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Journal ArticleDOI

Contributions of the sodium pump and ionic gradients to the membrane potential of a molluscan neurone

01 Nov 1970-The Journal of Physiology (J Physiol)-Vol. 210, Iss: 4, pp 897-917
TL;DR: The membrane potential of the gastro‐oesophageal giant neurone of the marine mollusc, Anisodoris nobilis, was examined during changes of temperature and of the ionic medium.
Abstract: 1. The membrane potential of the gastro-oesophageal giant neurone of the marine mollusc, Anisodoris nobilis, was examined during changes of temperature and of the ionic medium.2. The response of the membrane potential to rapid changes in the external K concentration was prompt, stable, and reversible up to 200 mM-K, and was independent of the external Cl concentration.3. Warming the cell produced a prompt hyperpolarization that was approximately 10 times greater than predicted by the Nernst or constant field equations. Electrogenic activity of the Na-K exchange pump was shown to be responsible for this effect.4. At temperatures below 5 degrees C, the relationship between the membrane potential and the external K concentration could be predicted by a constant field equation.5. At temperatures above 5 degrees C, the membrane potential could not be predicted by the constant field equation except after inhibition of the electrogenic Na pump with ouabain or the reduction of internal Na.6. Inhibition of the electrogenic Na pump by low external K concentrations was dependent upon the external Na concentration.7. It is concluded that the membrane potential is the sum of ionic and metabolic components, and that the behaviour of the ionic component can be predicted by a constant field type equation.
Citations
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TL;DR: The sections in this article are: Electrotonic Synaptic Transmission, Functional Considerations in Mode of Transmission, Evaluation and Prospects, and Some “Unusual” Properties of Chemically Mediated Transmission.
Abstract: The sections in this article are: 1 Electrically Mediated Synaptic Transmission 1.1 Electrotonic Synapses 1.2 Rectifying Electrotonic Synapses 1.3 Electrical Inhibition 1.4 Electrical Interactions Across Extracellular Space 2 Functions of Electrotonic Transmission 2.1 Short Latency in Through-conducting Systems 2.2 Reciprocity and Short Latency in Highly Synchronized Systems 2.3 Synchronization in Relay Nuclei and Effector Organs 2.4 Asynchronous Activity and Reciprocal Excitation 2.5 Pathways of Electrotonic Coupling in Synchronization 2.6 Synaptic Control of Degree of Coupling 2.7 Cellular Control of Electrotonic Junctions 2.8 Functions of Electrotonic Junctions in Nonelectrical Communication 3 Some “Unusual” Properties of Chemically Mediated Transmission 3.1 Tonic Release of Transmitter 3.2 PSP's Involving a Conductance Decrease and Cytoplasmic Messengers 3.3 Dual- and Multiple-action Synapses 4 Functional Considerations in Mode of Transmission 4.1 Input-Output Relations of Electrically Excitable Membrane 4.2 Identification of Mode of Transmission 4.3 Properties with Clear Advantages to Either Mode 4.4 Properties with at Most a Modest Advantage to Either Mode 4.5 Evaluation and Prospects

183 citations

Journal ArticleDOI
TL;DR: It is suggested that the results cannot be accounted for by the diffusion of the major ions or by an electrogenic pump in combination with a large passive H + flux.

177 citations

Journal ArticleDOI
TL;DR: Recessed‐tip Na+‐sensitive micro‐electrodes were used to measure [Na+]i continuously in snail neurones for experiments lasting up to several hours, resulting in averages of 3·6 m M.
Abstract: 1. Recessed-tip Na+-sensitive micro-electrodes were used to measure [Na+]i continuously in snail neurones for experiments lasting up to several hours. The average resting [Na+]i in twenty-two cells was 3·6 m M. 2. Inhibition of the Na pump by ouabain caused [Na+]i to increase at an average rate of 0·54 m-mole/min. This corresponds to a passive influx of Na quantitatively similar to that observed in squid axons. 3. Changing external K over the range 1-8 m M had little effect on [Na+]i, but K-free or 0·25 m M-K Ringer caused a rise in [Na+]i. 4. Increasing membrane potential by up to 90 mV caused an increased influx of Na, but did not inhibit the pump. 5. Reducing external Na caused a decrease in [Na+]i but did not affect the pump rate at a given [Na+]i. The pump rate at low [Na+]i was proportional to [Na+]i minus a threshold value of about 1 m M. 6. The Na pump appeared still to be electrogenic at subnormal rates of activity. 7. It is concluded that, given sufficient external K, the rate of the Na pump depends principally on [Na+]i. Changes in external Na or membrane potential appear to affect the pump only indirectly, by changing the Na influx and thus [Na+]i.

161 citations

Journal ArticleDOI
TL;DR: It is postulated that neuronal membrane hyperpolarization with warming is responsible for several of the effects seen, including increased excitatory transmission and decreased population spikes seen in fully submerged rat hippocampal tissue slices.

151 citations

Journal ArticleDOI
TL;DR: The hyperpolarization between bursts in the R 15 cell of Aplysia is accompanied by an increase in membrane slope conductance and this results in a change in the concentration of Na6(CO3)(SO4)2 in the cell.
Abstract: 1. The hyperpolarization between bursts in the R 15 cell of Aplysia is accompanied by an increase in membrane slope conductance. 2. The post-burst hyperpolarization can be observed with ouabain, lithium, or potassium-free solution if artificial inward current is applied. The hyperpolarization can be observed with dinitrophenol or cooling to 10° C, with no injected current. Thus, the hyperpolarization apparently is not due to the cyclic activity of an electrogenic pump. 3. A reversal potential for the post-burst hyperpolarization can be demonstrated by passage of inward current during the inter-burst period. The reversal of direction of the potential depends on recent occurrence of a burst. 4. The reversal potential varies with external potassium concentration, but not with chloride or sodium. 5. The post-burst hyperpolarization is not blocked by external tetraethylammonium at a concentration which greatly prolongs the action potentials. 6. During the onset of spike blockage by, and recovery from, calcium-free+tetrodotoxin saline, the bursts of action potentials appear to be driven by endogenous waves of membrane potential. 7. The hyperpolarizing phase of the waves in calcium-free+tetrodotoxin medium is accompanied by an increased slope conductance. 8. A reversal potential can be demonstrated for the hyperpolarization following a wave in calcium-free+tetrodotoxin medium by applying inward current during the interwave period. 9. The waves in calcium-free+tetrodotoxin medium are blocked by ouabain but can be reinstated by artificial hyperpolarization. 10. The post-burst hyperpolarization and the post-wave hyperpolarization appear to result from a periodic increase in membrane conductance, primarily to potassium ions.

119 citations

References
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Journal ArticleDOI
TL;DR: A theoretical picture has been presented based on the use of the general kinetic equations for ion motion under the influence of diffusion and electrical forces and on a consideration of possible membrane structures that shows qualitative agreement with the rectification properties and very good agreementwith the membrane potential data.
Abstract: Impedance and potential measurements have been made on a number of artificial membranes. Impedance changes were determined as functions of current and of the composition of the environmental solutions. It was shown that rectification is present in asymmetrical systems and that it increases with the membrane potential. The behavior in pairs of solutions of the same salt at different concentrations has formed the basis for the studies although a few experiments with different salts at the same concentrations gave results consistent with the conclusions drawn. A theoretical picture has been presented based on the use of the general kinetic equations for ion motion under the influence of diffusion and electrical forces and on a consideration of possible membrane structures. The equations have been solved for two very simple cases; one based on the assumption of microscopic electroneutrality, and the other on the assumption of a constant electric field. The latter was found to give better results than the former in interpreting the data on potentials and rectification, showing agreement, however, of the right order of magnitude only. Although the indications are that a careful treatment of boundary conditions may result in better agreement with experiment, no attempt has been made to carry this through since the data now available are not sufficiently complete or reproducible. Applications of the second theoretical case to the squid giant axon have been made showing qualitative agreement with the rectification properties and very good agreement with the membrane potential data.

2,685 citations

Journal ArticleDOI
TL;DR: The most widely accepted theory of the restirng potential of muscle is that the electrical potential difference between the inside and outside of a muscle fibre arises from the concentration gradients of the potassium and chloride ions.
Abstract: The most widely accepted theory of the restirng potential of muscle is that the electrical potential difference between the inside and outside of a muscle fibre arises from the concentration gradients of the potassium and chloride ions. If we follow Boyle & Conway (1941), the membrane is assumed to be permeable to K and Cl but to be impermeable or sparingly permeable to other ions. Since K is more concentrated inside and Cl is more concentrated outside, the interior of the fibre should be electrically negative to the external solution. If K and Cl are distributed passively, the concentration ratios and the membrane potential under equilibrium conditions ought to conform to the relation

1,392 citations

Journal ArticleDOI
TL;DR: This work has shown that the sodium efflux from the axons of Loligo forbesi increases when external sodium is replaced by lithium.
Abstract: 1. Previous work has shown that the sodium efflux from the axons of Loligo forbesi increases when external sodium is replaced by lithium. 2. The increase in efflux in lithium was unaffected by ouabain but was abolished by removal of external calcium; in these respects it differed from the potassium-dependent sodium efflux which was abolished by ouabain but not reduced by removal of external calcium. 3. Strontium but not magnesium could replace calcium in activating the ouabain-insensitive sodium efflux; lanthanum had an inhibitory effect. 4. Replacing all the external NaCl by choline chloride or dextrose gave a rise in Na efflux which was abolished by ouabain but not by removal of external calcium. 5. The rise in Na efflux resulting from partial replacement of NaCl by dextrose or choline chloride consisted of two components one of which was ouabain-insensitive and calcium-dependent and the other was inhibited by ouabain but calcium-insensitive. 6. The ouabain-insensitive component of the Na efflux was activated by low concentrations of Na, Li or K but inhibited by high concentrations of Na and to a lesser extent Li. The inhibiting effect of high Na was of the kind expected if these ions displace calcium from an external site. 7. The ouabain-insensitive component of the Na efflux was abolished by cyanide, had a Q10 of 2·7; and was roughly proportional to [Na]i2. It was much more variable in magnitude than the ouabain-sensitive, potassium-dependent component of the sodium efflux. 8. The calcium influx increased five to fortyfold when external NaCl was replaced by LiCl or dextrose, the increase for Li being larger than the increase for dextrose. 9. The calcium influx from Na, Li or dextrose sea water was increased three to tenfold by increasing the internal Na about fourfold. 10. The experiments provide evidence for a coupling between an inward movement of calcium and an outward movement of sodium.

887 citations