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Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1998 Feb 22;265(1393):271–277. doi: 10.1098/rspb.1998.0292

On the origin of skewed distributions of spontaneous synaptic potentials in autonomic ganglia.

M R Bennett 1, L Farnell 1, W G Gibson 1
PMCID: PMC1688881  PMID: 9523429

Abstract

The histograms of spontaneous synaptic potentials at synapses in autonomic ganglia are described by distributions consisting of mixtures of Gaussians, rather than by single Gaussian distributions. The possible origin of these mixed distributions is investigated, using Monte-Carlo simulations of the action of spontaneously released units of transmitter. A single unit of acetylcholine of fixed size, released from an active zone with receptor patches both beneath and adjacent to the zone, does not give rise to the observed histograms. But if the unit is of variable size, consisting of integer multiples of smaller units, and release is from an active zone onto either the receptor patch beneath, or in addition onto adjacent patches, then the histogram is well described by a mixture of Gaussians. However, this explanation is unlikely to be correct as present evidence suggests that in most cases the released unit of transmitter saturates the postsynaptic receptor patch beneath the active zone. The final case considered is where a unit of transmitter is spontaneously released from an active zone, simultaneously with a unit in an adjacent zone less than one micron away. The histogram of potentials then conforms to those observed even when there are differences in the sizes of the receptor patches. It is suggested that this kind of release could provide an explanation for distributions of spontaneous potentials that are mixtures of Gaussians.

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Selected References

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

  1. Bartol T. M., Jr, Land B. R., Salpeter E. E., Salpeter M. M. Monte Carlo simulation of miniature endplate current generation in the vertebrate neuromuscular junction. Biophys J. 1991 Jun;59(6):1290–1307. doi: 10.1016/S0006-3495(91)82344-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bennett M. R., Brain K. Autonomic synaptic transmission at single boutons and calyces. J Neurocytol. 1997 Sep;26(9):577–603. doi: 10.1023/a:1018537625551. [DOI] [PubMed] [Google Scholar]
  3. Bennett M. R., Farnell L., Gibson W. G., Lavidis N. A. Synaptic transmission at visualized sympathetic boutons: stochastic interaction between acetylcholine and its receptors. Biophys J. 1997 Apr;72(4):1595–1606. doi: 10.1016/S0006-3495(97)78806-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bennett M. R., Farnell L., Gibson W. G. Quantal transmitter release onto different patterns of receptor distributions at somatic neuromuscular junctions. J Theor Biol. 1996 Nov 21;183(2):231–236. doi: 10.1006/jtbi.1996.0216. [DOI] [PubMed] [Google Scholar]
  5. Bennett M. R., Gibson W. G., Robinson J. Probabilistic secretion of quanta and the synaptosecretosome hypothesis: evoked release at active zones of varicosities, boutons, and endplates. Biophys J. 1997 Oct;73(4):1815–1829. doi: 10.1016/S0006-3495(97)78212-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bennett M. R., Gibson W. G., Robinson J. Probabilistic secretion of quanta: spontaneous release at active zones of varicosities, boutons, and endplates. Biophys J. 1995 Jul;69(1):42–56. doi: 10.1016/S0006-3495(95)79873-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bennett M. R. The origin of Gaussian distributions of synaptic potentials. Prog Neurobiol. 1995 Jul;46(4):331–350. doi: 10.1016/0301-0082(94)00061-l. [DOI] [PubMed] [Google Scholar]
  8. Blackman J. G., Purves R. D. Intracellular recordings from ganglia of the thoracic sympathetic chain of the guinea-pig. J Physiol. 1969 Jul;203(1):173–198. doi: 10.1113/jphysiol.1969.sp008858. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bootman M. D., Berridge M. J. The elemental principles of calcium signaling. Cell. 1995 Dec 1;83(5):675–678. doi: 10.1016/0092-8674(95)90179-5. [DOI] [PubMed] [Google Scholar]
  10. Bornstein J. C. Spontaneous multiquantal release at synapses in guinea-pig hypogastric ganglia: evidence that release can occur in bursts. J Physiol. 1978 Sep;282:375–398. doi: 10.1113/jphysiol.1978.sp012470. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Brain K. L., Bennett M. R. Calcium in sympathetic varicosities of mouse vas deferens during facilitation, augmentation and autoinhibition. J Physiol. 1997 Aug 1;502(Pt 3):521–536. doi: 10.1111/j.1469-7793.1997.521bj.x. [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. Dennis M. J., Harris A. J., Kuffler S. W. Synaptic transmission and its duplication by focally applied acetylcholine in parasympathetic neurons in the heart of the frog. Proc R Soc Lond B Biol Sci. 1971 Apr 27;177(1049):509–539. doi: 10.1098/rspb.1971.0045. [DOI] [PubMed] [Google Scholar]
  14. Derkach V. A., Selyanko A. A., Skok V. I. Acetylcholine-induced current fluctuations and fast excitatory post-synaptic currents in rabbit sympathetic neurones. J Physiol. 1983 Mar;336:511–526. doi: 10.1113/jphysiol.1983.sp014595. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Erxleben C., Kriebel M. E. Characteristics of spontaneous miniature and subminiature end-plate currents at the mouse neuromuscular junction. J Physiol. 1988 Jun;400:645–658. doi: 10.1113/jphysiol.1988.sp017141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. FATT P., KATZ B. Spontaneous subthreshold activity at motor nerve endings. J Physiol. 1952 May;117(1):109–128. [PMC free article] [PubMed] [Google Scholar]
  17. Hartzell H. C., Kuffler S. W., Yoshikami D. The number of acetylcholine molecules in a quantum and the interaction between quanta at the subsynaptic membrane of the skeletal neuromuscular synapse. Cold Spring Harb Symp Quant Biol. 1976;40:175–186. doi: 10.1101/sqb.1976.040.01.019. [DOI] [PubMed] [Google Scholar]
  18. Hirst G. D., McLachlan E. M. Post-natal development of ganglia in the lower lumbar sympathetic chain of the rat. J Physiol. 1984 Apr;349:119–134. doi: 10.1113/jphysiol.1984.sp015147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Horch H. L., Sargent P. B. Perisynaptic surface distribution of multiple classes of nicotinic acetylcholine receptors on neurons in the chicken ciliary ganglion. J Neurosci. 1995 Dec;15(12):7778–7795. doi: 10.1523/JNEUROSCI.15-12-07778.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. MARTIN A. R., PILAR G. QUANTAL COMPONENTS OF THE SYNAPTIC POTENTIAL IN THE CILIARY GANGLION OF THE CHICK. J Physiol. 1964 Dec;175:1–16. doi: 10.1113/jphysiol.1964.sp007499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Margiotta J. F., Berg D. K., Dionne V. E. The properties and regulation of functional acetylcholine receptors on chick ciliary ganglion neurons. J Neurosci. 1987 Nov;7(11):3612–3622. doi: 10.1523/JNEUROSCI.07-11-03612.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Melamed N., Helm P. J., Rahamimoff R. Confocal microscopy reveals coordinated calcium fluctuations and oscillations in synaptic boutons. J Neurosci. 1993 Feb;13(2):632–649. doi: 10.1523/JNEUROSCI.13-02-00632.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Miledi R., Molenaar P. C., Polak R. L. Free and bound acetylcholine in frog muscle. J Physiol. 1982 Dec;333:189–199. doi: 10.1113/jphysiol.1982.sp014448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rang H. P. The characteristics of synaptic currents and responses to acetylcholine of rat submandibular ganglion cells. J Physiol. 1981 Feb;311:23–55. doi: 10.1113/jphysiol.1981.sp013571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Robinson J. Estimation of parameters for a model of transmitter release at synapses. Biometrics. 1976 Mar;32(1):61–68. [PubMed] [Google Scholar]
  26. Sargent P. B., Pang D. Z. Acetylcholine receptor-like molecules are found in both synaptic and extrasynaptic clusters on the surface of neurons in the frog cardiac ganglion. J Neurosci. 1989 Mar;9(3):1062–1072. doi: 10.1523/JNEUROSCI.09-03-01062.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sargent P. B. The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci. 1993;16:403–443. doi: 10.1146/annurev.ne.16.030193.002155. [DOI] [PubMed] [Google Scholar]
  28. Sitsapesan R., McGarry S. J., Williams A. J. Cyclic ADP-ribose, the ryanodine receptor and Ca2+ release. Trends Pharmacol Sci. 1995 Nov;16(11):386–391. doi: 10.1016/s0165-6147(00)89080-x. [DOI] [PubMed] [Google Scholar]
  29. Stern M. D. Theory of excitation-contraction coupling in cardiac muscle. Biophys J. 1992 Aug;63(2):497–517. doi: 10.1016/S0006-3495(92)81615-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Warren D., Lavidis N. A., Bennett M. R. Quantal secretion from visualized boutons on rat pelvic ganglion neurones. J Auton Nerv Syst. 1996 Jan 5;56(3):175–183. doi: 10.1016/0165-1838(95)00087-9. [DOI] [PubMed] [Google Scholar]
  31. Wathey J. C., Nass M. M., Lester H. A. Numerical reconstruction of the quantal event at nicotinic synapses. Biophys J. 1979 Jul;27(1):145–164. doi: 10.1016/S0006-3495(79)85208-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wilson Horch H. L., Sargent P. B. Synaptic and extrasynaptic distribution of two distinct populations of nicotinic acetylcholine receptor clusters in the frog cardiac ganglion. J Neurocytol. 1996 Jan;25(1):67–77. doi: 10.1007/BF02284786. [DOI] [PubMed] [Google Scholar]
  33. Yamada W. M., Zucker R. S. Time course of transmitter release calculated from simulations of a calcium diffusion model. Biophys J. 1992 Mar;61(3):671–682. doi: 10.1016/S0006-3495(92)81872-6. [DOI] [PMC free article] [PubMed] [Google Scholar]

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