Skip to main content
Biophysical Journal logoLink to Biophysical Journal
. 2000 Mar;78(3):1106–1118. doi: 10.1016/S0006-3495(00)76669-0

Quantal potential fields around individual active zones of amphibian motor-nerve terminals.

M R Bennett 1, L Farnell 1, W G Gibson 1, G T Macleod 1, P Dickens 1
PMCID: PMC1300714  PMID: 10692301

Abstract

The release of a quantum from a nerve terminal is accompanied by the flow of extracellular current, which creates a field around the site of transmitter action. We provide a solution for the extent of this field for the case of a quantum released from a site on an amphibian motor-nerve terminal branch onto the receptor patch of a muscle fiber and compare this with measurements of the field using three extracellular electrodes. Numerical solution of the equations for the quantal potential field in cylindrical coordinates show that the density of the field at the peak of the quantal current gives rise to a peak extracellular potential, which declines approximately as the inverse of the distance from the source at distances greater than about 4 microm from the source along the length of the fiber. The peak extracellular potential declines to 20% of its initial value in a distance of about 6 microm, both along the length of the fiber and in the circumferential direction around the fiber. Simultaneous recordings of quantal potential fields, made with three electrodes placed in a line at right angles to an FM1-43 visualized branch, gave determinations of the field strengths in accord with the numerical solutions. In addition, the three electrodes were placed so as to straddle the visualized release sites of a branch. The positions of these sites were correctly predicted on the basis of the theory and independently ascertained by FM1-43 staining of the sites. It is concluded that quantal potential fields at the neuromuscular junction that can be measured with available recording techniques are restricted to regions within about 10 microm of the release site.

Full Text

The Full Text of this article is available as a PDF (256.0 KB).

Selected References

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

  1. Adrian R. H., Almers W. Measurement of membrane capacity in skeletal muscle. Nat New Biol. 1973 Mar 14;242(115):62–64. doi: 10.1038/newbio242062a0. [DOI] [PubMed] [Google Scholar]
  2. Altman K. W., Plonsey R. Development of a model for point source electrical fibre bundle stimulation. Med Biol Eng Comput. 1988 Sep;26(5):466–475. doi: 10.1007/BF02441913. [DOI] [PubMed] [Google Scholar]
  3. Bennet M. R., Lavidis N. A. Variation in quantal secretion at different release sites along developing and mature motor terminal branches. Brain Res. 1982 Sep;281(1):1–9. doi: 10.1016/0165-3806(82)90107-9. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Bennett M. R., Gibson W. G. On the contribution of quantal secretion from close-contact and loose-contact varicosities to the synaptic potentials in the vas deferens. Philos Trans R Soc Lond B Biol Sci. 1995 Jan 30;347(1320):187–204. doi: 10.1098/rstb.1995.0021. [DOI] [PubMed] [Google Scholar]
  6. Bennett M. R., Gibson W. G., Poznanski R. R. Extracellular current flow and potential during quantal transmission from varicosities in a smooth muscle syncytium. Philos Trans R Soc Lond B Biol Sci. 1993 Oct 29;342(1300):89–99. doi: 10.1098/rstb.1993.0140. [DOI] [PubMed] [Google Scholar]
  7. Bennett M. R., Jones P., Lavidis N. A. The probability of quantal secretion along visualized terminal branches at amphibian (Bufo marinus) neuromuscular synapses. J Physiol. 1986 Oct;379:257–274. doi: 10.1113/jphysiol.1986.sp016252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Betz W. J., Bewick G. S. Optical monitoring of transmitter release and synaptic vesicle recycling at the frog neuromuscular junction. J Physiol. 1993 Jan;460:287–309. doi: 10.1113/jphysiol.1993.sp019472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Clark J., Plonsey R. The extracellular potential field of the single active nerve fiber in a volume conductor. Biophys J. 1968 Jul;8(7):842–864. doi: 10.1016/S0006-3495(68)86524-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. D'Alonzo A. J., Grinnell A. D. Profiles of evoked release along the length of frog motor nerve terminals. J Physiol. 1985 Feb;359:235–258. doi: 10.1113/jphysiol.1985.sp015583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. DEL CASTILLO J., KATZ B. Localization of active spots within the neuromuscular junction of the frog. J Physiol. 1956 Jun 28;132(3):630–649. doi: 10.1113/jphysiol.1956.sp005554. [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. Engel E., Barcilon V., Eisenberg R. S. The interpretation of current-voltage relations recorded from a spherical cell with a single microelectrode. Biophys J. 1972 Apr;12(4):384–403. doi: 10.1016/S0006-3495(72)86091-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Forti L., Bossi M., Bergamaschi A., Villa A., Malgaroli A. Loose-patch recordings of single quanta at individual hippocampal synapses. Nature. 1997 Aug 28;388(6645):874–878. doi: 10.1038/42251. [DOI] [PubMed] [Google Scholar]
  16. Gage P. W., Armstrong C. M. Miniature end-plate currents in voltage-clamped muscle fibre. Nature. 1968 Apr 27;218(5139):363–365. doi: 10.1038/218363b0. [DOI] [PubMed] [Google Scholar]
  17. Gundersen C. B., Katz B., Miledi R. The reduction of endplate responses by botulinum toxin. Proc R Soc Lond B Biol Sci. 1981 Nov 24;213(1193):489–493. doi: 10.1098/rspb.1981.0077. [DOI] [PubMed] [Google Scholar]
  18. Henery R., Gibson W. G., Bennett M. R. Quantal currents and potential in the three-dimensional anisotropic bidomain model of smooth muscle. Bull Math Biol. 1997 Nov;59(6):1047–1075. doi: 10.1007/BF02460101. [DOI] [PubMed] [Google Scholar]
  19. Hodgkin A. L., Nakajima S. Analysis of the membrane capacity in frog muscle. J Physiol. 1972 Feb;221(1):121–136. doi: 10.1113/jphysiol.1972.sp009743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Hodgkin A. L., Nakajima S. The effect of diameter on the electrical constants of frog skeletal muscle fibres. J Physiol. 1972 Feb;221(1):105–120. doi: 10.1113/jphysiol.1972.sp009742. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. KATZ B., MILEDI R. PROPAGATION OF ELECTRIC ACTIVITY IN MOTOR NERVE TERMINALS. Proc R Soc Lond B Biol Sci. 1965 Feb 16;161:453–482. doi: 10.1098/rspb.1965.0015. [DOI] [PubMed] [Google Scholar]
  22. KATZ B., THESLEFF S. On the factors which determine the amplitude of the miniature end-plate potential. J Physiol. 1957 Jul 11;137(2):267–278. doi: 10.1113/jphysiol.1957.sp005811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Katz B., Miledi R. Release of acetylcholine from a nerve terminal by electric pulses of variable strength and duration. Nature. 1965 Sep 4;207(5001):1097–1098. doi: 10.1038/2071097a0. [DOI] [PubMed] [Google Scholar]
  24. Lavidis N. A., Bennett M. R. Probabilistic secretion of quanta from visualized sympathetic nerve varicosities in mouse vas deferens. J Physiol. 1992 Aug;454:9–26. doi: 10.1113/jphysiol.1992.sp019252. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Macleod G. T., Gan J., Bennett M. R. Vesicle-associated proteins and quantal release at single active zones of amphibian (Bufo marinus) motor-nerve terminals. J Neurophysiol. 1999 Sep;82(3):1133–1146. doi: 10.1152/jn.1999.82.3.1133. [DOI] [PubMed] [Google Scholar]
  26. Magleby K. L., Stevens C. F. A quantitative description of end-plate currents. J Physiol. 1972 May;223(1):173–197. doi: 10.1113/jphysiol.1972.sp009840. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Muler A. L., Markin V. S. Elektricheskie svoistva anizotropnykh nervno-myshechnykh sintsitiev. III. Statsionarnaia forma fronta vozbuzhdeniia. Biofizika. 1977 Jul-Aug;22(4):671–675. [PubMed] [Google Scholar]
  28. Peskoff A. Electric potential in cylindrical syncytia and muscle fibers. Bull Math Biol. 1979;41(2):183–192. doi: 10.1007/BF02460877. [DOI] [PubMed] [Google Scholar]
  29. Peskoff A. Electric potential in three-dimensional electrically syncytial tissues. Bull Math Biol. 1979;41(2):163–181. doi: 10.1007/BF02460876. [DOI] [PubMed] [Google Scholar]
  30. Rattay F. Analysis of models for external stimulation of axons. IEEE Trans Biomed Eng. 1986 Oct;33(10):974–977. doi: 10.1109/TBME.1986.325670. [DOI] [PubMed] [Google Scholar]
  31. Rattay F. Analysis of models for extracellular fiber stimulation. IEEE Trans Biomed Eng. 1989 Jul;36(7):676–682. doi: 10.1109/10.32099. [DOI] [PubMed] [Google Scholar]
  32. Rattay F. Ways to approximate current-distance relations for electrically stimulated fibers. J Theor Biol. 1987 Apr 7;125(3):339–349. doi: 10.1016/s0022-5193(87)80066-8. [DOI] [PubMed] [Google Scholar]
  33. Robitaille R., Tremblay J. P. Frequency and amplitude gradients of spontaneous release along the length of the frog neuromuscular junction. Synapse. 1989;3(4):291–307. doi: 10.1002/syn.890030402. [DOI] [PubMed] [Google Scholar]
  34. Robitaille R., Tremblay J. P., Grenon G. Interrelation between MEPP amplitude and MEPP frequency in different regions along the frog neuromuscular junction. Brain Res. 1987 Apr 7;408(1-2):353–358. doi: 10.1016/0006-8993(87)90404-5. [DOI] [PubMed] [Google Scholar]
  35. Stephanova D., Trayanova N., Gydikov A., Kossev A. Extracellular potentials of a single myelinated nerve fiber in an unbounded volume conductor. Biol Cybern. 1989;61(3):205–210. doi: 10.1007/BF00198767. [DOI] [PubMed] [Google Scholar]
  36. Thomson P. C., Lavidis N. A., Robinson J., Bennett M. R. Probabilistic secretion of quanta at somatic motor-nerve terminals: the fusion-pore model, quantal detection and autoinhibition. Philos Trans R Soc Lond B Biol Sci. 1995 Aug 29;349(1328):197–214. doi: 10.1098/rstb.1995.0103. [DOI] [PubMed] [Google Scholar]
  37. Trayanova N., Henriquez C. S., Plonsey R. Extracellular potentials and currents of a single active fiber in a restricted volume conductor. Ann Biomed Eng. 1990;18(3):219–238. doi: 10.1007/BF02368439. [DOI] [PubMed] [Google Scholar]
  38. Tremblay J. P., Robitaille R., Grenon G. Distribution of spontaneous release along the frog neuromuscular junction. Neurosci Lett. 1984 Oct 12;51(2):247–252. doi: 10.1016/0304-3940(84)90559-7. [DOI] [PubMed] [Google Scholar]
  39. Van der Kloot W., Cohen I. Localizing the site of generation of uni-quantal endplate potentials using two intracellular microelectrodes. Neurosci Lett. 1985 Nov 20;62(1):57–62. doi: 10.1016/0304-3940(85)90284-8. [DOI] [PubMed] [Google Scholar]
  40. Van der Kloot W., Naves L. A. Localizing quantal currents along frog neuromuscular junctions. J Physiol. 1996 Nov 15;497(Pt 1):189–198. doi: 10.1113/jphysiol.1996.sp021759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Wernig A. Estimates of statistical release parameters from crayfish and frog neuromuscular junctions. J Physiol. 1975 Jan;244(1):207–221. doi: 10.1113/jphysiol.1975.sp010792. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Wernig A. Localization of active sites in the neuromuscular junction of the frog. Brain Res. 1976 Dec 10;118(1):63–72. doi: 10.1016/0006-8993(76)90841-6. [DOI] [PubMed] [Google Scholar]
  43. Zefirov A. L., Benish T. V., Fatkullin N. F., Cheranov S. Iu. Analiz sekretsii mediatora v aktivnoi zone dvigatel'nogo nervnogo okonchaniia. Neirofiziologiia. 1990;22(3):318–327. [PubMed] [Google Scholar]
  44. Zefirov A., Benish T., Fatkullin N., Cheranov S., Khazipov R. Localization of active zones. Nature. 1995 Aug 3;376(6539):393–394. doi: 10.1038/376393b0. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES