Advertisement

Membrane Noise Analysis

  • Harold Lecar
  • Frederick Sachs

Abstract

The fundamental units of excitability are membrane ionic channels. Excitation requires fast switches in membrane permeability, and these are effected by channels that are ion-selective and can be “gated” open and closed. A variety of experimental methods have contributed to establishing the present picture of discrete channels of molecular dimensions, each capable of carrying a rather high ion flux. In this chapter, we discuss an experimental method, membrane noise analysis, which allows one to estimate the ionic currents carried by individual channels. The reason gated ionic channels give rise to a special type of electrical noise is that channels can open and close at random under steadystate conditions. Because the ion flux through a single channel is relatively large, random channel transitions generate observable electrical current fluctuations. These characteristic current fluctuations, often called channel noise, can be distinguished from other types of electrical noise which may be generated in an excitable-cell preparation.

Keywords

Voltage Clamp Channel Noise Current Noise Noise Analysis Current Fluctuation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Adams, P. R., 1977, Relaxation experiments using bath-applied suberyldicholine, J. Physiol. (Lond.) 268:271–289.Google Scholar
  2. Akaike, N., Fishman, H. M., Lee, K. S., Moore, L. E., and Brown, A. M., 1978, The units of calcium conduction in helix neurones, Nature 274:379–382.PubMedCrossRefGoogle Scholar
  3. Alvarez, D., Latorre, R., and Verdugo, R., 1975, Kinetic characteristics of the excitability-inducing material channel in oxidized cholesterol and brain lipid membranes, J. Gen. Physiol. 65:421–439.PubMedCrossRefGoogle Scholar
  4. Anderson, C. R., and Stevens, C. F., 1973, Voltage clamp analysis of acetylcholine produced current fluctuations at frog neuromuscular junction, J. Physiol. (Lond.) 235:655–691.Google Scholar
  5. Anderson, C. R., Cull-Candy, S. G., and Miledi, R., 1976, Glutamate and quisqualate noise in voltage-clamped locust muscle fibres, Nature 261:151–152.PubMedCrossRefGoogle Scholar
  6. Barker, J. L., and McBurney, R. N., 1979, GABA and glycine may share the same conductance channel on cultured mammalian neurones, Nature 277:234–236.PubMedCrossRefGoogle Scholar
  7. Baylor, D. A., Hodgkin, A. L., and Lamb, T. D., 1974, The electrical response of turtle cones to flashes and steps of light, J. Physiol. (Lond.) 242:685–727.Google Scholar
  8. Beginisich, T., and Stevens, C. F., 1975, How many conductance states do potassium channels have? Biophys. J. 15: 843–846.CrossRefGoogle Scholar
  9. Bendat, J. S., and Piersol, A. G., 1971, Random Data: Analysis and Measurement Procedures, Wiley-Interscience, New York.Google Scholar
  10. Bevan, S., Kullberg, R. W., and Rice, J., 1978, Acetylcholine-induced conductance fluctuations in cultured human myotubes, Nature 273:469–470.PubMedCrossRefGoogle Scholar
  11. Cochran, W. T., Cooley, J. W., Favin, D. L., Helms, H. D., Kaenel, R. A., Lang, W. W., Maling, G. C., Jr., Nelson, D. E., Rader, C. M., and Welch, P. D., 1967, What is the fast Fourier transform?, Proc. IEEE 55:1664–1674.CrossRefGoogle Scholar
  12. Colquhoun, D., and Hawkes, A. G., 1977, Relaxation and fluctuation of membrane currents that flow through drug-operated channels, Proc. R. Soc. London B199:231–262.CrossRefGoogle Scholar
  13. Colquhoun, D., Dionne, V. E., Steinbach, J. H., and Stevens, C. F., 1975, Conductance of channels opened by acetylcholine-like drugs in muscle end-plate, Nature 253:204–206.PubMedCrossRefGoogle Scholar
  14. Conti, F., and Wanke, E., 1975, Channel noise in nerve membrane and lipid bilayers, Q. Rev. Biophys. 8:451–506.PubMedCrossRefGoogle Scholar
  15. Conti, F., DeFelice, L. J., and Wanke, E., 1975, Potassium and sodium ion current noise in the membrane of the squid giant axon, J. Physiol. (Lond.) 248:45–82.Google Scholar
  16. Conti, F., Hille, B., Neumcke, B., Nonner, W., and Stämpfli, R., 1976a, Measurement of the conductance of the sodium channel from current fluctuations at the node of Ranvier, J. Physiol. (Lond.) 262:699–727.Google Scholar
  17. Conti, F., Hille, B., Neumcke, B., Nonner, W., and Stämpfli, R., 1976b, Conductance of the sodium channel in myelinated nerve fibres with modified sodium inactivation, J. Physiol. (Lond.) 262:729–742.Google Scholar
  18. Crawford, A. C., and McBurney, R. N., 1976, On the elementary conductance event produced by l-glutamate and quanta of the natural transmitter at the neuromuscular junctions of Maia squindo, J. Physiol. (Lond.) 259:205–225.Google Scholar
  19. Cull-Candy, S. G., Miledi, R., and Trautmann, A., 1978, Acetylcholine-induced channels and transmitter release at human endplates, Nature 271:74–75.PubMedCrossRefGoogle Scholar
  20. DeFelice, L. J., 1977, Fluctuation analysis in neurobiology, Int. Rev. Neurobiol. 20:169–208.PubMedCrossRefGoogle Scholar
  21. DeFelice, L. J., and Firth, D. P., 1971, Spontaneous voltage fluctuations in glass microelectrodes, IEEE Trans. Biomed. Eng. 18:339–351.PubMedCrossRefGoogle Scholar
  22. Derksen, H. E., 1965, Axon membrane voltage fluctuations, Acta Physiol. Pharmacol. Neerl. 13:373–466.PubMedGoogle Scholar
  23. Derksen, H. E., and Verveen, A. A., 1966, Fluctuations of resting neural membrane potential, Science 151:1388–1389.PubMedCrossRefGoogle Scholar
  24. Dionne, V. E., and Ruff, R. L., 1977, Endplate current fluctuations reveal only one channel type at frog neuromuscular junction, Nature 266:263–265.PubMedCrossRefGoogle Scholar
  25. Dionne, V. E., and Stevens, C. F., 1975, Voltage dependence of agonist effectiveness of the frog neuromuscular junction: Resolution of a paradox, J. Physiol. (Lond.) 251:245–270.Google Scholar
  26. Dodge, F. A., Jr., Knight, B. W., and Toyoda, J., 1968, Voltage noise in Limulus visual cells, Science 160:88–90.PubMedCrossRefGoogle Scholar
  27. Dreyer, F., Müller, K. D., Peper, K., and Sterz, R., 1976a, The M. Omohyoideus of the mouse as a convenient mammalian muscle preparation, Pflügers Arch. 367:115–122.PubMedCrossRefGoogle Scholar
  28. Dreyer, F., Walther, G., and Peper, K., 1976b, Junctional and extra junctional acetylcholine receptors in normal and denervated frog muscle fibers, Pflügers Arch. 366:1–9.PubMedCrossRefGoogle Scholar
  29. Dudel, J., Finger, W., and Stettmeier, H., 1977, GABA-induced membrane current noise and the time course of the inhibitory synaptic current in crayfish muscle, Neurosci. Lett. 6:203–208.PubMedCrossRefGoogle Scholar
  30. Ehrenstein, G., and Lecar, H., 1977, Electrically gated ionic channels in lipid bilayers, Q. Rev. Biophys. 10:1–34.PubMedCrossRefGoogle Scholar
  31. Ehrenstein, G., Lecar, H., and Nossal, R., 1970, The nature of the negative resistance in biomolecular lipid membranes containing excitability inducing material, J. Gen. Physiol. 55:119–133.PubMedCrossRefGoogle Scholar
  32. Eisenberg, M., Hall, J. E., and Mead, C. A., 1973, The nature of the voltage-dependent conductance induced by alamethicin in black lipid membranes, J. Membr. Biol. 14:143–176.PubMedCrossRefGoogle Scholar
  33. Fischbach, G. D., and Lass, Y., 1978a, Acetylcholine noise in cultured chick myoballs, J. Physiol. (Lond.) 280:515–526.Google Scholar
  34. Fischbach, G. D., and Lass, Y., 1978b, A transition temperature for acetylcholine channel conductance in chick myoballs, J. Physiol. (Lond.) 280:527–536.Google Scholar
  35. Fishman, H. M., 1973, Relaxation spectra of potassium channel noise from squid axon membranes, Proc. Natl. Acad. Sci. USA 70:876–879.PubMedCrossRefGoogle Scholar
  36. Fishman, H.M., and Moore, L. E., 1977, Ion movements and kinetics in squid axon. II. Spontaneous electrical fluctuations, Ann. NY. Acad. Sci. 303:399–423.PubMedGoogle Scholar
  37. Gage, P. W., McBurney, R. N., and Schneider, G. T., 1975, Effects of some aliphatic alcohols on the conductance change caused by a quantum of acetylcholine at the toad end-plate, J. Physiol. (Lond.) 244:409–429.Google Scholar
  38. Gardner, M., 1978, White and brown music, fractal curves and one-over-f fluctuations, Sci. Am. 239 (April): 16–31.CrossRefGoogle Scholar
  39. Hagins, W. A., 1965, Electrical signs of information flow in photoreceptors, Cold Spring Harbor Symp. Quant. Biol. 30:403–418.PubMedCrossRefGoogle Scholar
  40. Hill, T. L., and Chen, Y. D., 1972, On the theory of ion transport across the nerve membrane. IV. Noise from the open-close kinetics of K+ channels, Biophys. J. 12:948–959.PubMedCrossRefGoogle Scholar
  41. Jackson, M. B., and Lecar, H., 1979, Single postsynaptic channel currents in tissue cultured muscle, Nature 282:863–864.PubMedCrossRefGoogle Scholar
  42. Kam, Z., Shore, H. B., and Feher, G., 1975, Simple schemes for measuring autocorrelation functions, Rev. Sci. Instrum. 46:269–277.CrossRefGoogle Scholar
  43. Katz, B., and Miledi, R., 1972, The statistical nature of the acetylcholine potential and its molecular components, J. Physiol. (Lond.) 224:665–699.Google Scholar
  44. Katz, B., and Miledi, R., 1973, The characteristics of “endplate noise” produced by different depolarizing drugs, J. Physiol. (Lond.) 230:707–717.Google Scholar
  45. Katz, B., and Miledi, R., 1975, The effect of procaine on the action of acetylcholine at the neuromuscular junction, J. Physiol. (Lond.) 249:269–284.Google Scholar
  46. Keynes, R. D., 1975, Organization of the ionic channels in nerve membranes, in: The Nervous System (D. R. Tower, ed.), Vol. I: The Basic Neurosciences, pp. 165–175, Raven Press, New York.Google Scholar
  47. Kittel, C., 1961, Elementary Statistical Physics, John Wiley & Sons, New York.Google Scholar
  48. Krawczyk, S., 1978, Ionic channel formation in a living cell membrane, Nature 273:56–57.PubMedCrossRefGoogle Scholar
  49. Kuffler, S. W., and Nicholls, J. G., 1976, From Neuron to Brain, Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  50. Lamb, T. D., and Simon, E. J., 1977, Analysis of electrical noise in turtle cones, J. Physiol. (Lond.) 272:435–468.Google Scholar
  51. Lass, Y., and Fischbach, G. D., 1976, A discontinuous relationship between the acetylcholine-activated channel conductance and temperature, Nature 263:150–151.PubMedCrossRefGoogle Scholar
  52. Latorre, R., Alvarez, O., Ehrenstein, G., Espinoza, M., and Reyes, J., 1975, The nature of the voltage-dependent conductance of the hemocyanin channel, J. Membr. Biol. 25:163–182.PubMedCrossRefGoogle Scholar
  53. Lecar, H., and Nossal, R., 1971, Theory of threshold fluctuations in nerves, Biophys. J. 11:1048–1067, 1068-1083.PubMedCrossRefGoogle Scholar
  54. Lecar, H., Ehrenstein, G., and Latorre, R., 1975, Mechanism for channel gating in excitable bilayers, Ann. N.Y. Acad. Sci. 264:304–313.PubMedCrossRefGoogle Scholar
  55. Lee, Y. W., 1960, Statistical Communication Theory, John Wiley & Sons, New York.Google Scholar
  56. Lindemann, B., and Van Driessche, W., 1977, Sodium specific membrane channels of frog skin are pores: Current fluctuations reveal high turnover, Science 195:292–294.PubMedCrossRefGoogle Scholar
  57. Loewenstein, W. R., Kanno, Y., and Socolar, S. J., 1978, Quantum jumps of conductance during formation of membrane channels at cell-cell junction, Nature 274:133–136.PubMedCrossRefGoogle Scholar
  58. Machlup, S., 1954, Spectrum of a two-parameter random signal, J. Appl. Phys. 25:341–343.CrossRefGoogle Scholar
  59. Magleby, K. L., and Stevens, C. F., 1972, A quantitative description of end-plate currents, J. Physiol. (Lond.) 223:173–197.Google Scholar
  60. McBurney, R. N., and Barker, J. L., 1978, Gaba-induced conductance fluctuations in cultured spinal neurones, Nature 274:596–597.PubMedCrossRefGoogle Scholar
  61. Mueller, P., Rudin, D. O., Tien, H. T., and Wescott, W. C., 1962, Reconstitution of excitable cell membrane structure in vitro, Circulation 26:1167–1177.Google Scholar
  62. Neher, E., and Sakmann, B., 1976a, Noise analysis of drug induced voltage clamp currents in denervated frog muscle fibres, J. Physiol. (Lond.) 258:705–729.Google Scholar
  63. Neher, E., and Sakmann, B., 1976b, Single-channel currents recorded from membrane of denervated frog muscle fibers, Nature 260:799–802.PubMedCrossRefGoogle Scholar
  64. Neher, E., and Steinbach, H. H., 1978, Local anaesthetics transiently block currents through single acetylcholine-receptor channels, J. Physiol. (Lond.) 277:153–176.Google Scholar
  65. Neher, E., and Stevens, C. F., 1977, Conductance fluctuations and ionic pores in membranes, Annu. Rev. Biophys. Bioengr. 6:345–381.CrossRefGoogle Scholar
  66. Neher, E., Sakmann, B., and Steinbach, J. H., 1978, The extracellular patch clamp: A method for resolving currents through individual open channels in biological membranes, Pflügers Arch. 375:219–228.PubMedCrossRefGoogle Scholar
  67. Nelson, D. J., and Sachs, F., 1979, Single ionic channels observed in tissue cultured muscle, Nature 282:861–863.PubMedCrossRefGoogle Scholar
  68. Patlak, J., Gration, K. A. F., and Usherwood, P. N. R., 1979, Single glutamate-activated channels in locust muscle, Nature 278:643–645.PubMedCrossRefGoogle Scholar
  69. Poussart, D. J. M., 1969, Nerve membrane current noise: Direct measurements under voltage clamp, Proc. Natl. Acad. Sci. USA 64:95–99.PubMedCrossRefGoogle Scholar
  70. Rice, S. O., 1954, Mathematical analysis of noise, in: Selected Papers on Noise and Stochastic Processes (N. Wax, ed.), pp. 133–294, Dover Publications, New York.Google Scholar
  71. Ruff, R. L., 1976, Local anesthetic alteration of miniature endplate currents and endplate current fluctuations, Biophys. J. 16:433–439.PubMedCrossRefGoogle Scholar
  72. Sachs, F., and Lecar, H., 1973, Acetylcholine noise in tissue culture muscle cells, Nature [New Biol.] 246:214–216.Google Scholar
  73. Sachs, F., and Lecar, H., 1977, Acetylcholine-induced current fluctuations in tissue-cultured muscle cells under voltage clamp, Biophys. J. 17:129–143.PubMedCrossRefGoogle Scholar
  74. Sakmann, B., 1975, Noise analysis of acetylcholine-induced currents in normal and denervated rat muscle fibre, Pflügers Arch. 359:R89.Google Scholar
  75. Sakmann, B., and Boheim, G., 1979, Alamethicin-induced single channel conductance fluctuations in biological membranes, Nature 282:336–339.PubMedCrossRefGoogle Scholar
  76. Schuetze, S. M., Frank, E. F., and Fischbach, G. D., 1978, Channel open time and metabolic stability of synaptic and extrasynaptic acetylcholine receptors on cultured myotubes, Proc. Natl. Acad. Sci. USA 75:520–523.PubMedCrossRefGoogle Scholar
  77. Schwartz, E. A., 1977, Voltage noise observed in rods of the turtle retina, J. Physiol. (Lond.) 272:217–246.Google Scholar
  78. Siebenga, E., Meyer, A., and Verveen, A. A., 1973, Membrane shot noise in electrically depolarized nodes of Ranvier, Pflügers Arch. 341:87–96.PubMedCrossRefGoogle Scholar
  79. Sigworth, F. J., 1977, Sodium channels in nerve apparently have two conductance states, Nature 270:215–267.CrossRefGoogle Scholar
  80. Stephens, C. L., Jackson, M. B., and Lecar, H., 1980, Single C channel currents in living cells, J. Immunol. 124:1541.Google Scholar
  81. Stevens, C. F., 1976, A comment on Martin’s relation, Biophys. J. 16:891–895.PubMedCrossRefGoogle Scholar
  82. Ten Hoopen, M., and Verveen, A. A., 1962, Nerve-model experiments on fluctuation in excitability, Proc. Int. Conf. Cybernetics in Medicine (N. Wiener and J. P. Schade, eds.), pp. 8–21, Elsevier, Amsterdam.Google Scholar
  83. Van Helden, D., Hamill, O. P., and Gage, P. W., 1977, Permeant cations alter endplate channel characteristics, Nature 269:711–713.PubMedCrossRefGoogle Scholar
  84. Verveen, A. A., and DeFelice, L. J., 1974, Membrane noise, Prog. Biophys. Mol. Biol. 28:189–265.PubMedCrossRefGoogle Scholar
  85. Verveen, A. A., and Derksen, H. E., 1968, Fluctuation phenomena in nerve membrane, Proc. IEEE 56:906–916.CrossRefGoogle Scholar
  86. Verveen, A. A., and Derksen, H. E., 1969, Amplitude distribution of axon membrane noise voltage, Acta Physiol. Pharmacol. Neerl. 15:353–379.PubMedGoogle Scholar
  87. Verveen, A. A., Derksen, H. E., and Schick, K. L., 1967, Voltage fluctuations of neural membrane, Nature 216:588–589.PubMedCrossRefGoogle Scholar
  88. Wong, F., 1978, Nature of the light-induced conductance changes in neutral photoreceptors of Limulus, Nature 276:76–78.PubMedCrossRefGoogle Scholar

Copyright information

© Plenum Press, New York 1981

Authors and Affiliations

  • Harold Lecar
    • 1
  • Frederick Sachs
    • 2
  1. 1.Laboratory of Biophysics, Intramural Research Program, National Institute of Neurological and Communicative Disorders and StrokeNational Institutes of HealthBethesdaUSA
  2. 2.Department of Pharmacology and TherapeuticsState University of New YorkBuffaloUSA

Personalised recommendations