Journal of Neurocytology

, Volume 15, Issue 1, pp 63–74 | Cite as

Reorganization of synaptic ultrastructure at facilitated lobster neuromuscular terminals

  • R. G. Chiang
  • C. K. Govind


Prolonged stimulation of the single excitor axon to the lobster distal accessory flexor muscle in the presence of ouabain caused long-term facilitation at its neuromuscular synapses. Hence the extracellularly recorded synaptic potentials failed less frequently and increased their mean amplitude, compared to the non-facilitated (control) potentials from homologous sites in the contralateral muscle. The fine structure of synaptic terminals between matched pairs of facilitated and control preparations was compared with the aid of serial section electron microscopy. Differences between facilitated and control preparations were similar both when the latter were bathed in normal saline or ouabain-containing saline, suggesting that the changes were related to the electrical stimulation rather than to the presence of ouabain. First, the facilitated terminals were smaller in surface area than the control. Second, the number and size of synaptic contacts in the facilitated terminals resembled those in the control. Third, presynaptic dense bodies or active sites increased in number although their sizes remained unaltered in the facilitated terminal. This increase is attributed to the addition of dense bodies at existing synaptic contacts since synaptic contacts remained constant in number between facilitated and control preparations. Fourth, the number and size of synaptic vesicles were unaffected by prolonged stimulation although there was a redistribution of vesicles such that they appeared to be channelled in distinct streams to synaptic contacts. Fifth, mitochondria increased in number and were situated closer to the dense bodies at facilitated nerve terminals than at control terminals. Overall, these changes denote considerable reorganization of the synaptic terminals associated with elevated transmitter release.


Ouabain Dense Body Synaptic Contact Synaptic Terminal Control Preparation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Acosta-Urquidi, J. (1978) Dormant synapses in a crustacean neuromuscular system.Canadian Journal of Zoology 56, 463–8.Google Scholar
  2. Allen, R. D., Lasek, R. J., Gilbert, S. O., Hodge, A. J. &Govind, C. K. (1982) Fast axonal transport in lobster axons.Biological Bulletin 163, 379Google Scholar
  3. Atwood, H. L. (1982) Synapses and neurotransmitters. InThe Biology of Crustacea, Vol. 3,Neurobiology: Structure and Function (edited byBliss, D. E., Atwood, H. L. &Sandeman, D. C.), pp. 105–50. New York: Academic Press.Google Scholar
  4. Atwood, H. L., Charlton, M. P. &Thompson, C. S. (1983) Neuromuscular transmission in crustaceans is enhanced by a sodium ionophere, monensin, and by prolonged stimulation.Journal of Physiology 335, 179–95.PubMedGoogle Scholar
  5. Atwood, H. L., Lang, F. &Morin, W. A. (1972) Synaptk vesicles: selective depletion in crayfish excitatory and inhibitory axons.Science 176, 1353–5.PubMedGoogle Scholar
  6. Atwood, H. L. &Marin, L. (1983) Ultrastructure of synapses with different transmitter-releasing characteristics on motor axon terminals of a crab,Hyas areneas.Cell and Tissue Research 231, 103–15.PubMedGoogle Scholar
  7. Atwood, H. L., Swernachuk, L. E. &Gruenwald, C. R. (1975) Long term synaptic facilitation during sodium accumulation in nerve terminals.Brain Research 100, 198–204.PubMedGoogle Scholar
  8. Birks, R. J. (1971) Effects of stimulation on synaptic vesicles in sympathetic ganglia as shown by fixation in the presence of Mg2+.Journal of Physiology 215, 26–31.Google Scholar
  9. Botham, R. P., Beadle, D. J., Hart, R. J., Potter, C. &Wilson, R. G. (1978) Stimulation induced depletion of the synaptic vesicles in excitatory motor nerve terminals of the locust,Locusta migratoria L.Expericntia 34, 207–8.Google Scholar
  10. Bryan, J. S. &Atwood, H. L. (1981) Two types Of synaptic depression at synapses of a single crustacean motor axon.Marine Behaviour and Physiology 8, 99–121.Google Scholar
  11. Ceccarelli, B., Hurlbut, W. P. &Mauro, A. (1972) Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation.Journal of Cell Biology 54, 30–8.PubMedGoogle Scholar
  12. Ceccarelli, B., Hurlbut, W. P. &Mauro, A. (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction.Journal of Cell Biology 57, 499–524.PubMedGoogle Scholar
  13. Chiang, R. G. &Govind, C. K. (1984) Decrease in transmitter output and synaptic ultrastructure at lobster neuromuscular terminals with decentralization.Brain Research 299, 265–79.PubMedGoogle Scholar
  14. Cohen, M. J. (1963) The crustacean myochordotonal organ as a proprioceptive system.Comparative Biochemistry and Physiology 8, 223–43.Google Scholar
  15. Couteaux, R. &Pécot-Dechavassine, M. (1970) Vesicles synaptiques et poches au niveau des ‘zones active’ de la jonction neuromusculaire.Comptes Rendus de l'Academie des Sciences, Series D 271, 2346–9.Google Scholar
  16. Del Castillo, J. &Katz, B. (1954) Quantal components of the endplate potential,Journal of Physiology 124, 560–73.PubMedGoogle Scholar
  17. Dudel, J. &Kuffler, S. W. (1961) The quantal nature of transmission and miniature potentials at the crayfish neuromuscular Junction.Journal of Physiology 155, 514–29.PubMedGoogle Scholar
  18. Govind, C. K. &Chiang, R. G. (1979) Correlation between presynaptic dense bodies and transmitter output at lobster neuromuscular terminals by serial section electron microscopy.Brain Research 161, 377–88.PubMedGoogle Scholar
  19. Govind, C. K., Derosa, R. A. &Pearce, J. (1980) Presynaptic dense bars at neuromuscular synapses of the lobsterHomarus americanus.Cell and Tissue Research 207, 81–8.PubMedGoogle Scholar
  20. Govind, C. K. &Meiss, D. E. (1979) Quantitative comparison of low- and high-output neuromuscular synapses from a motoneuron of the lobsterHomanis americanus.Cell and Tissue Research 198, 455–63.PubMedGoogle Scholar
  21. Govind, C. K. &Pearce, J. (1982) Proliferation and relocation of developing lobster neuromuscular synapses.Developmental Biology 90, 67–78.PubMedGoogle Scholar
  22. Heuser, J. E. &Reese, T. S. (1981) Structural changes after transmitter release at the frog neuromuscular junction.Journal of Cell Biology 88, 564–80.PubMedGoogle Scholar
  23. Heuser, J. E., Reese, T. S., Dennis, M. J., Jan, Y., Jan, E. &Evans, L. (1979) Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release.Journal of Cell Biology 81, 275–300.PubMedGoogle Scholar
  24. Heuser, J. E., Reese, T. S. &Landis, D. M. D. (1974) Functional changes in frog neuromuscular junction studied with freeze-fracture.Journal of Neurocytology 3, 104–31.Google Scholar
  25. Hubbard, J. I. &Kwanbunbumpen, S. (1968) Evidence for the vesicle hypothesis,Journal of Physiology 194, 407–20.PubMedGoogle Scholar
  26. Katz, B. (1966)Nerve, Muscle und Synapse. New York: McGraw Hill.Google Scholar
  27. Korneeiussen, H. (1972) Ultrastructure of normal and stimulated motor endplates with comments on the origin and fate of synaptic vesicles.Zeitschrift für Zellforschung und mikroskopische Anatomie 130, 28–36.Google Scholar
  28. McKinlay, R. G. &Usherwood, P. N. R. (1973) The role of the synaptic vesicle in transmission at the insect nerve-muscle junction.Life Sciences 13, 1051–6.PubMedGoogle Scholar
  29. Meiss, D. E. &Govind, C. K. (1979) Regional differentiation of neuromuscular synapses in a lobster receptor muscle.Jounml of Experimental Biology 79, 99–114.Google Scholar
  30. Meiss, D. E. &Govind, C. K. (1980) Heterogeneity of excitatory synapses at the ends of single muscle fibers in lobster,Homarus americanus.Journal of Neurobiology 11, 381–95.PubMedGoogle Scholar
  31. Model, P. G., Highstein, S. M. &Bennett, M. V. E. (1975) Depletion of vesicles and fatigue of transmission at a vertebrate central synapse.Brain Research 98, 209–28.PubMedGoogle Scholar
  32. Reinecke, W. &Walther, C. (1981) Ultrastructural changes with high activity and subsequent recovery at locust motor nerve terminals. A stereological analysis.Neuroscience 6, 489–503.PubMedGoogle Scholar
  33. Sherman, R. G. &Atwood, H. L. (1971) Synaptic facilitation: long-term neuromuscular facilitation in crustaceans.Science 171, 1248–50.PubMedGoogle Scholar
  34. Titmus, M. J. (1981) Ultrastructure of fast excitatory, slow excitatory and inhibitory neuromuscular junctions in locusts.Journal of Neumcytology 10, 363–85.Google Scholar
  35. Zimmerman, H. &Denston, C. R. (1977) Recycling of synaptic vesicles in the cholinergic synapses of theTorpedo electric organ during induced transmitter release.Neuroscience 2, 695–714.PubMedGoogle Scholar

Copyright information

© Chapman and Hall Ltd 1986

Authors and Affiliations

  • R. G. Chiang
    • 1
  • C. K. Govind
    • 1
  1. 1.Department of Zoology, Scarborough CampusUniversity of TorontoWest HillCanada

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