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. 1974 Aug;241(1):69–89. doi: 10.1113/jphysiol.1974.sp010641

Crayfish neuromuscular facilitation activated by constant presynaptic action potentials and depolarizing pulses

Robert S Zucker
PMCID: PMC1331073  PMID: 4153766

Abstract

1. Experiments were conducted to test the hypothesis that facilitation of transmitter release in response to repetitive stimulation of the exciter motor axon to the crayfish claw opener muscle is due to an increase in the amplitude or duration of the action potential in presynaptic terminals. No consistent changes were found in the nerve terminal potential (n.t.p.) recorded extracellularly at synaptic sites on the surface of muscle fibres.

2. Apparent changes in n.t.p. are attributed to three causes.

(i) Some recordings are shown to be contaminated by non-specific muscle responses which grow during facilitation.

(ii) Some averaged n.t.p.s exhibit opposite changes in amplitude and duration which suggest a change in the synchrony of presynaptic nerve impulses at different frequencies.

(iii) Some changes in n.t.p. are blocked by γ-methyl glutamate, an antagonist of the post-synaptic receptor, which suggests that these changes are caused by small muscle movements.

3. The only change in n.t.p. believed to represent an actual change in the intracellular signal is a reduction in n.t.p. amplitude to the second of two stimuli separated by a brief interval.

4. Tetra-ethyl ammonium ions increase synaptic transmission about 20% and prolong the n.t.p. about 15%. This result suggests that an increase in n.t.p. large enough to increase transmission by the several hundred per cent occurring during facilitation would be detected.

5. The nerve terminals are electrically excitable, and most synaptic sites have a diphasic or triphasic n.t.p., which suggests that the motor neurone terminals are actively invaded by nerve impulses.

6. When nerve impulses are blocked in tetrodotoxin, depolarization of nerve terminals increases the frequency of miniature excitatory junctional potentials (e.j.p.s), and a phasic e.j.p. can be evoked by large, brief depolarizing pulses. Responses to repetitive or paired depolarizations of constant amplitude and duration exhibit a facilitation similar to that of e.j.p.s evoked by nerve impulses.

7. It is concluded that facilitation in the crayfish claw opener is not due to a change in the presynaptic action potential, but is due to some change at a later step in the depolarization—secretion process.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Atwood H. L., Lang F. Differential responses of crab neuromuscular synapses to cesium ion. J Gen Physiol. 1973 Jun;61(6):747–766. doi: 10.1085/jgp.61.6.747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Atwood H. L., Morin W. A. Neuromuscular and axoaxonal synapses of the crayish opener muscle. J Ultrastruct Res. 1970 Aug;32(3):351–369. doi: 10.1016/s0022-5320(70)80015-6. [DOI] [PubMed] [Google Scholar]
  3. Atwood H. L. Variation in physiological properties of crustacean motor synapses. Nature. 1967 Jul 1;215(5096):57–58. doi: 10.1038/215057a0. [DOI] [PubMed] [Google Scholar]
  4. Benoit P. R., Mambrini J. Modification of transmitter release by ions which prolong the presynaptic action potential. J Physiol. 1970 Oct;210(3):681–695. doi: 10.1113/jphysiol.1970.sp009235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Birks R. I., Cohen M. W. The influence of internal sodium on the behaviour of motor nerve endings. Proc R Soc Lond B Biol Sci. 1968 Jul 9;170(1021):401–421. doi: 10.1098/rspb.1968.0047. [DOI] [PubMed] [Google Scholar]
  6. Bittner G. D., Harrison J. A reconsideration of the Poisson hypothesis for transmitter release at the crayfish neuromuscular junction. J Physiol. 1970 Jan;206(1):1–23. doi: 10.1113/jphysiol.1970.sp008994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bittner G. D., Kennedy D. Quantitative aspects of transmitter release. J Cell Biol. 1970 Dec;47(3):585–592. doi: 10.1083/jcb.47.3.585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bloedel J., Gage P. W., Llinás R., Quastel D. M. Transmitter release at the squid giant synapse in the presence of tetrodotoxin. Nature. 1966 Oct 1;212(5057):49–50. doi: 10.1038/212049a0. [DOI] [PubMed] [Google Scholar]
  9. Braun M., Schmidt R. F. Potential changes recorded from the frog motor nerve terminal during its activation. Pflugers Arch Gesamte Physiol Menschen Tiere. 1966;287(1):56–80. doi: 10.1007/BF00362454. [DOI] [PubMed] [Google Scholar]
  10. CURTIS D. R., ECCLES J. C. Synaptic action during and after repetitive stimulation. J Physiol. 1960 Feb;150:374–398. doi: 10.1113/jphysiol.1960.sp006393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DEL CASTILLO J., KATZ B. Localization of active spots within the neuromuscular junction of the frog. J Physiol. 1956 Jun 28;132(3):630–649. doi: 10.1113/jphysiol.1956.sp005554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. DEL CASTILLO J., KATZ B. Quantal components of the end-plate potential. J Physiol. 1954 Jun 28;124(3):560–573. doi: 10.1113/jphysiol.1954.sp005129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. DEL CASTILLO J., KATZ B. Statistical factors involved in neuromuscular facilitation and depression. J Physiol. 1954 Jun 28;124(3):574–585. doi: 10.1113/jphysiol.1954.sp005130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. DUDEL J., KUFFLER S. W. Mechanism of facilitation at the crayfish neuromuscular junction. J Physiol. 1961 Mar;155:530–542. doi: 10.1113/jphysiol.1961.sp006645. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. DUDEL J., KUFFLER S. W. The quantal nature of transmission and spontaneous miniature potentials at the crayfish neuromuscular junction. J Physiol. 1961 Mar;155:514–529. doi: 10.1113/jphysiol.1961.sp006644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. DUDEL J. POTENTIAL CHANGES IN THE CRAYFISH MOTOR NERVE TERMINAL DURING REPETITIVE STIMULATION. Pflugers Arch Gesamte Physiol Menschen Tiere. 1965 Jan 11;282:323–337. doi: 10.1007/BF00412507. [DOI] [PubMed] [Google Scholar]
  17. DUDEL J. PRESYNAPTIC INHIBITION OF THE EXCITATORY NERVE TERMINAL IN THE NEUROMUSCULAR JUNCTION OF THE CRAYFISH. Pflugers Arch Gesamte Physiol Menschen Tiere. 1963 Sep 9;277:537–557. [PubMed] [Google Scholar]
  18. DUDEL J. THE MECHANISM OF PRESYNAPTIC INHIBITION AT THE CRAYFISH NEUROMUSCULAR JUNCTION. Pflugers Arch Gesamte Physiol Menschen Tiere. 1965 May 10;284:66–80. doi: 10.1007/BF00412368. [DOI] [PubMed] [Google Scholar]
  19. Dudel J. The effect of polarizing current on action potential and transmitter release in crayfish motor nerve terminals. Pflugers Arch. 1971;324(3):227–248. doi: 10.1007/BF00586421. [DOI] [PubMed] [Google Scholar]
  20. HUBBARD J. I. REPETITIVE STIMULATION AT THE MAMMALIAN NEUROMUSCULAR JUNCTION, AND THE MOBILIZATION OF TRANSMITTER. J Physiol. 1963 Dec;169:641–662. doi: 10.1113/jphysiol.1963.sp007286. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. HUBBARD J. I., SCHMIDT R. F. An electrophysiological investigation of mammalian motor nerve terminals. J Physiol. 1963 Apr;166:145–167. doi: 10.1113/jphysiol.1963.sp007096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Johnson E. W., Wernig A. The binomial nature of transmitter release at the crayfish neuromuscular junction. J Physiol. 1971 Nov;218(3):757–767. doi: 10.1113/jphysiol.1971.sp009642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. KATZ B., MILEDI R. PROPAGATION OF ELECTRIC ACTIVITY IN MOTOR NERVE TERMINALS. Proc R Soc Lond B Biol Sci. 1965 Feb 16;161:453–482. doi: 10.1098/rspb.1965.0015. [DOI] [PubMed] [Google Scholar]
  24. KATZ B., MILEDI R. THE EFFECT OF CALCIUM ON ACETYLCHOLINE RELEASE FROM MOTOR NERVE TERMINALS. Proc R Soc Lond B Biol Sci. 1965 Feb 16;161:496–503. doi: 10.1098/rspb.1965.0017. [DOI] [PubMed] [Google Scholar]
  25. KUNO M. MECHANSIM OF FACILITATION AND DEPRESSION OF THE EXCITATORY SYNAPTIC POTENTIAL IN SPINAL MOTONEURONES. J Physiol. 1964 Dec;175:100–112. doi: 10.1113/jphysiol.1964.sp007505. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Katz B., Miledi R. A study of synaptic transmission in the absence of nerve impulses. J Physiol. 1967 Sep;192(2):407–436. doi: 10.1113/jphysiol.1967.sp008307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Katz B., Miledi R. Tetrodotoxin and neuromuscular transmission. Proc R Soc Lond B Biol Sci. 1967 Jan 31;167(1006):8–22. doi: 10.1098/rspb.1967.0010. [DOI] [PubMed] [Google Scholar]
  28. Katz B., Miledi R. The release of acetylcholine from nerve endings by graded electric pulses. Proc R Soc Lond B Biol Sci. 1967 Jan 31;167(1006):23–38. doi: 10.1098/rspb.1967.0011. [DOI] [PubMed] [Google Scholar]
  29. Kuno M., Weakly J. N. Quantal components of the inhibitory synaptic potential in spinal mononeurones of the cat. J Physiol. 1972 Jul;224(2):287–303. doi: 10.1113/jphysiol.1972.sp009895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. LILEY A. W. The quantal components of the mammalian end-plate potential. J Physiol. 1956 Sep 27;133(3):571–587. doi: 10.1113/jphysiol.1956.sp005610. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. LLOYD D. P. C. Post-tetanic potentiation of response in monosynaptic reflex pathways of the spinal cord. J Gen Physiol. 1949 Nov;33(2):147–170. doi: 10.1085/jgp.33.2.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Lang F., Atwood H. L., Morin W. A. Innervation and vascular supply of the crayfish opener muscle: scanning and transmission electron microscopy. Z Zellforsch Mikrosk Anat. 1972;127(2):189–200. doi: 10.1007/BF00306801. [DOI] [PubMed] [Google Scholar]
  33. Linder T. M. Calcium and facilitation at two classes of crustacean neuromuscular synapses. J Gen Physiol. 1973 Jan;61(1):56–73. doi: 10.1085/jgp.61.1.56. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. MARTIN A. R., PILAR G. PRESYNAPTIC AND POST-SYNAPTIC EVENTS DURING POST-TETANIC POTENTIATION AND FACILITATION IN THE AVIAN CILIARY GANGLION. J Physiol. 1964 Dec;175:17–30. doi: 10.1113/jphysiol.1964.sp007500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Miledi R., Slater C. R. The action of calcium on neuronal synapses in the squid. J Physiol. 1966 May;184(2):473–498. doi: 10.1113/jphysiol.1966.sp007927. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Ortiz C. L. Crayfish neuromuscular junction: facilitation with constant nerve terminal potential. Experientia. 1972 Sep 15;28(9):1035–1036. doi: 10.1007/BF01918655. [DOI] [PubMed] [Google Scholar]
  37. Sherman R. G., Atwood H. L. Correlated electrophysiological and ultrastructural studies of a crustacean motor unit. J Gen Physiol. 1972 May;59(5):586–615. doi: 10.1085/jgp.59.5.586. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sherman R. G., Atwood H. L. Synaptic facilitation: long-term neuromuscular facilitation in crustaceans. Science. 1971 Mar 26;171(3977):1248–1250. doi: 10.1126/science.171.3977.1248. [DOI] [PubMed] [Google Scholar]
  39. TAKEUCHI A., TAKEUCHI N. Electrical changes in pre- and postsynaptic axons of the giant synapse of Loligo. J Gen Physiol. 1962 Jul;45:1181–1193. doi: 10.1085/jgp.45.6.1181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. WALL P. D., JOHNSON A. R. Changes associated with post-tetanic potentiation of a monosynaptic reflex. J Neurophysiol. 1958 Mar;21(2):148–158. doi: 10.1152/jn.1958.21.2.148. [DOI] [PubMed] [Google Scholar]
  41. Zucker R. S. Changes in the statistics of transmitter release during facilitation. J Physiol. 1973 Mar;229(3):787–810. doi: 10.1113/jphysiol.1973.sp010167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Zucker R. S. Characteristics of crayfish neuromuscular facilitation and their calcium dependence. J Physiol. 1974 Aug;241(1):91–110. doi: 10.1113/jphysiol.1974.sp010642. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Zucker R. S. Excitability changes in crayfish motor neurone terminals. J Physiol. 1974 Aug;241(1):111–126. doi: 10.1113/jphysiol.1974.sp010643. [DOI] [PMC free article] [PubMed] [Google Scholar]

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