scholarly journals The Influence of External Potassium on the Inactivation of Sodium Currents in the Giant Axon of the Squid, Loligo pealei

1969 ◽  
Vol 53 (6) ◽  
pp. 685-703 ◽  
Author(s):  
William J. Adelman ◽  
Yoram Palti

Isolated giant axons were voltage-clamped in seawater solutions having constant sodium concentrations of 230 mM and variable potassium concentrations of from zero to 210 mM. The inactivation of the initial transient membrane current normally carried by Na+ was studied by measuring the Hodgkin-Huxley h parameter as a function of time. It was found that h reaches a steady-state value within 30 msec in all solutions. The values of h∞, τh, αh,and ßh as functions of membrane potential were determined for various [Ko]. The steady-state values of the h parameter were found to be inversely related, while the time constant, τh, was directly related to external K+ concentration. While the absolute magnitude as well as the slopes of the h∞ vs. membrane potential curves were altered by varying external K+, only the magnitude and not the shape of the corresponding τh curves was altered. Values of the two rate constants, αh and ßh, were calculated from h∞ and τh values. αh is inversely related to [Ko] while ßh is directly related to [Ko] for hyperpolarizing membrane potentials and is independent of [Ko] for depolarizing membrane potentials. Hodgkin-Huxley equations relating αh and ßh to Em were rewritten so as to account for the observed effects of [Ko]. It is concluded that external potassium ions have an inactivating effect on the initial transient membrane conductance which cannot be explained solely on the basis of potassium membrane depolarization.

1978 ◽  
Vol 235 (1) ◽  
pp. C63-C68 ◽  
Author(s):  
R. F. Abercrombie ◽  
P. de Weer

The operation of the sodium pump of giant axons of the squid, Loligo pealei, has been studied simultaneously in two independent ways: 1) by measuring sodium efflux with 22Na, and 2) by calculating the transmembrane current generated by the pump from measurements of membrane resistance and digitalis-sensitive membrane potential. In normal, untreated axons, the effect of increasing the external potassium concentration on both sodium efflux and pump current is similar, which suggests that Na:K pump stoichiometry remains relatively constant in the range of 0-20 mM external K. The data are compatible with a 3:2 Na:K ratio. In axons whose intracellular ADP level has been elevated by injection of L-arginine, a large, electrically silent, cardiotonic steroid-sensitive sodium efflux takes place in the absence of external potassium; this suggests that pump-mediated Na:Na exchange is 1:1 or electroneutral. Finally, elevation of external potassium levels causes the appearance, in high-ADP axons, of electrogenic pumping, with little effect on sodium efflux; hence, in contrast to what is seen in normal (low-ADP) axons, the charge translocated, per sodium ion extruded, increases sharply with increasing extracellular potassium levels.


1941 ◽  
Vol 24 (4) ◽  
pp. 551-563 ◽  
Author(s):  
Kenneth S. Cole ◽  
Howard J. Curtis

The squid giant axon was placed in a shallow narrow trough and current was sent in at two electrodes in opposite sides of the trough and out at a third electrode several centimeters away. The potential difference across the membrane was measured between an inside fine capillary electrode with its tip in the axoplasm between the pair of polarizing electrodes, and an outside capillary electrode with its tip flush with the surface of one polarizing electrode. The initial transient was roughly exponential at the anode make and damped oscillatory at the sub-threshold cathode make with the action potential arising from the first maximum when threshold was reached. The constant change of membrane potential, after the initial transient, was measured as a function of the total polarizing current and from these data the membrane potential is obtained as a function of the membrane current density. The absolute value of the resting membrane resistance approached at low polarizing currents is about 23 ohm cm.2. This low value is considered to be a result of the puncture of the axon. The membrane was found to be an excellent rectifier with a ratio of about one hundred between the high resistance at the anode and the low resistance at the cathode for the current range investigated. On the assumption that the membrane conductance is a measure of its ion permeability, these experiments show an increase of ion permeability under a cathode and a decrease under an anode.


1987 ◽  
Vol 65 (2) ◽  
pp. 222-229 ◽  
Author(s):  
Rosanne Hoffmann ◽  
Mary A. Bisson

Electrophysiological experiments were performed on internodal cells of Chara buckellii cultured in saline and freshwater media to see whether the membrane potential (Evo) and membrane conductance (Gm) are dominated by passive K+ conductance (K state), passive H+ conductance (H state), or active proton pumping (P state). Unlike other euryhaline charophytes, C. buckellii cells cultured under saline conditions were not dominated by any one state, showing little dependence on external K+ concentration and pH (pH°). Chara buckellii cells cultured in freshwater share some membrane properties with other freshwater charophytes. Freshwater cells appeared to be in the P state between pH° 5 and 7 as expected but never attained the H state usually observed at high pH° (> 10). Freshwater cells also showed a temporary, threefold increase in Gm at pH° 5, which could not be explained by an increase in passive Cl− or K+ conductance. Evidence consistent with an electrogenic Cl−/2H+ symport in freshwater-grown C. buckellii at pH° 5 and 7 is also presented.


1967 ◽  
Vol 50 (7) ◽  
pp. 1929-1953 ◽  
Author(s):  
Alfred Strickholm ◽  
B. Gunnar Wallin

The changes in membrane potential of isolated, single crayfish giant axons following rapid shifts in external ion concentrations have been studied. At normal resting potential the immediate change in membrane potential after a variation in external potassium concentration is quite marked compared to the effect of an equivalent chloride change. If the membrane is depolarized by a maintained potassium elevation, the immediate potential change due to a chloride variation becomes comparable to that of an equivalent potassium change. There is no appreciable effect on membrane potential when external sodium is varied, at normal or at a depolarized membrane potential. Starting from the constant field equation, expressions for the permeability ratios PCl/PK, PNa/PK, and for intracellular potassium and chloride concentrations are derived. At normal resting membrane potential, PCl/PK is 0.13 but at a membrane potential of -53 mv (external potassium level increased about five times) it is 0.85. The intracellular concentrations of potassium and chloride are estimated to be 233 and 34 mM, respectively, and it is pointed out that this is not compatible with ions distributed in a Nernst equilibrium across the membrane. It is also stressed that the information given by a plot of membrane potential vs. the logarithm of external potassium concentrations is very limited and rests upon several important assumptions.


1976 ◽  
Vol 68 (4) ◽  
pp. 405-420 ◽  
Author(s):  
B G Kennedy ◽  
P De Weer

Strophanthidin-sensitive and insensitive unidirectional fluxes of Na were measured in fog sartorius muscles whose internal Na levels were elevated by overnight storage in the cold. ATP levels were lowered, and ADP levels raised, by metabolic poisoning with either 2,4-dinitrofluorobenzene or iodoacetamide. Strophanthidin-sensitive Na efflux and influx both increased after poisoning, while strophanthidin-insensitives fluxes did not. The increase in efflux did not require the presence of external K but was greatly attenuated when Li replaced Na as the major external cation. Membrane potential was not markedly altered by 2,4-dinitrofluorobenzene. These observations indicate that the sodium pump of frog skeletal muscle resembles that of squid giant axon and human erythrocyte in its ability to catalyze Na-Na exchange to an extent determined by intracellular ATP/ADP levels.


1969 ◽  
Vol 54 (5) ◽  
pp. 589-606 ◽  
Author(s):  
William J. Adelman ◽  
Yoram Palti

Giant axons were voltage-clamped in solutions of constant sodium concentration (230 mM) and variable potassium concentrations (from 0 to 210 mM). The values of the peak initial transient current, Ip, were measured as a function of conditioning prepulse duration over the range from less than 1 msec to over 3 min. Prepulse amplitudes were varied from Em = -20 mv to Em = -160 mv. The attenuation of the Ip values in high [Ko] was found to vary as a function of time when long duration conditioning potentials were applied. In both high and low [Ko], Ip values which had reached a quasi-steady—state level within a few milliseconds following a few milliseconds of hyperpolarization were found to increase following longer hyperpolarization. A second plateau was reached with a time constant of about 100–500 msec and a third with a time constant in the range of 30 to 200 sec. The intermediate quasi-steady—state level was absent in K-free ASW solutions. Sodium inactivation curves, normalized to Ipmax values obtained at either the first or second plateaus, were significantly different in different [Ko]. The inactivation curves, however, tended to superpose after about 1 min of hyperpolarizing conditioning. The time courses and magnitudes of the intermediate and very slow sodium conductance restorations induced by long hyperpolarizing pulses are in agreement with those predicted from the calculated rates and magnitudes of [K+] depletion in the space between the axolemma and the Schwann layer.


1957 ◽  
Vol 40 (6) ◽  
pp. 859-885 ◽  
Author(s):  
Ichiji Tasaki ◽  
Susumu Hagiwara

1. Intracellular injection of tetraethylammonium chloride (TEA) into a giant axon of the squid prolongs the duration of the action potential without changing the resting potential (Fig. 3). The prolongation is sometimes 100-fold or more. 2. The action potential of a giant axon treated with TEA has an initial peak followed by a plateau (Fig. 3). The membrane resistance during the plateau is practically normal (Fig. 4). Near the end of the action potential, there is an apparent increase in the membrane resistance (Fig. 5D and Fig. 6, right). 3. The phenomenon of abolition of action potentials was demonstrated in the squid giant axon treated with TEA (Fig. 7). Following an action potential abolished in its early phase, there is no refractoriness (Fig. 8). 4. By the method of voltage clamp, the voltage-current relation was investigated on normal squid axons as well as on axons treated with TEA (Figs. 9 and 10). 5. The presence of stable states of the membrane was demonstrated by clamping the membrane potential with two voltage steps (Fig. 11). Experimental evidence was presented showing that, in an "unstable" state, the membrane conductance is not uniquely determined by the membrane potential. 6. The effect of low sodium water was investigated in the axon treated with TEA (Fig. 12). 7. The similarity between the action potential of a squid axon under TEA and that of the vertebrate cardiac muscle was stressed. The experimental results were interpreted as supporting the view that there are two stable states in the membrane. Initiation and abolition of an action potential were explained as transitions between the two states.


1975 ◽  
Vol 229 (5) ◽  
pp. 1249-1253 ◽  
Author(s):  
DM Easton ◽  
CE Swenberg

Impulse propagation velocity as a function of temperature in the range 5--20degreesC was obtained by external recording from the giant axon of Loligo pealei. The stellar nerve was set into a chamber allowing continuous superfusion, temperature control, and double recording of the impulse. Velocity was calculated from the interval between the spike peaks. The Q10 of velocity was about 1.8. At all temperatures, the velocity increased with time so that only data obtained during the 1st h or 2 could be generally considered to be comparable. Impulse block occurred below --3.4degreesC, in contrast to the giant axon of L. vulgaris, which blocks at about 0degreeC, but at the higher range of temperatures, the velocity in the L. pealei axons was not as well sustained as in those of L. vulgaris. The expected impulse velocity was calculated from Huxley's stability function f(beta) by approximating that function to a fourth-order polynominal and by substituting into it suitable ratios of available Q10 values relating to membrane conductance, ionic current, capacitance, and axoplasmic resistance. The calculation provided an improved fit to published experimental data on L. vulgaris. The difference in slope of the log velocity versus temperature plots, between the presumably warm acclimatized L. vulgaris and the cold-acclimatized L. pealei, was present in both experimental and calculated curves.


1992 ◽  
Vol 165 (1) ◽  
pp. 43-60 ◽  
Author(s):  
ISABEL BERMUDEZ ◽  
DAVID J. BEADLE ◽  
JACK A. BENSON

1. Three different responses were evoked by pressure micro-application of serotonin onto freshly dissociated, current- and voltage-clamped neuronal somata from the thoracic ganglia of the locust Locusta migratoria. 2. In some neurones, an inward current, I(5HT)K, resulting from a decrease in potassium conductance, with slow kinetics and maximum activation at membrane potentials of −60 to - 70 mV, was evoked by serotonin and by the 5-HT3 agonist 2-methyl serotonin. This current was completely abolished by either 10 mmoll−1 caesium or 5 mmoll−1 rubidium and partially blocked by 50 mmoll−1 tetraethylammonium or 5 mmoll−1 4-aminopyridine. The response was antagonised by the 5-HT2-specific compounds, ketanserin and ritanserin. 3. In other somata, serotonin, 2-methyl serotonin and the 5-HT3 antagonist ICS205 930 evoked a second current, I(5HT)Na, which was due to an increase in sodium permeability and had slow kinetics similar to that of I(5HT)K. This current was inward over the membrane potential range −30 to - 80 mV and increased with hyperpolarisation. The response was blocked by sodium-free saline and the 5-HT3 receptor antagonist MDL 72222. 4. In other neurones, at membrane potentials more positive than - 50 mV, serotonin pulses could activate a third current, I(5HT)X, which increased with depolarisation of the membrane potential and had comparatively fast kinetics. Activation of the current was accompanied by a decrease in membrane conductance. This response was completely blocked by 4-aminopyridine and weakly inhibited by both caesium and tetraethylammonium and is, therefore, probably a potassium current. 5. The three currents described here differ in their pharmacology, their ionic mechanisms and their dependence on membrane potential from the serotoninactivated currents reported for vertebrates and they provide evidence for the mechanism of action of serotonin as a neurotransmitter in insects. Note: Present address: Pharmacology Institute, University of Zurich, Gloriastrasse 32, CH-8006 Zurich, Switzerland.


1972 ◽  
Vol 50 (5) ◽  
pp. 416-422 ◽  
Author(s):  
Jean Pierre Caillé ◽  
O. F. Schanne

We measured the membrane potential of the liver cell in vivo at 38 °C as we increased the external potassium. For the range of K concentration from 20.4 to 78 mM, the membrane potential of the liver cell decreased with a slope of 20.2 mV per decade change in external K concentration. The tissue content of K, Na, and Cl was analyzed under the same experimental conditions. The cytoplasmic resistivity (111 ± 17.5 Ω-cm) was used as a criterion for the state of the ions in the cytoplasm. This result, when it is compared with the value predicted from the ionic content, suggests that either the ionic mobility or the ionic activity in the cytoplasm of the liver cell is less than in a simple salt solution. An analytical expression, derived with the use of irreversible thermodynamics, permits us to calculate the transport numbers for the ions K, Na, and Cl in the membrane of the liver cell (tK 0.28, tNa 0.12, tCl 0.61).


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