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. 1985 Nov;368:627–640. doi: 10.1113/jphysiol.1985.sp015880

Characterization of miniature inhibitory post-synaptic potentials in rat spinal motoneurones.

H Kojima, T Takahashi
PMCID: PMC1192619  PMID: 4078752

Abstract

Intracellular recordings were made from motoneurones in the isolated spinal cord of neonatal rats. After action potentials had been abolished by tetrodotoxin (TTX, 10(-6) g/ml), small (approximately 0.4 mV) depolarizing potentials occurred spontaneously in motoneurones at low frequencies (approximately 1.5 Hz). These potentials were detectable only after the intracellular Cl- concentration of motoneurones was raised by using KCl electrodes and most of them were blocked by strychnine, suggesting that they are inhibitory post-synaptic potentials (i.p.s.p.s). These spontaneous i.p.s.p.s under TTX are designated as 'miniature i.p.s.p.s' in order to distinguish them from i.p.s.p.s arising from spontaneous impulse activities of interneurones or afferent fibres. The miniature i.p.s.p.s were still observed after Ca2+ in saline was substituted by Mg2+ or Mn2+. In low Ca2+ and high Mg2+ saline, the amplitude distribution of miniature i.p.s.p.s was essentially the same as in normal saline. The frequency of miniature i.p.s.p.s increased when external Ca2+ concentration was raised. The frequency decreased to about 60% of the control when external Ca2+ was substituted by Mg2+ (2-4 mM), whereas it increased to more than 20-fold when substituted by Mn2+ (3-5 mM). When the external K+ concentration was raised, the frequency of miniature i.p.s.p.s under TTX increased non-linearly with the K+ concentration. The maximum slope in the relation between the log frequency and log K+ concentration was about 3.6. When the osmotic pressure was increased by adding sucrose, miniature i.p.s.p.s increased in frequency. The effect of osmotic pressure was relatively mild compared with that reported for the miniature end-plate potentials (e.p.p.s) in the frog. When the temperature was raised, the frequency of miniature i.p.s.p.s increased. The relation between frequency and temperature fitted approximately to a straight line in Arrhenius plot with a Q10 of about 2.6. These characteristics of the miniature i.p.s.p.s closely resemble those of the miniature e.p.p.s. It is concluded that the miniature i.p.s.p.s recorded in motoneurones are equivalent in nature to the miniature e.p.p.s in neuromuscular junctions, thus reflecting the spontaneous release of quantal packages of the inhibitory transmitter.

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Selected References

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  1. ARAKI T., ITO M., OSCARSSON O. Anion permeability of the synaptic and non-synaptic motoneurone membrane. J Physiol. 1961 Dec;159:410–435. doi: 10.1113/jphysiol.1961.sp006818. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alnaes E., Rahamimoff R. On the role of mitochondria in transmitter release from motor nerve terminals. J Physiol. 1975 Jun;248(2):285–306. doi: 10.1113/jphysiol.1975.sp010974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. BOYD I. A., MARTIN A. R. Spontaneous subthreshold activity at mammalian neural muscular junctions. J Physiol. 1956 Apr 27;132(1):61–73. doi: 10.1113/jphysiol.1956.sp005502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. BROCK L. G., COOMBS J. S., ECCLES J. C. The recording of potentials from motoneurones with an intracellular electrode. J Physiol. 1952 Aug;117(4):431–460. doi: 10.1113/jphysiol.1952.sp004759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Balnave R. J., Gage P. W. The inhibitory effect of manganese on transmitter release at the neuromuscular junction of the toad. Br J Pharmacol. 1973 Feb;47(2):339–352. doi: 10.1111/j.1476-5381.1973.tb08332.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Barton S. B., Cohen I. S., van der Kloot W. The calcium dependence of spontaneous and evoked quantal release at the frog neuromuscular junction. J Physiol. 1983 Apr;337:735–751. doi: 10.1113/jphysiol.1983.sp014652. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blankenship J. E., Kuno M. Analysis of spontaneous subthreshold activity in spinal motoneurons of the cat. J Neurophysiol. 1968 Mar;31(2):195–209. doi: 10.1152/jn.1968.31.2.195. [DOI] [PubMed] [Google Scholar]
  8. Blioch Z. L., Glagoleva I. M., Liberman E. A., Nenashev V. A. A study of the mechanism of quantal transmitter release at a chemical synapse. J Physiol. 1968 Nov;199(1):11–35. doi: 10.1113/jphysiol.1968.sp008637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown T. H., Wong R. K., Prince D. A. Spontaneous miniature synaptic potentials in hippocampal neurons. Brain Res. 1979 Nov 9;177(1):194–199. doi: 10.1016/0006-8993(79)90931-4. [DOI] [PubMed] [Google Scholar]
  10. Colomo F., Erulkar S. D. Miniature synaptic potentials at frog spinal neurones in the presence of tertodotoxin. J Physiol. 1968 Nov;199(1):205–221. doi: 10.1113/jphysiol.1968.sp008649. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cull-Candy S. G., Miledi R., Trautmann A., Uchitel O. D. On the release of transmitter at normal, myasthenia gravis and myasthenic syndrome affected human end-plates. J Physiol. 1980 Feb;299:621–638. doi: 10.1113/jphysiol.1980.sp013145. [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. Edwards F. R., Redman S. J., Walmsley B. Non-quantal fluctuations and transmission failures in charge transfer at Ia synapses on spinal motoneurones. J Physiol. 1976 Aug;259(3):689–704. doi: 10.1113/jphysiol.1976.sp011489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Edwards F. R., Redman S. J., Walmsley B. Statistical fluctuations in charge transfer at Ia synapses on spinal motoneurones. J Physiol. 1976 Aug;259(3):665–688. doi: 10.1113/jphysiol.1976.sp011488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Elmqvist D., Feldman D. S. Calcium dependence of spontaneous acetylcholine release at mammalian motor nerve terminals. J Physiol. 1965 Dec;181(3):487–497. doi: 10.1113/jphysiol.1965.sp007777. [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. FURSHPAN E. J. The effects of osmotic pressure changes on the spontaneous activity at motor nerve endings. J Physiol. 1956 Dec 28;134(3):689–697. doi: 10.1113/jphysiol.1956.sp005675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fulton B. P., Miledi R., Takahashi T. Electrical synapses between motoneurons in the spinal cord of the newborn rat. Proc R Soc Lond B Biol Sci. 1980 Jun 23;208(1170):115–120. doi: 10.1098/rspb.1980.0045. [DOI] [PubMed] [Google Scholar]
  19. HUBBARD J. I. The effect of calcium and magnesium on the spontaneous release of transmitter from mammalian motor nerve endings. J Physiol. 1961 Dec;159:507–517. doi: 10.1113/jphysiol.1961.sp006824. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Harada Y., Takahashi T. The calcium component of the action potential in spinal motoneurones of the rat. J Physiol. 1983 Feb;335:89–100. doi: 10.1113/jphysiol.1983.sp014521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Hofmann W. W., Parsons R. L., Feigen G. A. Effects of temperature and drugs on mammalian motor nerve terminals. Am J Physiol. 1966 Jul;211(1):135–140. doi: 10.1152/ajplegacy.1966.211.1.135. [DOI] [PubMed] [Google Scholar]
  22. Hubbard J. I., Jones S. F., Landau E. M. An examination of the effects of osmotic pressure changes upon transmitter release from mammalian motor nerve terminals. J Physiol. 1968 Aug;197(3):639–657. doi: 10.1113/jphysiol.1968.sp008579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hubbard J. I., Jones S. F., Landau E. M. On the mechanism by which calcium and magnesium affect the spontaneous release of transmitter from mammalian motor nerve terminals. J Physiol. 1968 Feb;194(2):355–380. doi: 10.1113/jphysiol.1968.sp008413. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Hubbard J. I., Stenhouse D., Eccles R. M. Origin of synaptic noise. Science. 1967 Jul 21;157(3786):330–331. doi: 10.1126/science.157.3786.330. [DOI] [PubMed] [Google Scholar]
  25. Jack J. J., Redman S. J., Wong K. The components of synaptic potentials evoked in cat spinal motoneurones by impulses in single group Ia afferents. J Physiol. 1981 Dec;321:65–96. doi: 10.1113/jphysiol.1981.sp013972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. KATZ B., MILEDI R. A STUDY OF SPONTANEOUS MINIATURE POTENTIALS IN SPINAL MOTONEURONES. J Physiol. 1963 Sep;168:389–422. doi: 10.1113/jphysiol.1963.sp007199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. KUNO M. QUANTAL COMPONENTS OF EXCITATORY SYNAPTIC POTENTIALS IN SPINAL MOTONEURONES. J Physiol. 1964 Dec;175:81–99. doi: 10.1113/jphysiol.1964.sp007504. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Katz B., Miledi R. A study of synaptic transmission in the absence of nerve impulses. J Physiol. 1967 Sep;192(2):407–436. doi: 10.1113/jphysiol.1967.sp008307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Katz B., Miledi R. Tetrodotoxin-resistant electric activity in presynaptic terminals. J Physiol. 1969 Aug;203(2):459–487. doi: 10.1113/jphysiol.1969.sp008875. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Kuno M. Quantum aspects of central and ganglionic synaptic transmission in vertebrates. Physiol Rev. 1971 Oct;51(4):647–678. doi: 10.1152/physrev.1971.51.4.647. [DOI] [PubMed] [Google Scholar]
  31. Kuno M., Weakly J. N. Quantal components of the inhibitory synaptic potential in spinal mononeurones of the cat. J Physiol. 1972 Jul;224(2):287–303. doi: 10.1113/jphysiol.1972.sp009895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. LILEY A. W. An investigation of spontaneous activity at the neuromuscular junction of the rat. J Physiol. 1956 Jun 28;132(3):650–666. doi: 10.1113/jphysiol.1956.sp005555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Landau E. M. The interaction of presynaptic polarization with calcium and magnesium in modifying spontaneous transmitter release from mammalian motor nerve terminals. J Physiol. 1969 Aug;203(2):281–299. doi: 10.1113/jphysiol.1969.sp008864. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Lederer W. J., Spindler A. J., Eisner D. A. Thick slurry bevelling: a new technique for bevelling extremely fine microelectrodes and micropipettes. Pflugers Arch. 1979 Sep;381(3):287–288. doi: 10.1007/BF00583261. [DOI] [PubMed] [Google Scholar]
  35. Miledi R., Thies R. Tetanic and post-tetanic rise in frequency of miniature end-plate potentials in low-calcium solutions. J Physiol. 1971 Jan;212(1):245–257. doi: 10.1113/jphysiol.1971.sp009320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Miledi R. Transmitter release induced by injection of calcium ions into nerve terminals. Proc R Soc Lond B Biol Sci. 1973 Jul 3;183(1073):421–425. doi: 10.1098/rspb.1973.0026. [DOI] [PubMed] [Google Scholar]
  37. Otsuka M., Konishi S. Electrophysiology of mammalian spinal cord in vitro. Nature. 1974 Dec 20;252(5485):733–734. doi: 10.1038/252733a0. [DOI] [PubMed] [Google Scholar]
  38. Redman S. Junctional mechanisms at group Ia synapses. Prog Neurobiol. 1979;12(1):33–83. doi: 10.1016/0301-0082(79)90010-8. [DOI] [PubMed] [Google Scholar]
  39. Shapovalov A. I., Shiriaev B. I., Tamarova Z. A. Synaptic activity in motoneurons of the immature cat spinal cord in vitro. Effects of manganese and tetrodotoxin. Brain Res. 1979 Jan 19;160(3):524–528. doi: 10.1016/0006-8993(79)91080-1. [DOI] [PubMed] [Google Scholar]
  40. Takahashi T. Inhibitory miniature synaptic potentials in rat motoneurons. Proc R Soc Lond B Biol Sci. 1984 Mar 22;221(1222):103–109. doi: 10.1098/rspb.1984.0025. [DOI] [PubMed] [Google Scholar]
  41. Takahashi T. Intracellular recording from visually identified motoneurons in rat spinal cord slices. Proc R Soc Lond B Biol Sci. 1978 Jul 26;202(1148):417–421. doi: 10.1098/rspb.1978.0076. [DOI] [PubMed] [Google Scholar]
  42. Ward D., Crowley W. J., Johns T. R. Effects of temperature at the neuromuscular junction. Am J Physiol. 1972 Jan;222(1):216–219. doi: 10.1152/ajplegacy.1972.222.1.216. [DOI] [PubMed] [Google Scholar]

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