Monte Carlo simulation study. Biophys J 73:2874-2890.
43. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404.
44. Lin XY, Glanzman DL (1996) Long-term depression of Aplysia sensorimotor synapses in cell culture: Inductive role of a rise in postsynaptic calcium. J Neurophysiol 76:2111-2114.
45. Liu G, Choi S, Tsien RW (1999) Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22:395-409.
46. Llinas R, Sugimori M, Silver RB (1992) Microdomains of high calcium concentration in a presynaptic terminal. Science 256:677-679.
47. Matveev V, Wang XJ (2000) Implications of all-or-none synaptic transmission and short-term depression beyond vesicle depletion: A computational study. J Neurosci 20:1575-1588.
48. Melkonian DS (1993) Transient analysis of a chemical synaptic transmission. Biol Cybern 68:341-350.
49. Murthy VN, Sejnowski TJ, Stevens CF (1997) Heterogeneous release properties of visualized individual hippocampal synapses. Neuron 18:599-612.
50. Narasimhan K, Linden DJ (1996) Defining a minimal computational unit for cerebellar long-term depression. Neuron 17:333-341.
51. Patil PG, Brody DL, Yue DT (1998) Preferential closed-state inactivation of neuronal calcium channels. Neuron 20:1027-1038.
52. Redman RS, Silinsky EM (1994) ATP released together with acetylcholine as the mediator of neuromuscular depression at frog motor nerve endings. J Physiol (Lond) 477:117-127.
53. Redman S (1990) Quantal analysis of synaptic potentials in neurons of the central nervous system. Physiol Rev 70:165-198.
54. Roberts WM, Jacobs RA, Hudspeth AJ (1991) The hair cell as a presynaptic terminal. Ann NY Acad Sci 635:221-233.
55. Rosenmund C, Clements JD, Westbrook GL (1993) Nonuniform probability of glutamate release at a hippocampal synapse. Science 262:754-757.
56. Royer S, Coulson RL, Klein M (2000) Switching off and on of synaptic sites at Aplysia sensorimotor synapses. J Neurosci 20:626-638.
57. Stevens CF, Wang Y (1995) Facilitation and depression at single central synapses. Neuron 14:795-802.
58. Sugita S, Baxter DA, Byrne JH (1997) Differential effects of 4-aminopyridine, serotonin, and phorbol esters on facilitation of sensorimotor connections in Aplysia. J Neurophysiol 77:177-185.
59. Thies RE (1965) Neuromuscular depression and the apparent depletion of transmitter in mammalian muscle. J Neurophysiol 28:427-442.
60. Trussell LO, Zhang S, Raman IM (1993) Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10:1185-1196.
61. Varela JA, Sen K, Gibson J, Fost J, Abbott LF, Nelson SB (1997) A quantitative description of short-term plasticity at excitatory synapses in layer 2/3 of rat primary visual cortex. J Neurosci 17:7926-7940.
62. 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.
63. Wojtowicz JM, Marin L, Atwood HL (1994) Activity-induced changes in synaptic release sites at the crayfish neuromuscular junction. J Neurosci 14:3688-3703.
64. Yamada WM, Zucker RS (1992) Time course of transmitter release calculated from simulations of a calcium diffusion model. Biophys J 61:671-682.
65. Zucker RS, Bruner J (1977) Long-lasting depression and the depletion hypothesis at crayfish neuromuscular junctions. J Comp Physiol 121:223-240.