Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Normal variations in presynaptic active zones of frog neuromuscular junctions


Neuromuscular junctions of frog cutaneous pectoris muscles were examined by the complementary-replica freeze-fracture technique. The large number of active zones revealed in this way permitted quantitation of normal and disrupted zones in control muscles and in muscles deprived of external calcium for periods of up to eight hours. Although some 87% of the active zones examined had the usual appearance of two double rows of intramembrane particles flanking a low ridge, several varieties of disrupted active zones appeared in which the rows were interrupted, dispersed, rotated, or reduced to single rows. The frequency of disruptions was not increased by calcium deprivation. Disorganized active zones at tips of neuromuscular junctions may represent normal remodelling of the junctions.

This is a preview of subscription content, log in to check access.


  1. Blioch, Z. L., Glagoleva, I. M., Liberman &Nenashev, V. A. (1968) A Study of the mechanism of quantal transmitter release at a chemical synapse.Journal of Physiology 199, 11–35.

  2. Block, R. J. &Geiger, B. (1980) The localization of acetylcholine receptor clusters in areas of cell substrate contact in cultures of rat myotubes.Cell 21, 25–35.

  3. Ceccarelli, B., Grohovaz, F., Hurlbut, W. P. &Iezzi, N. (1979) Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. I. Effects of black widow spider venom and Ca2+-free solutions on the structure of the active zone.Journal of Cell Biology 81, 163–77.

  4. Erulkar, S. D., Rahamimoff, R. &Rotshenker, S. (1978) Quelling of spontaneous transmitter release by nerve impulses in low extracellular calcium solutions.Journal of Physiology 278, 491–500.

  5. Galli, P., Brenna, A., DeCamilli, P. &Meldolesi, J. (1976) Extracellular calcium and the organization of tight junctions in pancreatic acinar cells.Experimental Cell Research 99, 178–83.

  6. Heuser, J. E. (1976) Morphology of synaptic vesicle discharge and reformation at the frog neuromuscluar junction. InMotor Innervation of Muscle (edited byThesleff, S.), pp. 51–115. London: Academic Press.

  7. Heuser, J. E. (1980) 3-D visualization of membrane and cytoplasmic specialization at the frog neuromuscluar junction. InOntogenesis and Functional Mechanisms of Peripheral Synapses (edited byTaxi, J.), pp. 139–55. (Inserm Symposium No. 13). Amsterdam: Elsevier Biomedical Press.

  8. Heuser, J. E. &Reese, T. S. (1977) Structure of the synapse. InHandbook of Physiology —The Nervous System I (edited byKandel, E.), pp. 261–94. Washington, DC: American Physiological Society.

  9. Heuser, J. E. &Reese, T. S. (1981) Structural changes after transmitter release at the frog neuromuscular junction.Journal of Cell Biology 88, 564–80.

  10. Hubbard, J. E., Jones, S. F. &Landau, E. M. (1968) On the mechanism by which calcium and magnesium affect the spontaneous release of transmitter from mammalian motor nerve terminals.Journal of Physiology 194, 355–80.

  11. Ko, C.-P. (1981) Electrophysiological and freeze-fracture studies of changes following denervation at frog neuromuscular junctions.Journal of Physiology 321, 627–39.

  12. Llinas, R. (1977) Calcium and transmitter release in squid synapse. InSociety for Neuroscience Symposium, Vol. 2 (edited byCowan, W. M. &Ferendelli, J. A.), pp. 139–60. Bethesda: Society for Neuroscience.

  13. Lynch, K., Ko, C.-P., Pumplin, D. W. &Harris, C. D. (1980) Freeze-fracture of developing neuromuscular junctions in the tadpole.Society for Neuroscience, 10th Annual Meeting Abstract 191. 5.

  14. Pauli, B. U., Weinstein, R. S., Soble, L. W. &Alroy, J. (1977) Freeze-fracture of monolayer cultures,journal of Cell Biology 72, 763–9.

  15. Pumplin, D. W. &Reese, T. S. (1977) Action of brown widow spider venom and botulinum toxin on the frog neuromuscular junction examined with the freeze-fracture technique.Journal of Physiology 273, 443–97.

  16. Pumplin, D. W., Reese, T. S. &Llinas, R. (1981) Are the presynaptic particles the calcium channels?Proceedings of the National Academy of Science USA 78, 7210–4.

  17. Shotton, P. M., Heuser, J. E., Reese, B. F. &Reese, T. S. (1979) Postsynaptic membrane folds of the frog neuromuscular junction visualized by scanning electron microscopy.Neuroscience 4, 427–35.

  18. Singer, S. J. &Nicolson, G. L. (1972) The fluid mosaic model of the structure of cell membranes.Science 175, 720–5.

  19. Wernig, A., Pecot-Dechavassine, M. &Stover, H. (1980) Sprouting and regression of the nerve at the frog neuromuscular junction in normal conditions and after prolonged paralysis with curare.Journal of Neurocytology 9, 277–303.

Download references

Author information

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pumplin, D.W. Normal variations in presynaptic active zones of frog neuromuscular junctions. J Neurocytol 12, 317–323 (1983).

Download citation


  • Calcium
  • Normal Variation
  • Active Zone
  • Neuromuscular Junction
  • Control Muscle