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Quantal stores of excitatory transmitter in nerve-muscle synapses of crayfish evaluated from high-frequency asynchronous quantal release induced by veratridine or high concentrations of potassium

  • Excitable Tissues and Central Nervous Physiology
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Abstract

At single voltage-clamped opener muscle fibres of crayfish claw, 10–100 μmol/l veratridine increased within a few seconds the rate of asynchronous quantal release, ñ, of excitatory transmitter from ñ<1 quantum/s to ñ≃10,000 quanta/s. Thereafter ñ declined exponentially either with a single, τ(2)≃50 s, or with two time constants τ(1)≃19 s, τ(2)≃50 s. In total (t→∞), about 0.3 million quanta were released by veratridine in a single short fibre of about 1 mm length. These values were estimated by means of the noise analysis technique and they agreed with equivalent parameters of release when 100 mmol/l K+ were used as release stimulus. Strong quantal release could be elicited only once in a single muscle by veratridine. Furthermore, the effect of veratridine on quantal release could be completely prevented by pretreatment with tetrodotoxin. In another nerve-muscle preparation of crayfish, the abdominal superficial extensor muscle, up to 3 million excitatory quanta could be released by veratridine in a single fibre. In the latter muscle veratridine-induced asynchronous quantal release was strongly dependent on the extracellular concentration of Ca2+ whereas in the claw opener dependence of quantal release on extracellular Ca2+ was negligible.

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References

  • Atwood HL (1973) An attempt to account for the diversity of crustacean muscles. Am Zool 13:357–378

    Google Scholar 

  • Atwood HL, Swenarchuk LE, Gruenwald CR (1975) Long-term synaptic facilitation during sodium accumulation in nerve terminals. Brain Res 100:198–204

    Google Scholar 

  • Atwood HL, Charlton MP, Thompson CS (1983) Neuromuscular transmission in crustaceans is enhanced by a sodium ionophore, monensin, and by prolonged stimulation. J Physiol (Lond) 335:179–195

    Google Scholar 

  • Birks RI, Cohen MW (1968a) The action of sodium pump inhibitors on neuromuscular transmission. Proc R Soc London B: 381–399

    Google Scholar 

  • Birks RI, Cohen MW (1968b) The influence of internal sodium on the behaviour of motor nerve endings. Proc Roy Soc Lond [Biol]:401–421

  • Carafoli E, Crompton M (1978) The regulation of intracellular calcium by mitochondria. Ann NY Acad Sci USA 307:269–284

    Google Scholar 

  • Cull-Candy SG, Miledi R (1982) Properties of miniature excitatory junctional currents at the locust nerve-muscle junction. J Physiol (Lond) 326:527–551

    Google Scholar 

  • Del Castillo JB, Katz B (1954) Quantal components of the endplate potential. J Physiol (Lond) 124:560–573

    Google Scholar 

  • Del Castillo JB, Katz B (1956) Biophysical aspects of neuromuscular transmission. Prog Biophys Biophys Chem 6:121–170

    Google Scholar 

  • Dudel J (1981) The effect of reduced calcium on quantal unit current and release at the crayfish neuromuscular junction. Pflügers Arch 391:35–40

    Google Scholar 

  • Dudel J, Finger W, Stettmeier H (1980) Inhibitory synaptic channels activated by γ-aminobutyric acid (GABA) in crayfish muscle. Pflügers Arch 387:143–151

    Google Scholar 

  • Fesce R, Segal JR, Ceccarelli B, Hurlbut WP (1986) Effects of black widow spider venom and Ca2+ on quantal secretion at the frog neuromuscular junction. J Gen Physiol 88:59–81

    Google Scholar 

  • Finger W (1983) Effects of glycine on the crayfish neuromuscular junction. II. Release of inhibitory transmitter activated by glycine. Pflügers Arch 397:128–134

    Google Scholar 

  • Finger W (1985) Excitatory transmitter release induced by high concentrations of γ-aminobutyric acid (GABA) in crayfish neuromuscular junctions. Pflügers Arch 405:265–273

    Google Scholar 

  • Finger W, Martin C (1986a) Spontaneous excitatory postsynaptic currents in crayfish neuromuscular junctions in the absence and presence of serotonin and 3,4-diaminopyridine. J Comp Physiol A 159:13–20

    Google Scholar 

  • Finger W, Martin C (1986b) Repetitive axonal discharges elicited by serotonin and intracellular adenosine 3′,5′-cyclic monophosphate in the crayfish neuromuscular junction. Neurosci Lett 72:295–299

    Google Scholar 

  • Finger W, Martin C (1987a) Veratridine-induced high frequency release of excitatory transmitter quanta in crayfish nerve-muscle synapses. Pflügers Arch 408 (Suppl):R67/260

    Google Scholar 

  • Finger W, Martin C (1987b) Differential effect of intraterminal sodium on spontancous quantal release of transmitter in two neuromuscular junctions of crayfish. Neurosci Lett 75:293–298

    Google Scholar 

  • Finger W, Martin C (1987c) High-frequency asynchronous release of excitatory and inhibitory transmitter quanta triggered by veratridine in nerve-muscle synapses of crayfish. Abstracts of the 9th International Biophysics Congress, Jerusalem, Israel, August 23–28, 1987

  • Finger W, Martin C (1987d) Inhibitory effect of intraterminal lithium on asynchronous relcase of excitatory quanta induced by veratridine in nerve-muscle synapses of crayfish. Neurosci Lett 83:113–117

    Google Scholar 

  • Finger W, Martin C (1988) Effect of lithium on veratridine-induced quantal and non-quantal release from inhibitory nerve terminals in crayfish muscle. Pflügers Arch 411:478–480

    Google Scholar 

  • Finger W, Stettmeier H (1980) Efficacy of the two microelectrode voltage clamp technique in crayfish muscle. Pflügers Arch 387:133–141

    Google Scholar 

  • Finger W, Stettmeier H (1981) Analysis of miniature spontaneous inhibitory postsynaptic currents (sIPSCs) from current noise in crayfish opener muscle. Pflügers Arch 392:157–162

    Google Scholar 

  • Florey E, Cahill MA (1982) The innervation pattern of crustacean skeletal muscle. Morphometry and ultrastructure of terminals and synapses. Cell Tissue Res 224:527–541

    Google Scholar 

  • Glusman S, Kravitz EA (1982) The action of serotonin on excitatory nerve terminals in lobster nerve-muscle preparations. J Physiol (Lond) 325:223–241

    Google Scholar 

  • Hatt H, Smith DO (1976) Synaptic depression related to presynaptic axon conduction block. J Physiol (Lond) 259:367–393

    Google Scholar 

  • Hille B (1984) Ionic channels of excitable membranes. Sinauer Associates, Inc. Sunderland, Massachusetts

    Google Scholar 

  • Jahromi SS, Atwood HL (1974) Three-dimensional ultrastructure of the crayfish neuromuscular apparatus. J Cell Biol 63:599–613

    Google Scholar 

  • Jansson SE, Albuquerque EX, Daly J (1974) The pharmacology of batrachotoxin. VI. Effects on the mammalian motor nerve terminal. J Pharmacol Exp Ther 189:525–537

    Google Scholar 

  • Katz B (1969) The release of neural transmitter substances. In: The Sherrington Lectures, vol X, Liverpool: Liverpool University Press

    Google Scholar 

  • Leibowitz MD, Sutro JB, Hille B (1986) Voltage-dependent gating of veratridine-modified Na Channels. J Gen Physiol 87 (1986) 25–46

    Google Scholar 

  • Lnenicka GA, Mellon DeF (1983) Transmitter release during normal and altered growth of identified muscle fibres in the crayfish. J Physiol (Lond) 345:285–296

    Google Scholar 

  • Martin C (1986) Hochfrequente Freisetzung von Überträgerstoff aus Endigungen erregender oder hemmender Nerven am Flußkrebsmuskel. Dissertation, Technische Universität München. FRG

    Google Scholar 

  • Martin C, Finger W (1985) Tonic depolarization of excitatory nerve terminals in crayfish muscle by high concentrations of extracellular potassium. Neurosci Lett 53:309–314

    Google Scholar 

  • Martin C, Finger W (1988) Veratridine-induced high-frequency asynchronous release of inhibitory transmitter quanta in crayfish nerve-muscle synapses superfused with normal and lowcalcium saline. Pflügers Arch 411:469–477

    Google Scholar 

  • Parnas I, Atwood HL (1966) Phasic and tonic neuromuscular systems in the abdominal extensor muscle of crayfish and recklobster. Comp Biochem Physiol 18:701–723

    Google Scholar 

  • Rahamimoff R, Lev-Tov A, Meiri H (1980) Primary and secondary regulation of quantal transmitter release: calcium and sodium. J Exp Biol 89:5–18

    Google Scholar 

  • Sandoval ME (1981) On the role of mitochondria in neurotransmitter release. In: Tapia R, Cotman CW (eds). Regulatory mechanisms of synaptic transmission. Plenum Press, New York, pp 187–203

    Google Scholar 

  • Schoffelmeer ANM, Mulder AH (1983)3H Noradrenaline release from brain slices induced by an increase in the intracellular sodium concentration: role of intracellular calcium stores. J Neurochem 40:615–621

    Google Scholar 

  • Segal JR, Ceccarelli B, Fesce R, Hurlbut WP (1985) Miniature endplate potential frequency and amplitude determined by an extension of Campbell's theorem. Biophys J 47:183–202

    Google Scholar 

  • Smith SJ, Augustine GJ (1988) Calcium ions, active zones and synaptic transmitter release. TINS 11:458–464

    Google Scholar 

  • Stettmeier H, Finger W, Dudel J (1983) Glutamate activated postsynaptic channels in crayfish muscle investigated by noise analysis. Pflügers Arch 397:13–19

    Google Scholar 

  • Walther C (1981) Synaptic terminals from an identified motoneuron in locust muscle: comparison between first instar larva and adult. Neurosci Lett 27:237–242

    Google Scholar 

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This investigation was supported by the Deutsche Forschungsgemeinschaft, SFB 220

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Finger, W., Martin, C. Quantal stores of excitatory transmitter in nerve-muscle synapses of crayfish evaluated from high-frequency asynchronous quantal release induced by veratridine or high concentrations of potassium. Pflugers Arch. 414, 437–442 (1989). https://doi.org/10.1007/BF00585054

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  • DOI: https://doi.org/10.1007/BF00585054

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