The origin of the initial heat associated with a single impulse in mammalian non‐myelinated nerve fibres

Abstract

SUMMARY1. A study has been made of the temperature changes associated with the passage of a single impulse in rabbit desheathed vagus nerves.2. The initial changes consist of an evolution of positive heat followed by a reabsorption of most of it; i.e. there is a phase of positive and a phase of negative heat production.3. The size of the positive heat, its time of onset, and the time of onset of the negative heat have been measured by an analogue method of analysis. In addition, these parameters, together with the size of the negative heat and the duration of both phases of initial heat, have been studied with the aid of a computer, and also by conventional heat block analysis.4. At about 50 C the measured positive heat is 7-2 ,tcal/g. impulse. It starts as soon as the compound action potential reaches the thermopile and lasts for about 107 msec.5. This positive heat decreases with increasing temperature, the ratio of heat at 40 C to that at 140 C being 1*86.6. The measured negative heat at about 50 C is 4-9 /ucal/g. impulse. It starts 102 msec after the onset of positive heat, and lasts for about 240 msec.7. When the sodium of Locke solution is replaced by lithium the positive heat is reduced by 19 %, but the negative heat is increased by 22 %.8. In potassium-free solutions the positive heat is hardly affected (increase of 5 %), but the negative heat is more than doubled. As a result the nerve may become briefly colder than its initial temperature by about 2 #0 C.9. The effect of sodium-deficient solutions on the positive heat is somewhat variable, but the negative heat is consistently diminished. 11. Replacement of most of the sodium of Locke solution by barium reduces or abolishes the negative heat, and increases the measured size of the positive heat nearly threefold.12. Veratrine (10-5 g/ml.) produces a nearly tenfold increase in the net positive heat.13. Ouabain (1 mM) and antimycin A (1 ,ug/ml.) applied for 30-60 min have little effect on the initial heat production.14. Over the temperature range 5-15°C, and for the ionic solution changes described above, there is close agreement in timing between the positive heat and the rising phase of the action potential, and between the negative heat and the falling phase.15. Because of the inevitable temporal dispersion of the action potential over the face of the thermopile, the observed temperature changes are smaller than those which occur at a single point in the nerve close to a stimulating electrode. The corrected value of the positive heat at 50 C is 24*5 ,ucal/g. impulse, while that of the negative heat is 22-2 ,lcal/g. impulse.16. The heats of mixing of the ions in solution that interchange during the action potential are much too small to account for the observed initial heats, but an exchange of ions associated with fixed charges might make a significant contribution to the heats.17. The condenser theory, according to which the positive heat represents the dissipation of electrical energy stored in the membrane capacity, while the negative heat results f...

On soliton propagation in biomembranes and nerves

“…If the empirical pulse energy is greater than the electrostatic energy, the conventional mechanism for pulse propagation is insufficient and must be supplemented. This inequality, in fact, has been shown by Howarth et al (12). As mentioned, it had been proposed earlier that transitions are involved in the nerve pulse.…”

“…Various authors have noted that the action potential is accompanied by reversible mechanical dislocations, changes in volume and temperature (11-16, 27, 32), and changes in fluorescence, turbidity, and birefringence (17). In particular, data indicate that heat release is exactly in phase with the action potential (12,13), and that there is no net heat release after completion of the action potential. This finding suggests that the action potential is isentropic.…”

“…† The first of these assumptions is clearly true for lung surfactant and E. coli and B. subtilis membranes (Fig. 1) (12) discussed in detail the initial heat release and the subsequent reabsorption, which is in phase with the square of the voltage changes (13) as is the energy of a charging capacitor (see Fig. 4b).…”

“…nbi.dk͞Kaufmann). In fact, mechanical forces and dislocations as well as temperature responses of nerve membranes in-phase with the action potential have been found experimentally (11)(12)(13)(14)(15)(16). They are accompanied by changes in the fluorescence of membrane probes and changes in turbidity and birefringence (17).…”

Chemical Events in Conducting and Synaptic Membrances during Electrical Activity

“…For instance, drastic changes of ion concentrations on the inside or the outside of the axon have little effect on the electrical parameters, contrary to the prediction of the theory (14). The strong heat production and absorption that coincide with electrical activity (15) and the production during the rising and the absorption during the falling phase of the action current (16) cannot be explained by ion mixing or ion friction, as proposed by supporters of the theory (12,16); there is no alternative to the assumption, as was stressed by A. V. Hill (17), that this heat produced and absorbed must be attributed to chemical reactions effecting the permeability changes. Moreover, the concepts of the Cambridge group were developed on the basis of the PlanckNernst equations, which can only be applied to systems in equilibrium, whereas cell meinbranes-as is today widely accepted-necessitate the use of nonequilibrium thermodynamics (18).…”