Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1987 Jan;84(2):590–594. doi: 10.1073/pnas.84.2.590

Brief occurrence of a population of presynaptic intramembrane particles coincides with transmission of a nerve impulse.

D Muller, L M Garcia-Segura, A Parducz, Y Dunant
PMCID: PMC304256  PMID: 3467375

Abstract

Small pieces of Torpedo electric organ were cryofixed at 1-ms time intervals in a liquid medium at -190 degrees C before, during, and after the passage of a single nerve impulse. In contrast to studies using this or other preparations, these experiments were done without 4-aminopyridine or other drugs that potentiate transmitter release. Freeze-fracture replicas were made from the most superficial layers of the tissue, where the rate of cooling was rapid enough to retain ultrastructure in the absence of chemical fixation. We found that the transmission of an impulse was accompanied by the momentary appearance of a population of large intramembrane particles in both the protoplasmic (P) and the external (E) leaflets of the presynaptic plasma membrane. The change was very brief, appearing soon after the stimulus artifact. It lasted for 2-3 ms. Large pits denoting vesicle openings at the presynaptic membrane were found in a small proportion of nerve terminals; their number did not increase during transmission of the nerve impulse. Reducing the temperature from 16 to 5 degrees C slowed the time course of both the electrophysiological response and the change in intramembrane particles. The number of large particles did not increase when stimulation was applied in a low-Ca medium, a condition where the nerve terminals were still depolarized by the action potential but did not release the neurotransmitter. From these and other observations, we conclude that this transient change of intramembrane particles is closely linked to the mechanism of acetylcholine release at the nerve-electroplaque junction.

Full text

PDF
590

Images in this article

592Image
on p.592
592Image
on p.592

Selected References

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

  1. Cartaud J., Benedetti E. L. A morphological study of the cholinergic receptor protein from Torpedo marmorata in its membrane environment and in its detergent-extracted purified form. J Cell Sci. 1978 Feb;29:313–337. doi: 10.1242/jcs.29.1.313. [DOI] [PubMed] [Google Scholar]
  2. Dunant Y., Eder L., Servetiadis-Hirt L. Acetylcholine release evoked by single or a few nerve impulses in the electric organ of Torpedo. J Physiol. 1980 Jan;298:185–203. doi: 10.1113/jphysiol.1980.sp013075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Dunant Y., Jones G. J., Loctin F. Acetylcholine measured at short time intervals during transmission of nerve impulses in the electric organ of Torpedo. J Physiol. 1982 Apr;325:441–460. doi: 10.1113/jphysiol.1982.sp014161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dunant Y., Muller D. Quantal release of acetylcholine evoked by focal depolarization at the Torpedo nerve-electroplaque junction. J Physiol. 1986 Oct;379:461–478. doi: 10.1113/jphysiol.1986.sp016264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Garcia-Segura L. M., Muller D., Dunant Y. Increase in the number of presynaptic large intramembrane particles during synaptic transmission at the Torpedo nerve-electroplaque junction. Neuroscience. 1986 Sep;19(1):63–79. doi: 10.1016/0306-4522(86)90006-0. [DOI] [PubMed] [Google Scholar]
  6. Garcia-Segura L. M., Perrelet A. Postsynaptic membrane domains in the molecular layer of the cerebellum: a correlation between presynaptic inputs and postsynaptic plasma membrane organization. Brain Res. 1984 Nov 12;321(2):255–266. doi: 10.1016/0006-8993(84)90178-1. [DOI] [PubMed] [Google Scholar]
  7. Heuser J. E., Reese T. S., Dennis M. J., Jan Y., Jan L., Evans L. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol. 1979 May;81(2):275–300. doi: 10.1083/jcb.81.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Heuser J. E., Reese T. S. Structural changes after transmitter release at the frog neuromuscular junction. J Cell Biol. 1981 Mar;88(3):564–580. doi: 10.1083/jcb.88.3.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Heuser J. E., Salpeter S. R. Organization of acetylcholine receptors in quick-frozen, deep-etched, and rotary-replicated Torpedo postsynaptic membrane. J Cell Biol. 1979 Jul;82(1):150–173. doi: 10.1083/jcb.82.1.150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Israël M., Lesbats B., Manaranche R., Morel N., Gulik-Krzywicki T., Dedieu J. C. Rearrangement of intramembrane particles as a possible mechanism for the release of acetylcholine. J Physiol (Paris) 1982;78(4):348–356. [PubMed] [Google Scholar]
  11. Israël M., Lesbats B., Morel N., Manaranche R., Gulik-Krzywicki T., Dedieu J. C. Reconstitution of a functional synaptosomal membrane possessing the protein constituents involved in acetylcholine translocation. Proc Natl Acad Sci U S A. 1984 Jan;81(1):277–281. doi: 10.1073/pnas.81.1.277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Israël M., Manaranche R., Morel N., Dedieu J. C., Gulik-Krzywicki T., Lesbats B. Redistribution of intramembrane particles related to acetylcholine release by cholinergic synaptosomes. J Ultrastruct Res. 1981 May;75(2):162–178. doi: 10.1016/s0022-5320(81)80132-3. [DOI] [PubMed] [Google Scholar]
  13. Jones G. J. On estimating freezing times during tissue rapid freezing. J Microsc. 1984 Dec;136(Pt 3):349–360. doi: 10.1111/j.1365-2818.1984.tb00546.x. [DOI] [PubMed] [Google Scholar]
  14. Kuno M., Turkanis S. A., Weakly J. N. Correlation between nerve terminal size and transmitter release at the neuromuscular junction of the frog. J Physiol. 1971 Mar;213(3):545–556. doi: 10.1113/jphysiol.1971.sp009399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Orci L., Perrelet A., Dunant Y. A peculiar substructure in the postsynaptic membrane of Torpedo electroplax. Proc Natl Acad Sci U S A. 1974 Feb;71(2):307–310. doi: 10.1073/pnas.71.2.307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Takano Y., Kamiya H. Effect of ionic environment on densities of membrane-associated particles in presynaptic membranes observed in freeze-fractured synaptosomes. Experientia. 1979 Aug 15;35(8):1076–1078. doi: 10.1007/BF01949951. [DOI] [PubMed] [Google Scholar]
  17. Tokunaga A., Sandri C., Akert K. Increase of large intramembranous particles in the presynaptic active zone after administration of 4-aminopyridine. Brain Res. 1979 Oct 5;174(2):207–219. doi: 10.1016/0006-8993(79)90845-x. [DOI] [PubMed] [Google Scholar]
  18. Torri-Tarelli F., Grohovaz F., Fesce R., Ceccarelli B. Temporal coincidence between synaptic vesicle fusion and quantal secretion of acetylcholine. J Cell Biol. 1985 Oct;101(4):1386–1399. doi: 10.1083/jcb.101.4.1386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Venzin M., Sandri C., Akert S. K., Wyss U. R. Membrane associated particles of the presynaptic active zone in rat spinal cord. A morphometric analysis. Brain Res. 1977 Jul 22;130(3):393–404. doi: 10.1016/0006-8993(77)90104-4. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES