The Journal of Membrane Biology

, Volume 2, Issue 1, pp 351–374 | Cite as

Membrane excitability and dissipative instabilities

  • Robert Blumenthal
  • Jean-Pierre Changeux
  • René Lefever


Electrical excitation is interpreted in terms of a cooperative structural transition of membrane protomers coupled with the translocation of a permeant molecule in a non-equilibrium environment. Equations for flow of permeant and for membrane conformation are derived for the simple case of a single non-charged permeant. On the basis of a few simple physical assumptions, the theory predicts several important properties of electrically excitable membranes: the steepness of the relation between membrane conductance and potential, the presence of a negative conductance, and the occurrence of instabilities following rapid perturbations of membrane environment, giving rise to some simple cases of action potentials. Several experimental tests of the membrane with its changes of electrical properties are proposed. From a thermodynamic point of view, an electrically excitable membrane, in its resting state, lies beyond a dissipative instability and consequently is in a non-equilibrium state but with stable organization, a “dissipative structure” of Prigogine. Membrane excitation following a small perturbation of the environment would correspond to a jump from such an organization to another stable organization but close to thermodynamic equilibrium. It is shown how the cooperative molecular properties of the membrane are amplified by energy dissipation at the macroscopic level.


Macroscopic Level Dissipative Structure Membrane Conductance Thermodynamic Point Membrane Excitability 
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.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Adam, G. 1968. Theorie der Nervenerregung als kooperativer Kationenaustausch in einem zweidimensionalen Gitter. I. Ionenstrom nach einem depolarisierenden Sprung im Membranpotential.Z. Naturforsch. 23b:181.Google Scholar
  2. Adelman, W. J., Senft, J. P. 1968. Dynamic asymmetries in the squid axon membrane.J. Gen. Physiol. 51:102S.Google Scholar
  3. Baker, P. F., Hodgkin, A. L., Shaw, T. I. 1961. Replacement of the protoplasm of a giant nerve fibre with artificial solutions.Nature 190:885.Google Scholar
  4. Blumenthal, R., Changeux, J. P., Lefever, R. 1970. Une théorie de l'excitation électrique des membranes biologiques.Compt. Rend. Acad. Sci., Paris 270D:389.Google Scholar
  5. Carnay, L., Barry, W. H. 1969. Turbidity, birefingence and fluorescence changes in skeletal muscle coincident with the action potential.Science 165:608.Google Scholar
  6. Changeux, J. P. 1961. The feedback control mechanism of biosyntheticl-threonine deaminase byl-isoleucine.Cold Spring Harbor Symp. Quant. Biol. 26:313.Google Scholar
  7. — 1966. Responses of acetylcholinesterase fromTorpedo marmorata to salts and curarizing drugs.Mol. Pharmacol. 2:369.Google Scholar
  8. — 1969. Remarks on the symmetry and cooperative properties of biological membranes.In: Nobel Symp. No. 11, Symmetry and Function of Biological Systems at the Macromolecular Level. A. Engström and B. Strandberg, editors. p. 235. John Wiley, New York.Google Scholar
  9. Changeux, J. P., Blumenthal, R., Kasai, M., Podleski, T. 1970. Conformational transitions in the course of membrane excitation.In: Ciba Foundation Symposium, Molecular Properties of Drug Receptors. (in press)Google Scholar
  10. —, Podleski, T. R. 1968. On the excitability and cooperativity of the electroplax membrane.Proc. Nat. Acad. Sci. 59:944.Google Scholar
  11. —, Rubin, M. M. 1968. Allosteric interactions in aspartate transcarbamylase. III. Interpretations of experimental data in terms of the model of Monod, Wyman and Changeux.Biochemistry 7:553.Google Scholar
  12. —, Thiéry, J. 1968. On the excitability and cooperativity of biological membranes.In: Regulatory Functions of Biological Membranes. J. Jarnefelt, editor. BBA Library, Vol. 11. Elsevier, Amsterdam.Google Scholar
  13. ——, Tung, Y., Kittel, C. 1967. On the cooperativity of biological membranes.Proc. Nat. Acad. Sci. 57:335.Google Scholar
  14. Cohen, L. B., Keynes, R. D., Hille, B. 1968. Light scattering and birefringence changes during activity.Nature 218:438.Google Scholar
  15. Cole, K. S. 1955. Ions, potentials and the nerve impulse.In: Electrochemistry in Biology and Medicine. T. Shedlovsky, editor. p. 121. John Wiley, New York.Google Scholar
  16. — Moore, J. W. 1960. Potassium ion current in the squid giant axon: Dynamic characteristic.Biophys. J. 1:1.Google Scholar
  17. Dodge, F. A., Frankenhaeuser, B. 1959. Sodium currents in the myelinated nerve fibre ofXenopus laevis investigated with the voltage clamp technique.J. Physiol. 148:188.Google Scholar
  18. Erlanger, J., Gasser, H. S. 1937. Electrical signs of nervous activity. University of Pennsylvania Press, Philadelphia.Google Scholar
  19. Gerhart, J. C., Pardee, A. B. 1962. The enzymology of control by feedback inhibition.J. Biol. Chem. 237:891.Google Scholar
  20. Gordon, R. 1968. Steady-state properties of Ising lattice membranes.J. Chem. Phys. 49:570.Google Scholar
  21. Grundfest, H. 1966. Heterogeneity of excitable membranes: Electrophysiological and pharmalogical evidence and some consequence.Ann. N.Y. Acad. Sci. 137:901.Google Scholar
  22. Hill, T. L. 1956. Statistical Mechanics. McGraw-Hill, New York.Google Scholar
  23. — 1967. Electric fields and the cooperativity of biological membranes.Proc. Nat. Acad. Sci. 58:111.Google Scholar
  24. Hill, T. L., Kedem, O. Studies in irreversible thermodynamics. III. Models for steady state and active transport across membranes.J. Theoret. Biol. 10:339.Google Scholar
  25. Hille, B. 1968. Pharmacological modification of the sodium channels of frog nerve.J. Gen. Physiol. 51:199.Google Scholar
  26. Hodgkin, A. L. 1964. The Conduction of the Nervous Impulse. Liverpool University Press, Liverpool.Google Scholar
  27. — Huxley, A. F. 1952. A quantitative description of membrane current and its application to conduction and excitation in nerve.J. Physiol. 117:500.Google Scholar
  28. Katchalsky, A., Spangler, R. 1968. Dynamics of membrane processes.Quart. Rev. Biophys. 1:127.Google Scholar
  29. Koshland, D. E. 1963. The role of flexibility in enzyme action.Cold Spring Harbor Symp. Quant. Biol. 28:473.Google Scholar
  30. Lapicque, L. 1909. Definition expérimentale de l'excitabilité.Compt. Rend. Soc. Biol. 67:280.Google Scholar
  31. Lefever, R. 1968. Dissipative structures in chemical systems.J. Chem. Phys. 49:4977.Google Scholar
  32. — Nicolis, G., Prigogine, I. 1967. On the occurrence of oscillations around the steady state in systems of chemical reactions far from equilibrium.J. Chem. Phys. 47:1045.Google Scholar
  33. Mauro, A. 1962. Space charge regions in fixed charge membranes and the associated property of capacitance.Biophys. J. 2:179.Google Scholar
  34. Monod, J., Changeux, J. P., Jacob, J. 1963. Allosteric proteins and cellular control systems.J. Mol. Biol. 6:306.Google Scholar
  35. —, Jacob, F. 1961. General conclusions: Teleonomic mechanisms in cellular metabolism, growth and differentiation.Cold Spring Harbor Symp. Quant. Biol. 26:389.Google Scholar
  36. —, Wyman, J., Changeux, J. P. 1965. On the nature of allosteric transitions: A plausible model.J. Mol. Biol. 12:88.Google Scholar
  37. Mueller, P., Rudin, D. O. 1968. Resting and action potentials in experimental bimolecular lipid membranes.J. Theoret. Biol. 18:222.Google Scholar
  38. Mullins, L. J. 1956. The structure of nerve cell membranes.In: Molecular Structure and Functional Activity of Nerve Cells. p. 123. American Institute of Biological Sciences, Washington, D.C.Google Scholar
  39. Nachmansohn, D. 1959. Chemical and Molecular Basis of Nerve Activity. Academic Press, New York.Google Scholar
  40. Narahashi, T., Moore, J. W. 1968. Neuroactive agents and membrane conductance.J. Gen. Physiol. 51:93S.Google Scholar
  41. Podleski, T. R., Changeux, J. P. 1970. On the excitability and cooperativity of the electroplax membrane.In: Fundamental Concepts of Drug-Receptor Interactions, Proc. 3rd Ann. Buffalo-Milan Symp. on Mol. Pharmacol. August 28th, 1968. F. Danielli, J. F. Moran and D. J. Triggle, editors. 93. New York Academic Press.Google Scholar
  42. Prigogine, I. 1967. Introduction to Thermodynamics of Irreversible Processes. Interscience Publ., New York.Google Scholar
  43. — 1969a. Structure, Dissipation and Life.In: Theoretical Physics and Biology. M. Marois editor. North Holland Publishing Co., Amsterdam.Google Scholar
  44. Prigogine, I. 1969b. Dissipative structures in biological systems. Report at the 2nd Intern. Conf. on Theoret. Phys. & Biol. Institut de la Vie, Versailles, July, 1969. To be published by North Holland, Amsterdam.Google Scholar
  45. —, Lefever, R. 1968. Symmetry breaking instabilities in dissipative systems II.J. Chem. Phys. 48:1695.Google Scholar
  46. —— Goldbeter, A., Herschkowitz-Kaufman, M. 1969. Symmetry breaking instabilities in biological systems.Nature 223:913.Google Scholar
  47. — Nicolis, G. 1967. On symmetry breaking instabilities in dissipative systems.J. Chem. Phys. 46:3542.Google Scholar
  48. Strässler, S., Kittel, C. 1965. Degeneracy and the order of the phase transformation in the molecular field approximation.Phys. Rev. 139:A758.Google Scholar
  49. Tasaki, I. 1968. Nerve Excitation: A Macromolecular Approach p. 201. C. Thomas, Springfield, Ill.Google Scholar
  50. — Carnay, L., Sandlin, R., Watanabe, A. 1969. Fluorescence changes during conduction in nerves stained with acridine orange.Science 163:683.Google Scholar
  51. — Watanabe, A., Sandlin, R., Carnay, L. 1968. Changes in fluorescence, turbidity and birefringence associated with nerve excitation.Proc. Nat. Acad. Sci. 61:883.Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1970

Authors and Affiliations

  • Robert Blumenthal
    • 1
    • 2
  • Jean-Pierre Changeux
    • 1
    • 2
  • René Lefever
    • 1
    • 2
  1. 1.Département de Biologie MoléculaireInstitut PasteurParisFrance
  2. 2.Faculté des SciencesUniversité Libre de BruxellesBrusselsBelgium

Personalised recommendations