Abstract
In the last 15 years, a debate has emerged about the validity of the famous Hodgkin-Huxley model for nerve impulse. Mechanical models have been proposed. This note reviews the experimental properties of the nerve impulse and discusses the proposed alternatives. The experimental data, which rule out some of the alternative suggestions, show that while the Hodgkin-Huxley model may not be complete, it nevertheless includes essential features that should not be overlooked in the attempts made to improve, or supersede, it.
Similar content being viewed by others
References
Von Helmholtz, H.: Messungen über den zeitlichen Verlauf der Zuckung animalischer Muskeln und die Fortpflanzungsgeschwindigkeit der Reizung in den Nerven. Archiv für Anatomie, Physiologie und wissenschaftliche Medicin 276–364 (1850)
Von Helmholtz, H.: Note sur la vitesse de propagation de l’agent nerveux dans les nerfs rachidiens. C. R. Acad. Sci. (Paris) XXX, 204–-206 (1850)
Von Helmholtz, H.: Deuxième note sur la vitesse de propagation de l’agent nerveux. C. R. Acad. Sci. (Paris) XXXIII, 262–-265 (1851). available at: https://www.academie-sciences.fr/archivage_site/activite/hds/textes/tsf_Debru1.pdf
Hodgkin, A.L., Huxley, A.F.: A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. 117, 500–544 (1952)
Vandenberg, J.I., Waxman, S.G.: Hodgkin and Huxley and the basis for electrical signalling: a remarkable legacy still going strong. J. Physiol. 590.11, 2569–2570 (2012)
Schwiening, C.J.: A brief historical perspective: Hodgkin and Huxley. J. Physiol. 590.11, 2571-–2575 (2012)
Heimburg, T., Jackson, A.D.: On soliton propagation in biomembranes and nerves. Proc. Natl. Acad. Sci. U.S.A. 102, 9790–9795 (2005)
Holland, L., de Regt, H.W., Drukarch, B.: Thinking about the nerve impulse: The prospects for the development of a comprehensive account of nerve impulse propagation. Front. Cell. Neurosci. 13, art. 208 (2019)
Seyfarth, E.-A.: Julius Bernstein (1839–1917): pioneer neurobiologist and biophysicist. Biol. Cybern. 94, 2–8 (2006)
Bernstein, J.: Ueber den zeitlichen Verlauf der negativen Schwankung des Nervenstroms. Pflügers Archiv. 1, 173–207 (1868)
Bernstein, J.: Untersuchungen zur Thermodynamik der bioelectrischen Ströme. Pflügers Archiv. 92, 521–562 (1902)
Overton, E.: Beiträge zur allgemeinen Muskel- und Nervenphysiologie. II Ueber die Unentbehrlichkeit von Natrium- (oder Lithium-)Ionen fü,r den Contractionsact des Muskels. Pflügers 92, 346–386 (1902)
Hodgkin, A.L.: Chance and design in electrophysiology: an informal account of certain experiments on nerve carried out between 1934 and 1952. J. Phys. 263, 1–21 (1976)
Hodgkin, A.L.: Evidence for electrical transmission in nerve. Part I. J. Phys. 90, 183–210 (1937)
Hodgkin, A.L.: The subthreshold potentials in a crustacean nerve fibre. Proc. Roy. Soc. London B 126, 87–121 (1938)
Cole, K.S., Curtis, H.J.: Electric impedance of the squid giant axon during activity. J. Gen. Physiol. 22, 649–670 (1939)
Hodgkin, A.L.: The relation between conduction velocity and the electrical resistance outside a nerve fibre. J. Phys. 94, 560–570 (1939)
Curtis, H.J., Cole, K.S.: Membrane resting and action potential from the squid giant axon. J. Cell. Comp. Physiol. 19, 135–144 (1942)
Hodgkin, A.L., Huxley, A.F.: Resting and action potentials in single nerve fibres. J. Physiol. 104, 176–195 (1945)
Huxley, A.F.: Hodgkin and the action potential. J. Physiol. 538, 2 (2002)
Hodgkin, A.L., Katz, B.: The effect of sodium ions on the electrical activity of the giant axon of the squid. J. Physiol. 108, 37–77 (1949)
Hodgkin, A.L., Keynes, R.D.: Active transport of cations in giant axons from Sepia and Loligo. J. Physiol. 128, 28–60 (1955)
Hodgkin, A.L., Keynes, R.D.: The potassium permeability of a giant nerve fibre. J. Physiol. 128, 61–88 (1955)
Hodgkin, A.L., Katz, B.: The effect of temperature on the electrical activity of the giant axon of the squid. J. Physiol. 109, 240–249 (1949)
Feng, T.P.: The heat production of nerve. Ergeb. Physiol. Biol. Chem. Exp. Pharmakol. 38, 73–132 (1936)
Howarth, J.V., Keynes, R.D., Ritchie, J.M.: The origin of the initial heat associated with a single impulse in mammalian non-myelinated nerve fibres. J. Physiol. 194, 745–793 (1968)
Howarth, J.V., Keynes, R.D., Ritchie, J.M., vin Muralt, A.: The heat production associated with the passage of a single impulse in olfactory nerve fibres. J. Physiol. 249, 349–368 (1975)
de Lichtervelde, A.C.L., de Souza, J.P., Bazant, M.Z.: Heat of nervous conduction: a thermodynamic framework. Phys. Rev. E 101, 022406 (2020)
Tasaki, I., Watanabe, A., Sandlin, R., Carnay, L.: Changes in fluorescence, turbidity and birefringence associated with nerve excitation. Proc. Natl. Acad. Sci. U.S.A. 61, 883–888 (1968)
Hill, B.C., Schubert, E.D., Nokes, M.A., Michelson, R.P.: Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential. Science 196, 426–428 (1977)
Iwasa, K., Tasaki, I.: Mechanical changes in squid giant axons associated with production of action potential. Biochem. Biophys. Res. Commun 95, 1328–1331 (1980)
Iwasa, K., Tasaki, I., Gibbons, R.C.: Swelling of nerve fibers associated with action potentials. Science 210, 338–339 (1980)
Tasaki, I., Byrne, P.M.: Discontinuous volume transitions in ionic gels and their possible involvement in the nerve excitation process. Biopolymers 32, 1019–1023 (1992)
Tasaki, I.: Rapid structural changes in nerve fibers and cells associated with their excitation processes. Jap. J. Physiol. 49, 125–138 (1999)
Tasaki, I.: Evidence for phase transition in nerve fibers, cells and synapses. Ferroelectrics 220, 305–316 (1999)
Jensen, M.Ø., Jogini, V., Borhani, D.W., Leffler, A.E., Dror, R.O., Shaw, D.E.: Mechanism of voltage gating in potassium channels. Science 336 (6078), 229–233 (2012)
Catterall, W.A.: From ionic currents to molecular mechanisms: The structure and function of voltage-gated sodium channels. Neuron 26, 13–25 (2000)
Dauxois, T., Peyrard, M.: Physics of Solitons. Cambridge University Press, Cambridge (2006)
Gonzalez-Perez, A., Mosgaard, L.D., Budvytyte, R., Nissen, S., Heimburg, T.: Penetration of action potentials during collision in the median and lateral giant axons of invertebrates. Phys. Rev. X 4, 031047 (2014)
Tasaki, I.: Collision of two nerve impulses in the nerve fibre. Biochim. Biophys. Acta 3, 494–-497 (1949)
Aslanidi, O.V., Mornev, O.A.: Can colliding nerve pulses be reflected?. JETP Lett. 65, 579–-585 (1997). (Pis’ma Zh. Éksp. Teor. Fiz. 65, No. 7, 553–558 10 April 1997)
Xu K., Zhong, G., Zhuang, X.: Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 339, 452–456 (2013)
Kotthaus, J.P.: A Mechatronics view at nerve conduction. arXiv:1909.06313 [physics.bio-ph] (2019)
Purcell, E.M.: Life at low Reynolds number. Am. J. Phys. 45, 3–11 (1977)
Neher, E., Sakmann, B.: Single-channel currents recorded from membrane of denervated frog muscle fibres. Nature 260, 799–802 (1976)
El Hady, A., Machta, B.B.: Mechanical surface waves accompany action potential propagation. Nat. Commun. 6, 6697 (2015)
Engelbrecht, J., Peets, T., Tamm, K.: Electromechanical coupling of waves in nerve fibres. Biomech. Model Mechanobiol. 17, 1771–-1783 (2018). arXiv:1802.07014v2
FitzHugh, R.: Impulses and physiological states in theoretical models of the nerve membrane. Biophys. J. 1, 445–466 (1961)
Nagumo, J., Arimoto, S., Yoshizawa, S.: An active pulse transmission line simulating nerve axon. In: Proceedings of the IRE, pp 2061–2070 (1962)
Krichen, S., Sharma, P.: Flexoelectricity: a perspective on an unusual electromechanical coupling. J. Appl. Mech. 83, 030801–1-6 (2016)
Chen, H., Garcia-Gonzalez, D., Jérusalem, A.: Computational model of the mechanoelectrophysiological coupling in axons with application to neuromodulation. Phys. Rev. E. 99, 032406 (2019)
Franks, N.P., Lieb, W.R.: Molecular and cellular mechanisms of general anaesthesia. Nature 367, 607–614 (1994)
Yakamura, T., Bertaccini, E., Trudell, J.R., Harris, R.A.: Anesthetics and ion channels: Molecular models and sites of action. Annu. Rev. Pharmacol. Toxicol. 43, 23–51 (2001)
El-Din, T.M.G., Lanaeus, M.J., Zheng, N. , Catterall, W.A.: Fenestrations control resting-state block of a voltage- gated sodium channel. Proc. Natl. Acad. Sci. U.S.A. 51, 13111–13116 (2018)
Pavel, M.A., Petersen, E.N., Wang, H., Lerner, R.A., Hansen, S.B.: Studies on the mechanism of general anesthesia. Proc. Natl. Acad. Sci. U.S.A. 117, 13757–13766 (2020)
Heimburg, T.: The important consequences of the reversible heat production in nerves and the adiabaticity of the action potential. arXiv:2002.06031v2 [physics.bio-ph] (2020)
Beyder, A., Rae, J.L., Bernard, C., Strege, P.R., Sachs, F., Farrugia, G.: Mechanosensitivity of Na v 1.5, a voltage-sensitive sodium channel. J. Physiol. 588, 4969–4985 (2010)
FitzHugh, R.: Computation of impulse initiation and saltatory conduction in a myelinated nerve fiber. Biophys. J. 2, 11–21 (1962)
Ori, H., Marder, E., Marom, S.: Cellular function given parametric variation in the Hodgkin and Huxley model of excitability. Proc. Natl. Acad. Sci. U.S.A. 115, E8211–E8218 (2018)
Strassberg, A.E., DeFelice, L.J.: Limitations of the Hodgkin-Huxley formalism: Effects of single channel kinetics on transmembrane voltage dynamics. Neural Comput. 5, 843–855 (1993)
Meunier, C., Segev, I.: Playing the Devil’s advocate: is the Hodgkin–Huxley model useful? Trends Neurosci. 25, 558–563 (2002)
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no conflict of interest.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Peyrard, M. How is information transmitted in a nerve?. J Biol Phys 46, 327–341 (2020). https://doi.org/10.1007/s10867-020-09557-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10867-020-09557-2