Thinking about the nerve impulse: A critical analysis of the electricity-centered conception of nerve excitability

Abbott, 1958, The positive and negative heat production associated with a nerve impulse, Proc. R. Soc. Lond. B Biol. Sci., 148, 149, 10.1098/rspb.1958.0012 Adrian, 1914, The all-or-none principle in nerve, J. Physiol., 47, 460, 10.1113/jphysiol.1914.sp001637 Almog, 2016, Is realistic neuronal modeling realistic?, J. Neurophysiol., 116, 2180, 10.1152/jn.00360.2016 Andersen, 2009, Towards a thermodynamic theory of nerve pulse propagation, Prog. Neurobiol., 88, 104, 10.1016/j.pneurobio.2009.03.002 Appali, 2012, A comparison of the Hodgkin–Huxley model and the soliton theory for the action potential in nerves, Volume 16, 275 Bailer-Jones, 2003, When scientific models represent, Int Stud Philos Sci, 17, 59, 10.1080/02698590305238 Bailer-Jones, 2009 Baluška, 2016, On having no head: cognition throughout biological systems, Front. Psychol., 7, 902, 10.3389/fpsyg.2016.00902 Bean, 2007, The action potential in mammalian central neurons, Nat. Rev. Neurosci., 8, 451, 10.1038/nrn2148 Behrends, 2012, Evolution of the ion channel concept: the historical perspective, Chem. Rev., 112, 6218, 10.1021/cr300349g Bennett, 1999, The early history of the synapse: from Plato to Sherrington, Brain Res. Bull., 50, 95, 10.1016/S0361-9230(99)00094-5 Bernstein, 1912 Beyder, 2010, Mechanosensitivity of NaV1.5, a voltage-sensitive sodium channel, J. Physiol., 588, 4969, 10.1113/jphysiol.2010.199034 Biondi, 1972, An engineering study of the peristaltic drive of axonal flow, Proc. Natl. Acad. Sci. U.S.A., 69, 1732, 10.1073/pnas.69.7.1732 Bishop, 1956, Natural history of the nerve impulse, Physiol. Rev., 36, 376, 10.1152/physrev.1956.36.3.376 Brunel, 2007, Quantitative investigations of electrical nerve excitation treated as polarization, Biol. Cybern., 97, 341, 10.1007/s00422-007-0189-6 Catterall, 2012, The Hodgkin-Huxley heritage: from channels to circuits, J. Neurosci., 32, 14064, 10.1523/JNEUROSCI.3403-12.2012 Clower, 1998, The transition from animal spirits to animal electricity: a neuroscience paradigm shift, J. Hist. Neurosci., 7, 201, 10.1076/jhin.7.3.201.1852 Cobb, 2002, Exorcizing the animal spirits: Jan Swammerdam on nerve function, Nat. Rev. Neurosci., 3, 395, 10.1038/nrn806 Cole, 1968 Cole, 1975, Neuromembranes: paths of ions, 143 Cook, 2008, The neuron-level phenomena underlying cognition and consciousness: synaptic activity and the action potential, Neuroscience, 153, 556, 10.1016/j.neuroscience.2008.02.042 Cook, 2014, From membrane excitability to metazoan psychology, Trends Neurosci., 37, 698, 10.1016/j.tins.2014.07.011 Craver, 2006, When mechanistic models explain, Synthese, 153, 355, 10.1007/s11229-006-9097-x Cremer, 1900, Über Wellen und Pseudowellen, Z. Biol., 40, 393 Crivellato, 2007, Soul, mind, brain: Greek philosophy and the birth of neuroscience, Brain Res. Bull., 71, 327, 10.1016/j.brainresbull.2006.09.020 Damasio, 2013, The nature of feelings: evolutionary and neurobiological origins, Nat. Rev. Neurosci., 14, 143, 10.1038/nrn3403 Danielli, 1935, A contribution to the theory of permeability of thin films, J. Cell. Comp. Physiol., 5, 495, 10.1002/jcp.1030050409 Daugman, 2001, Brain metaphor and brain theory, 23 De Palma, 2007, The ways of metaphor in neuroscience, or being on the right or wrong track, Nuncius, 22, 97, 10.1163/221058707X00053 De Palma, 2011, Bernstein’s long path to membrane theory: radical change and conservation in nineteenth-century German electrophysiology, J. Hist. Neurosci., 20, 306, 10.1080/0964704X.2010.532024 De Schutter, 2008, Why are computational neuroscience and systems biology so separate?, PLoS Comput. Biol., 4, 10.1371/journal.pcbi.1000078 Debanne, 2004, Information processing in the axon, Nat. Rev. Neurosci., 5, 304, 10.1038/nrn1397 Debanne, 2013, What are the mechanisms for analogue and digital signalling in the brain?, Nat. Rev. Neurosci., 14, 63, 10.1038/nrn3361 Drew, 2011, Sodium channel mechanosensitivity: pay a-tension to voltage sensor movement, J. Physiol., 589, 1003, 10.1113/jphysiol.2011.205880 du Bois-Reymond, 1884, Volume 2 El Hady, 2015, Mechanical surface waves accompany action potential propagation, Nat. Commun., 6, 6697, 10.1038/ncomms7697 Engelbrecht, 2016 Famm, 2013, Drug discovery: a jump-start for electroceuticals, Nature, 496, 159, 10.1038/496159a Ferrao Santos, 2010, Network excitability dysfunction in Alzheimer’s disease: insights from in vitro and in vivo models, Rev. Neurosci., 21, 153, 10.1515/REVNEURO.2010.21.3.153 Fields, 2011, Signaling by neuronal swelling, Sci. Signal., 4, tr1, 10.1126/scisignal.4155tr1 Finger, 2011, The Shocking History of Electric Fishes Follmann, 2015, Dynamics of signal propagation and collision in axons, Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 92, 10.1103/PhysRevE.92.032707 Forscher, 1989, Calcium and polyphosphoinositide control of cytoskeletal dynamics, Trends Neurosci., 12, 468, 10.1016/0166-2236(89)90098-2 Galbraith, 1993, Mechanical and electrical responses of the squid giant axon to simple elongation, J. Biomech. Eng., 115, 13, 10.1115/1.2895464 Galvani, 1791, De viribus electricitatis in motu musculari commentarius, Bon. Sci. Art. Inst. Acad. Comm., 7, 363 Gilbert, 1975, Axoplasm architecture and physical properties as seen in the myxicola giant axon, J. Physiol., 253, 257, 10.1113/jphysiol.1975.sp011190 Gonzalez-Perez, 2014, Penetration of action potentials during collision in the median and lateral giant axons of invertebrates, Phys. Rev. X, 4 Gonzalez-Perez, 2016, Solitary electromechanical pulses in lobster neurons, Biophys. Chem., 216, 51, 10.1016/j.bpc.2016.06.005 Gorter, 1925, On bimolecular layers of lipoids on the chromocytes of the blood, J. Exp. Med., 41, 439, 10.1084/jem.41.4.439 Gu, 2014, Physiological and pathological functions of mechanosensitive ion channels, Mol. Neurobiol., 50, 339, 10.1007/s12035-014-8654-4 Guillery, 2007, Relating the neuron doctrine to the cell theory. Should contemporary knowledge change our view of the neuron doctrine?, Brain Res. Rev., 55, 411, 10.1016/j.brainresrev.2007.01.005 Harmon, 1966, Neural modeling, Physiol. Rev., 46, 513, 10.1152/physrev.1966.46.3.513 Heimburg, 2005, On soliton propagation in biomembranes and nerves, Proc. Natl. Acad. Sci. U.S.A., 102, 9790, 10.1073/pnas.0503823102 Heimburg, 2006 Hermann, 1899, Zur Theorie der Erregungsleitung und der elektrischen Erregung, Pflug. Arch. Gesamte Physiol. Menschen Tiere, 75, 574, 10.1007/BF01664248 Hill, 1912, The absence of temperature changes during the transmission of a nervous impulse, J. Physiol., 43, 433, 10.1113/jphysiol.1912.sp001485 Hill, 1950, The volume change resulting from stimulation of a giant nerve fibre, J. Physiol., 111, 304, 10.1113/jphysiol.1950.sp004481 Hill, 1977, Laser interferometer measurement of changes in crayfish axon diameter concurrent with action potential, Science, 196, 426, 10.1126/science.850785 Hille, 1967, The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion, J. Gen. Physiol., 50, 1287, 10.1085/jgp.50.5.1287 Hille, 1977, Ionic basis of resting and action potentials, 99 Hille, 2001 Hodgkin, 1964, The ionic basis of nervous conduction, Science, 145, 1148, 10.1126/science.145.3637.1148 Hodgkin, 1964 Hodgkin, 1939, Action potentials recorded from inside a nerve fibre, Nature, 144, 710, 10.1038/144710a0 Hodgkin, 1945, Resting and action potentials in single nerve fibres, J. Physiol., 104, 176, 10.1113/jphysiol.1945.sp004114 Hodgkin, 1952, Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo, J. Physiol., 116, 449, 10.1113/jphysiol.1952.sp004717 Hodgkin, 1952, A quantitative description of membrane current and its application to conduction and excitation in nerve, J. Physiol., 117, 500, 10.1113/jphysiol.1952.sp004764 Hodgkin, 1949, The effect of sodium ions on the electrical activity of the giant axon of the squid, J. Physiol., 108, 37, 10.1113/jphysiol.1949.sp004310 Hodgkin, 1946, The electrical constants of a crustacean nerve fibre, Proc. R. Soc. Lond. B Biol. Sci., 133, 444, 10.1098/rspb.1946.0024 Howarth, 1968, The origin of the initial heat associated with a single impulse in mammalian non-myelinated nerve fibres, J. Physiol., 194, 745, 10.1113/jphysiol.1968.sp008434 Iwasa, 1980, Mechanical changes in squid giant axons associated with production of action potentials, Biochem. Biophys. Res. Commun., 95, 1328, 10.1016/0006-291X(80)91619-8 Iwasa, 1980, Swelling of nerve fibers associated with action potentials, Science, 210, 338, 10.1126/science.7423196 Julian, 1962, The effects of mechanical stimulation on some electrical properties of axons, J. Gen. Physiol., 46, 297, 10.1085/jgp.46.2.297 Keener, 2009 Keijzer, 2013, What nervous systems do: early evolution, input–output, and the skin brain thesis, Adapt. Behav., 21, 67, 10.1177/1059712312465330 Kim, 2007, A mechanical spike accompanies the action potential in mammalian nerve terminals, Biophys. J., 92, 3122, 10.1529/biophysj.106.103754 Kirkland, 2002, High-tech brains: a history of technology-based analogies and models of nerve and brain function, Perspect. Biol. Med., 45, 212, 10.1353/pbm.2002.0033 Kovács, 2004, Mechanism of Blebbistatin Inhibition of Myosin II. J. Biol. Chem., 279, 35557 Kuhn, 1996 Lapicque, 1907, Recherches quantitatives sur l’excitation électrique des nerfs traitée comme une polarisation, J. Physiol. Pathol. Gen., 9, 620 Le Bihan, 2007, The’ wet mind’: water and functional neuroimaging, Phys. Med. Biol., 52, R57, 10.1088/0031-9155/52/7/R02 Lucas-Lopez, 2008, The small molecule tool (S)-(-)-blebbistatin: novel insights of relevance to myosin inhibitor design, Org. Biomol. Chem., 6, 2076, 10.1039/b801223g Matsumoto, 1984, A proposed membrane model for generation of sodium currents in squid giant axons, J. Theor. Biol., 107, 649, 10.1016/S0022-5193(84)80137-X Matsumoto, 1979, Restoration of the excitability of squid giant axon by tubulin-tyrosine ligase and microtubule proteins, J. Biochem., 86, 1155, 10.1093/oxfordjournals.jbchem.a132611 Matsumoto, 1984, Axonal microtubules necessary for generation of sodium current in squid giant axons: I. Pharmacological study on sodium current and restoration of sodium current by microtubule proteins and 260K protein, J. Membr. Biol., 77, 77, 10.1007/BF01925858 Matsumoto, 1984, Axonal microtubules necessary for generation of sodium current in squid giant axons: II. Effect of colchicine upon asymmetrical displacement current, J. Membr. Biol., 77, 93, 10.1007/BF01925859 Metuzals, 1978, Subaxolemmal filamentous network in the giant nerve fiber of the squid (loligo pealei L.) and its possible role in excitability, J. Cell Biol., 78, 597, 10.1083/jcb.78.2.597 Meunier, 2002, Playing the devil’s advocate: is the Hodgkin–Huxley model useful?, Trends Neurosci., 25, 558, 10.1016/S0166-2236(02)02278-6 Morris, 2011, Voltage-gated channel mechanosensitivity: fact or friction?, Front. Physiol., 2, 25, 10.3389/fphys.2011.00025 Morris, 2007, Nav channel mechanosensitivity: activation and inactivation accelerate reversibly with stretch, Biophys. J., 93, 822, 10.1529/biophysj.106.101246 Mueller, 2014, A quantitative overview of biophysical forces impinging on neural function, Phys. Biol., 11, 051001, 10.1088/1478-3975/11/5/051001 Narahashi, 1964, Tetrodotoxin blockage of sodium conductance increase in lobster giant axons, J. Gen. Physiol., 47, 965, 10.1085/jgp.47.5.965 Neher, 1976, Single-channel currents recorded from membrane of denervated frog muscle fibres, Nature, 260, 799, 10.1038/260799a0 Overton, 1902, Beiträge zur allgemeinen Muskel- und Nervenphysiologie. II. Mitt. Über die Unentbehrlichkeit von Natrium (oder Lithium) Ionen für den Kontraktionsakt des Muskels, Pflug. Arch. Gesamte Physiol. Menschen Tiere, 92, 346, 10.1007/BF01659816 Patton, 2015 Phillips, 2013 Piccolino, 1998, Animal electricity and the birth of electrophysiology: the legacy of Luigi Galvani, Brain Res. Bull., 46, 381, 10.1016/S0361-9230(98)00026-4 Purves, 2012 Raichle, 2010, Two views of brain function, Trends Cogn. Sci., 14, 180, 10.1016/j.tics.2010.01.008 Rall, 1962, Theory of physiological properties of dendrites, Ann. N. Y. Acad. Sci., 96, 1071, 10.1111/j.1749-6632.1962.tb54120.x Ranade, 2015, 87, 1162 Rojas, 1963, Micro-injection of trypsin into axons of squid, Nature, 199, 78, 10.1038/199078b0 Rvachev, 2010, On axoplasmic pressure waves and their possible role in nerve impulse propagation, Biophys. Rev. Lett., 5, 73, 10.1142/S1793048010001147 Shrivastava, 2014 Smith, 1993, The use and abuse of metaphors in the history of brain science, J. Hist. Neurosci., 2, 283, 10.1080/09647049309525577 Smith, 1996, Sherrington’s legacy: evolution of the synapse concept, 1890s‐1990s, J. Hist. Neurosci., 5, 43, 10.1080/09647049609525650 Smith, 2012 Szentágothai, 1975, From the last skirmishes around the neuron theory to the functional anatomy of neuron networks, 103 Takahashi, 2016, Mechanosensitive ion channels, AIMS Biophys., 3, 63, 10.3934/biophy.2016.1.63 Takenaka, 1969, Morphology and electrophysiological properties of squid giant axons perfused intracellularly with protease solution, J. Gen. Physiol., 53, 81, 10.1085/jgp.53.1.81 Tasaki, 1949, Collision of two nerve impulses in the nerve fibre, Biochim. Biophys. Acta, 3, 494, 10.1016/0006-3002(49)90121-3 Tasaki, 1999, Rapid structural changes in nerve fibers and cells associated with their excitation processes, Jpn. J. Physiol., 49, 125, 10.2170/jjphysiol.49.125 Tasaki, 1992, Heat production associated with a propagated impulse in bullfrog myelinated nerve fibers, Jpn. J. Physiol., 42, 805, 10.2170/jjphysiol.42.805 Tasaki, 1992, Rapid structural changes in nerve fibers evoked by electric current pulses, Biochem. Biophys. Res. Commun., 188, 559, 10.1016/0006-291X(92)91092-5 Tasaki, 1993, The origin of rapid changes in birefringence, light scattering and dye absorbance associated with excitation of nerve fibers, Jpn. J. Physiol., 43, S67 Tasaki, 1957, Demonstration of two stable potential states in the squid giant axon under tetraethylammonium chloride, J. Gen. Physiol., 40, 859, 10.1085/jgp.40.6.859 Tasaki, 1982, Rapid pressure changes and surface displacements in the squid giant axon associated with production of action potentials, Jpn. J. Physiol., 32, 69, 10.2170/jjphysiol.32.69 Tasaki, 1964, Effects of various potassium salts and proteases upon excitability of intracellularly perfused squid giant axons, Proc. Natl. Acad. Sci. U.S.A., 52, 804, 10.1073/pnas.52.3.804 Tasaki, 1965, Effects of internal and external ionic environment on excitability of squid giant axon. A macromolecular approach, J. Gen. Physiol., 48, 1095, 10.1085/jgp.48.6.1095 Tasaki, 1989, Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse, Biophys. J., 55, 1033, 10.1016/S0006-3495(89)82902-9 Tejada, 2013, The epilepsies: complex challenges needing complex solutions, Epilepsy Behav., 26, 212, 10.1016/j.yebeh.2012.09.029 Terakawa, 1985, Potential-dependent variations of the intracellular pressure in the intracellularly perfused squid giant axon, J. Physiol., 369, 229, 10.1113/jphysiol.1985.sp015898 Terakawa, 1982, Electrical responses to mechanical stimulation of the membrane of squid giant axons, Pflugers Arch., 395, 59, 10.1007/BF00584969 Tigerstedt, 1880 Tsukita, 1986, Subaxolemmal cytoskeleton in squid giant axon. II. Morphological identification of microtubule- and microfilament-associated domains of axolemma, J. Cell Biol., 102, 1710, 10.1083/jcb.102.5.1710 Tyler, 2012, The mechanobiology of brain function, Nat. Rev. Neurosci., 13, 867, 10.1038/nrn3383 Valenstein, 2002, The discovery of chemical neurotransmitters, Brain Cogn., 49, 73, 10.1006/brcg.2001.1487 Verkhratsky, 2006, From Galvani to patch clamp: the development of electrophysiology, Pflug. Arch., 453, 233, 10.1007/s00424-006-0169-z Wang, 2009, Membrane trauma and Na+ leak from Nav1.6 channels, Am. J. Physiol. Cell Physiol., 297, C823, 10.1152/ajpcell.00505.2008 Wells, 1981, Membrane potential changes during stretch in squid giant axons, Biophys. J., 33, 91a Wilke, 1912, Das Problem der Reizleitung im Nerven vom Standpunkte der Wellenlehre aus betrachtet, Pflug. Arch. Gesamte Physiol. Menschen Tiere, 144, 35, 10.1007/BF01681175 Xu, 2013, Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons, Science, 339, 452, 10.1126/science.1232251 Young, 1938, The functioning of the giant nerve fibres of the squid, J. Exp. Biol., 15, 170, 10.1242/jeb.15.2.170 Young, 1975, Sources of discovery in neuroscience, 15