Skip to main content
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
. 1986 Feb;83(4):1115–1119. doi: 10.1073/pnas.83.4.1115

Facilitating and nonfacilitating synapses on pyramidal cells: a correlation between physiology and morphology.

J M Bower, L B Haberly
PMCID: PMC323022  PMID: 3081890

Abstract

Pyramidal cells in piriform cortex receive excitatory inputs from two different sources that are segregated onto adjacent segments of their apical dendrites. The present studies show that excitatory postsynaptic potentials (EPSPs) evoked by primary olfactory tract afferents that terminate on distal apical segments display paired shock facilitation whereas ESPSs evoked by intrinsic association fibers that terminate on proximal apical segments do not. An ultrastructural comparison of the presynaptic elements of these two fiber systems has revealed that the facilitating olfactory tract afferent synapses have a much lower packing density of synaptic vesicles than do the nonfacilitating association fiber synapses. Further, a search of the literature has revealed that where both morphological and physiological data are available for the same synapses, this same correlation appears to apply. We propose a hypothesis to account for this correlation based on synaptic vesicles to buffer internal calcium and the biochemical characteristics of preterminal calcium-dependent mechanisms affecting the number of vesicles available for release.

Full text

PDF
1115

Selected References

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

  1. BISHOP P. O., BURKE W., HAYHOW W. R. Repetitive stimulation of optic nerve and lateral geniculate synapses. Exp Neurol. 1959 Dec;1:534–555. doi: 10.1016/0014-4886(59)90016-0. [DOI] [PubMed] [Google Scholar]
  2. Bittner G. D. Differentiation of nerve terminals in the crayfish opener muscle and its functional significance. J Gen Physiol. 1968 Jun;51(6):731–758. doi: 10.1085/jgp.51.6.731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Caviness V. S., Jr, Korde M. G., Williams R. S. Cellular events induced in the molecular layer of the piriform cortex by ablation of the olfactory bulb in the mouse. Brain Res. 1977 Sep 23;134(1):13–34. doi: 10.1016/0006-8993(77)90922-2. [DOI] [PubMed] [Google Scholar]
  4. Chad J. E., Eckert R. Calcium domains associated with individual channels can account for anomalous voltage relations of CA-dependent responses. Biophys J. 1984 May;45(5):993–999. doi: 10.1016/S0006-3495(84)84244-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Collins W. F., 3rd, Honig M. G., Mendell L. M. Heterogeneity of group Ia synapses on homonymous alpha-motoneurons as revealed by high-frequency stimulation of Ia afferent fibers. J Neurophysiol. 1984 Nov;52(5):980–993. doi: 10.1152/jn.1984.52.5.980. [DOI] [PubMed] [Google Scholar]
  6. Conradi S., Cullheim S., Gollvik L., Kellerth J. O. Electron microscopic observations on the synaptic contacts of group Ia muscle spindle afferents in the cat lumbosacral spinal cord. Brain Res. 1983 Apr 11;265(1):31–39. doi: 10.1016/0006-8993(83)91330-6. [DOI] [PubMed] [Google Scholar]
  7. Dunant Y., Babel-Guéin E., Droz B. Calcium metabolism and acetylcholine release at the nerve-electroplaque junction. J Physiol (Paris) 1980 Sep;76(5):471–478. [PubMed] [Google Scholar]
  8. ECCLES J. C., OSCARSSON O., WILLIS W. D. Synaptic action of group I and II afferent fibres of muscle on the cells of the dorsal spinocerebellar tract. J Physiol. 1961 Oct;158:517–543. doi: 10.1113/jphysiol.1961.sp006783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Erulkar S. D. The modulation of neurotransmitter release at synaptic junctions. Rev Physiol Biochem Pharmacol. 1983;98:63–175. doi: 10.1007/BFb0033867. [DOI] [PubMed] [Google Scholar]
  10. Fyffe R. E., Light A. R. The ultrastructure of group Ia afferent fiber synapses in the lumbosacral spinal cord of the cat. Brain Res. 1984 May 23;300(2):201–209. doi: 10.1016/0006-8993(84)90831-x. [DOI] [PubMed] [Google Scholar]
  11. Gilbey M. P., Wooster M. J. Mono-and multi-synaptic origin of the early surface-negative wave recorded from guinea-pig olfactory cortex in vitro. J Physiol. 1979 Aug;293:153–172. doi: 10.1113/jphysiol.1979.sp012883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Haberly L. B., Bower J. M. Analysis of association fiber system in piriform cortex with intracellular recording and staining techniques. J Neurophysiol. 1984 Jan;51(1):90–112. doi: 10.1152/jn.1984.51.1.90. [DOI] [PubMed] [Google Scholar]
  13. Haberly L. B. Summed potentials evoked in opossum prepyriform cortex. J Neurophysiol. 1973 Jul;36(4):775–788. doi: 10.1152/jn.1973.36.4.775. [DOI] [PubMed] [Google Scholar]
  14. Haberly L., Behan M. Structure of the piriform cortex of the opossum. III. Ultrastructural characterization of synaptic terminals of association and olfactory bulb afferent fibers. J Comp Neurol. 1983 Oct 1;219(4):448–460. doi: 10.1002/cne.902190406. [DOI] [PubMed] [Google Scholar]
  15. Hirst G. D., Redman S. J., Wong K. Post-tetanic potentiation and facilitation of synaptic potentials evoked in cat spinal motoneurones. J Physiol. 1981 Dec;321:97–109. doi: 10.1113/jphysiol.1981.sp013973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hubbard J. I. Microphysiology of vertebrate neuromuscular transmission. Physiol Rev. 1973 Jul;53(3):674–723. doi: 10.1152/physrev.1973.53.3.674. [DOI] [PubMed] [Google Scholar]
  17. Huttner W. B., Schiebler W., Greengard P., De Camilli P. Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation. J Cell Biol. 1983 May;96(5):1374–1388. doi: 10.1083/jcb.96.5.1374. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Israël M., Manaranche R., Marsal J., Meunier F. M., Morel N., Frachon P., Lesbats B. Calcium uptake by cholinergic synaptic vesicles. J Physiol (Paris) 1980 Sep;76(5):479–485. [PubMed] [Google Scholar]
  19. Konnerth A., Heinemann U. Presynaptic involvement in frequency facilitation in the hippocampal slice. Neurosci Lett. 1983 Dec 11;42(3):255–260. doi: 10.1016/0304-3940(83)90271-9. [DOI] [PubMed] [Google Scholar]
  20. Kuno M., Weakly J. N. Facilitation of monosynaptic excitatory synaptic potentials in spinal motoneurones evoked by internuncial impulses. J Physiol. 1972 Jul;224(2):271–286. doi: 10.1113/jphysiol.1972.sp009894. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Landon D. N., Westgaard R. H., MacDermot J., Thompson E. J. The morphology of rat soleus neuromuscular junctions treated in vitro with purified beta-bungarotoxin. Brain Res. 1980 Nov 24;202(1):1–20. [PubMed] [Google Scholar]
  22. Llinás R., McGuinness T. L., Leonard C. S., Sugimori M., Greengard P. Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. Proc Natl Acad Sci U S A. 1985 May;82(9):3035–3039. doi: 10.1073/pnas.82.9.3035. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol. 1980 Aug;305:171–195. doi: 10.1113/jphysiol.1980.sp013357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. MACLEAN P. D., ROSNER B. S., ROBINSON F. Pyriform responses to electrical stimulation of olfactory fila, bulb and tract. Am J Physiol. 1957 May;189(2):395–400. doi: 10.1152/ajplegacy.1957.189.2.395. [DOI] [PubMed] [Google Scholar]
  25. Michaelson D. M., Avissar S., Ophir I., Pinchasi I., Angel I., Kloog Y., Sokolovsky M. On the regulation of acetylcholine release: a study utilizing Torpedo synaptosomes and synaptic vesicles. J Physiol (Paris) 1980 Sep;76(5):505–514. [PubMed] [Google Scholar]
  26. Nachshen D. A., Drapeau P. A buffering model for calcium-dependent neurotransmitter release. Biophys J. 1982 May;38(2):205–208. doi: 10.1016/S0006-3495(82)84548-7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Parnas H., Segel L. A. A theoretical explanation for some effects of calcium on the facilitation of neurotransmitter release. J Theor Biol. 1980 May 7;84(1):3–29. doi: 10.1016/s0022-5193(80)81035-6. [DOI] [PubMed] [Google Scholar]
  28. Parnas I., Parnas H., Dudel J. Neurotransmitter release and its facilitation in crayfish muscle. V. Basis for synapse differentiation of the fast and slow type in one axon. Pflugers Arch. 1982 Dec;395(4):261–270. doi: 10.1007/BF00580788. [DOI] [PubMed] [Google Scholar]
  29. Pumplin D. W., Reese T. S., Llinás R. Are the presynaptic membrane particles the calcium channels? Proc Natl Acad Sci U S A. 1981 Nov;78(11):7210–7213. doi: 10.1073/pnas.78.11.7210. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Rephaeli A., Parsons S. M. Calmodulin stimulation of 45Ca2+ transport and protein phosphorylation in cholinergic synaptic vesicles. Proc Natl Acad Sci U S A. 1982 Oct;79(19):5783–5787. doi: 10.1073/pnas.79.19.5783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Richards C. D. Potentiation and depression of synaptic transmission in the olfactory cortex of the guinea-pig. J Physiol. 1972 Apr;222(1):209–231. doi: 10.1113/jphysiol.1972.sp009794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Robson J. A., Mason C. A. The synaptic organization of terminals traced from individual labeled retino-geniculate axons in the cat. Neuroscience. 1979;4(1):99–111. doi: 10.1016/0306-4522(79)90220-3. [DOI] [PubMed] [Google Scholar]
  33. Schmidt R., Zimmermann H., Whittaker V. P. Metal ion content of cholinergic synaptic vesicles isolated from the electric organ of Torpedo: effect of stimulation-induced transmitter release. Neuroscience. 1980;5(3):625–638. doi: 10.1016/0306-4522(80)90060-3. [DOI] [PubMed] [Google Scholar]
  34. Scholfield C. N. A depolarizing inhibitory potential in neurones of the olfactory cortex in vitro. J Physiol. 1978 Feb;275:547–557. doi: 10.1113/jphysiol.1978.sp012207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Schwob J. E., Haberly L. B., Price J. L. The development of physiological responses of the piriform cortex in rats to stimulation of the lateral olfactory tract. J Comp Neurol. 1984 Feb 20;223(2):223–237. doi: 10.1002/cne.902230206. [DOI] [PubMed] [Google Scholar]
  36. Tauc L. Non vesicular release of neurotransmitter. Physiol Rev. 1982 Jul;62(3):857–893. doi: 10.1152/physrev.1982.62.3.857. [DOI] [PubMed] [Google Scholar]
  37. Tracey D. J., Walmsley B. Synaptic input from identified muscle afferents to neurones of the dorsal spinocerebellar tract in the cat. J Physiol. 1984 May;350:599–614. doi: 10.1113/jphysiol.1984.sp015220. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Winkelmann E., Brauer K., Marx I., David H. Elektronenmikroskopische und lichtmikroskopische Untersuchungen optischer und kortikaler Afferenzen im Corpus geniculatum laterale, pars dorsalis der Albinoratte unter besonderer Berücksichtigung der synaptischen Organisation. J Hirnforsch. 1976;17(4):305–333. [PubMed] [Google Scholar]
  39. Yamamoto C., McIlwain H. Electrical activities in thin sections from the mammalian brain maintained in chemically-defined media in vitro. J Neurochem. 1966 Dec;13(12):1333–1343. doi: 10.1111/j.1471-4159.1966.tb04296.x. [DOI] [PubMed] [Google Scholar]
  40. Zucker R. S., Stockbridge N. Presynaptic calcium diffusion and the time courses of transmitter release and synaptic facilitation at the squid giant synapse. J Neurosci. 1983 Jun;3(6):1263–1269. doi: 10.1523/JNEUROSCI.03-06-01263.1983. [DOI] [PMC free article] [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