Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1988 Oct;404:83–99. doi: 10.1113/jphysiol.1988.sp017280

The dependence of motoneurone membrane potential on extracellular ion concentrations studied in isolated rat spinal cord.

I D Forsythe 1, S J Redman 1
PMCID: PMC1190816  PMID: 2855355

Abstract

1. Intracellular recordings from ninety-nine motoneurones have been made in an in vitro hemisected spinal cord preparation. Their mean resting membrane potential in normal artificial cerebrospinal fluid (CSF) was -71 +/- 0.5 mV (+/- S.E.M.). The mean amplitude of the action potential was 84.0 +/- 1.4 mV (n = 50), and the mean input conductance was 101 +/- 7 nS (n = 49). 2. Both membrane potential and input conductance were sensitive to changes in [K+]o, [Na+]o, [Cl-]o and [Ca2+]o. 3. Replacement of extracellular Ca2+ by Mn2+ resulted in less than 1 mV hyperpolarization and a decrease in input conductance from 102 +/- 7 to 93 +/- 6 nS (n = 15). 4. At high [K+]o (greater than 10 mM) the membrane potential followed the potential predicted by the Nernst equation for K+ ions with a slope of 58 mV per 10-fold change in [K+]o. At low [K+]o (less than 10 mM) there was significant deviation from K+ equilibrium potential (EK). 5. [K+]i was found to be 106 mM when estimated from the reversal potential of the after-hyperpolarization of the antidromic action potential. 6. The reversal potential of the recurrent inhibitory postsynaptic potential (IPSP) in normal CSF was used to calculate [Cl-]i. This was 6.6 mM, which is less than would be expected if Cl- was passively distributed, indicating the presence of an outwardly directed Cl- pump. 7. Decreasing [Cl-]o from control (134 mM) to 4 mM resulted in a depolarization of 6.9 +/- 0.9 mV and a decrease in input conductance from 102 +/- 5 to 90 +/- 5 nS (n = 14) in 3 mM [K+]o. 8. Decreasing [Na+]o from 156 to 26 mM by substitution with choline resulted in a 6.2 +/- 0.5 mV hyperpolarization and a decrease in input conductance from from 102 +/- 4 to 76 +/- 4 nS (n = 5) in 3 mM [K+]o. 9. The input conductances for Na+, Cl- and K+ at the resting potential were calculated. After allowing for a microelectrode leak conductance, the relative input conductances were gNa/gK = 0.13 and gCl/gK = 0.25.

Full text

PDF
83

Images in this article

Selected References

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

  1. Adams P. R., Galvan M. Voltage-dependent currents of vertebrate neurons and their role in membrane excitability. Adv Neurol. 1986;44:137–170. [PubMed] [Google Scholar]
  2. BAKER P. F., HODGKIN A. L., SHAW T. I. The effects of changes in internal ionic concentrations on the electrical properties of perfused giant axons. J Physiol. 1962 Nov;164:355–374. doi: 10.1113/jphysiol.1962.sp007026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Belluzzi O., Sacchi O. A quantitative description of the sodium current in the rat sympathetic neurone. J Physiol. 1986 Nov;380:275–291. doi: 10.1113/jphysiol.1986.sp016285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bührle C. P., Sonnhof U. Intracellular ion activities and equilibrium potentials in motoneurones and glia cells of the frog spinal cord. Pflugers Arch. 1983 Feb;396(2):144–153. doi: 10.1007/BF00615519. [DOI] [PubMed] [Google Scholar]
  5. Bührle C. P., Sonnhof U. The ionic mechanism of the excitatory action of glutamate upon the membranes of motoneurones of the frog. Pflugers Arch. 1983 Feb;396(2):154–162. doi: 10.1007/BF00615520. [DOI] [PubMed] [Google Scholar]
  6. COOMBS J. S., ECCLES J. C., FATT P. The electrical properties of the motoneurone membrane. J Physiol. 1955 Nov 28;130(2):291–325. doi: 10.1113/jphysiol.1955.sp005411. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Czéh G., Kríz N., Syková E. Extracellular potassium accumulation in the frog spinal cord induced by stimulation of the skin and ventrolateral columns. J Physiol. 1981 Nov;320:57–72. doi: 10.1113/jphysiol.1981.sp013934. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Fulton B. P., Walton K. Electrophysiological properties of neonatal rat motoneurones studied in vitro. J Physiol. 1986 Jan;370:651–678. doi: 10.1113/jphysiol.1986.sp015956. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. GRANIT R., KERNELL D., SMITH R. S. DELAYED DEPOLARIZATION AND THE REPETITIVE RESPONSE TO INTRACELLULAR STIMULATION OF MAMMALIAN MOTONEURONES. J Physiol. 1963 Oct;168:890–910. doi: 10.1113/jphysiol.1963.sp007229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goldman D. E. POTENTIAL, IMPEDANCE, AND RECTIFICATION IN MEMBRANES. J Gen Physiol. 1943 Sep 20;27(1):37–60. doi: 10.1085/jgp.27.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Grafe P., Rimpel J., Reddy M. M., ten Bruggencate G. Changes of intracellular sodium and potassium ion concentrations in frog spinal motoneurons induced by repetitive synaptic stimulation. Neuroscience. 1982;7(12):3213–3220. doi: 10.1016/0306-4522(82)90243-3. [DOI] [PubMed] [Google Scholar]
  13. HODGKIN A. L., KATZ B. The effect of sodium ions on the electrical activity of giant axon of the squid. J Physiol. 1949 Mar 1;108(1):37–77. doi: 10.1113/jphysiol.1949.sp004310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. HUXLEY A. F., STAMPFLI R. Direct determination of membrane resting potential and action potential in single myelinated nerve fibers. J Physiol. 1951 Feb;112(3-4):476–495. doi: 10.1113/jphysiol.1951.sp004545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HUXLEY A. F., STAMPFLI R. Effect of potassium and sodium on resting and action potentials of single myelinated nerve fibers. J Physiol. 1951 Feb;112(3-4):496–508. doi: 10.1113/jphysiol.1951.sp004546. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. Hille B. The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. J Gen Physiol. 1967 May;50(5):1287–1302. doi: 10.1085/jgp.50.5.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hodgkin A. L., Huxley A. F. Resting and action potentials in single nerve fibres. J Physiol. 1945 Oct 15;104(2):176–195. doi: 10.1113/jphysiol.1945.sp004114. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Hösli L., Andrès P. F., Hösli E. Effects of potassium on the membrane potential of spinal neurones in tissue culture. Pflugers Arch. 1972;333(4):362–365. doi: 10.1007/BF00586215. [DOI] [PubMed] [Google Scholar]
  20. Iles J. F., Jack J. J. Ammonia mediated block of chloride pumping in cat motoneurones [proceedings]. J Physiol. 1978 Jul;280:20P–20P. [PubMed] [Google Scholar]
  21. Jiménez I., Rudomín P., Solodkin M., Vyklický L. Specific and nonspecific mechanisms involved in generation of PAD of group Ia afferents in cat spinal cord. J Neurophysiol. 1984 Nov;52(5):921–940. doi: 10.1152/jn.1984.52.5.921. [DOI] [PubMed] [Google Scholar]
  22. Llinas R., Baker R. A chloride-dependent inhibitory postsynaptic potential in cat trochlear motoneurons. J Neurophysiol. 1972 Jul;35(4):484–492. doi: 10.1152/jn.1972.35.4.484. [DOI] [PubMed] [Google Scholar]
  23. Llinas R., Baker R., Precht W. Blockage of inhibition by ammonium acetate action on chloride pump in cat trochlear motoneurons. J Neurophysiol. 1974 May;37(3):522–532. doi: 10.1152/jn.1974.37.3.522. [DOI] [PubMed] [Google Scholar]
  24. Lux H. D. Ammonium and chloride extrusion: hyperpolarizing synaptic inhibition in spinal motoneurons. Science. 1971 Aug 6;173(3996):555–557. doi: 10.1126/science.173.3996.555. [DOI] [PubMed] [Google Scholar]
  25. Lux H. D., Loracher C., Neher E. The action of ammonium on postsynaptic inhibition of cat spinal motoneurons. Exp Brain Res. 1970;11(5):431–447. doi: 10.1007/BF00233967. [DOI] [PubMed] [Google Scholar]
  26. Mayer M. L., Westbrook G. L. A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J Physiol. 1983 Jul;340:19–45. doi: 10.1113/jphysiol.1983.sp014747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Orkand R. K., Nicholls J. G., Kuffler S. W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J Neurophysiol. 1966 Jul;29(4):788–806. doi: 10.1152/jn.1966.29.4.788. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Schlue W. R., Deitmer J. W. Potassium distribution and membrane potential of sensory neurons in the leech nervous system. J Neurophysiol. 1984 Apr;51(4):689–704. doi: 10.1152/jn.1984.51.4.689. [DOI] [PubMed] [Google Scholar]
  30. Schwindt P. C., Crill W. E. Differential effects of TEA and cations on outward ionic currents of cat motoneurons. J Neurophysiol. 1981 Jul;46(1):1–16. doi: 10.1152/jn.1981.46.1.1. [DOI] [PubMed] [Google Scholar]
  31. Schwindt P. C., Crill W. E. Effects of barium on cat spinal motoneurons studied by voltage clamp. J Neurophysiol. 1980 Oct;44(4):827–846. doi: 10.1152/jn.1980.44.4.827. [DOI] [PubMed] [Google Scholar]
  32. Syková E. Extracellular K+ accumulation in the central nervous system. Prog Biophys Mol Biol. 1983;42(2-3):135–189. doi: 10.1016/0079-6107(83)90006-8. [DOI] [PubMed] [Google Scholar]
  33. Syková E., Orkand R. K. Extracellular potassium accumulation and transmission in frog spinal cord. Neuroscience. 1980;5(8):1421–1428. doi: 10.1016/0306-4522(80)90003-2. [DOI] [PubMed] [Google Scholar]
  34. Takahashi T., Tsuruhara H. Slow depolarizing potentials recorded from glial cells in the rat superficial dorsal horn. J Physiol. 1987 Jul;388:597–610. doi: 10.1113/jphysiol.1987.sp016633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Tasaki I., Byrne P. M. Mechanical changes in the amphibian spinal cord produced by afferent volleys of nerve impulses. Brain Res. 1984 Jun 3;301(2):265–272. doi: 10.1016/0006-8993(84)91095-3. [DOI] [PubMed] [Google Scholar]
  36. Walton K., Fulton B. P. Ionic mechanisms underlying the firing properties of rat neonatal motoneurons studied in vitro. Neuroscience. 1986 Nov;19(3):669–683. doi: 10.1016/0306-4522(86)90291-5. [DOI] [PubMed] [Google Scholar]
  37. Walton K., Fulton B. Hydrogen peroxide as a source of molecular oxygen for in vitro mammalian CNS preparations. Brain Res. 1983 Nov 14;278(1-2):387–393. doi: 10.1016/0006-8993(83)90280-9. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES