Effects of extracellular potassium accumulation and sodium pump activation on automatic canine Purkinje fibres

Abstract

SUMMARY1. Double barrel potassium-sensitive micro-electrodes were used to measure fluctuations in extracellular potassium ion concentration in large automatic canine Purkinje fibres.2. Slow accumulations of potassium were seen in the extracellular space during prolonged beating. Following cessation of prolonged beating, a depletion of extracellular potassium ions was noted.3. The time course of these slow changes in extracellular potassium concentration were shown to be a function of the diffusion properties of the preparation, and the rate and degree of activation of the sodium pump.4. Action potential duration and maximum diastolic potential were simultaneously monitored during and after these periods of rapid stimulation, using conventional intracellular micro-electrodes.5. Initial depolarization and later hyperpolarization of the maximum diastolic potential appeared to occur as a direct result of changes in extracellular potassium concentration and level of pump activation induced by the sudden and prolonged alteration in stimulus rate.6. Following prolonged stimulation, dramatic changes in the automatic beating rate were correlated with changes in extracellular potassium and pump rate, and their effects on the maximum diastolic potential and other parameters of the diastolic potential depolarization.7. For some locations of the potassium-sensitive electrode tip, large fluctuations in extracellular potassium were seen during single beats. Alterations in action potential duration during abrupt rate changes appear to derive in part from modulation by these extracellular potassium concentration fluctuations altering net membrane currents. Slower shifts in action potential duration appear correlated to the degree of sodium pump activation.

Changes in intra- and extracellular potassium and intracellular sodium activities induced by repetitive stimulation and their relation to membrane potential in guinea-pig papillary muscle.

“…In the present experiments, it has been shown that immediately after the onset of repetitive stimulation, extracellular K+ activity starts to increase, reaches the maximal level within 30 s, and then declines toward the prestimulation levels during the period of stimulation, and after cessation of stimulation aK temporarily decreases below the level of bathing solution, gradually returning to the prestimulation levels. The results were qualitatively similar to those reported for other cardiac tissues by previous authors MORAD, 1976, 1978;KUNZE, 1977;KLINE et al, 1980;BROWNING and STRAUSS, 1981 ;KLINE and KUPERSMITH, 1982). The magnitude of the initial increase in aK was dependent on the frequency of stimulation.…”

“…It is generally accepted that the hyperpolarization during and after prolonged trains of rapid stimulation has been attributed largely to electrogenic sodium pumping (VASSALLE, 1970;GADSBY and CRANEFIELD, 1979;KLINE et al, 1980;BOYETT and FEDIDA, 1981;KODAMA et al, 1981;COHEN et al, 1982;GADSBY and CRANEFIELD, 1982;GLITSCH, 1982;KLINE and KUPERSMITH, 1982;ELLIS, 1985), activated by a large rise of aNa (CoHEN et al, 1982;ELLIS, 1985). However, since the membrane potential of the cardiac tissue is influenced by the external potassium concentration as well as electrogenic Na-pumping activity, any changes in potassium distribution must be taken into consideration in evaluating changes in membrane potential.…”

“…However, since the membrane potential of the cardiac tissue is influenced by the external potassium concentration as well as electrogenic Na-pumping activity, any changes in potassium distribution must be taken into consideration in evaluating changes in membrane potential. In fact, it has been known that an accumulation of K+ in the extracellular space in the cardiac tissue at the beginning of a stimulus train, and then the increased extracellular K+ activity (ak) gradually declines toward the initial level during stimulation, and cessation of stimulation is followed by temporary aK depletion MORAD, 1976, 1978;Kunze, 1977;KLINE et al, 1980;BROWNING and STRAUSS, 1981;KLINE and KUPERSMITH, 1982). Thus, any in -INTRACELLULAR ION ACTIVITY AND RAPID STIMULATION 799 terpretation of the hyperpolarization is complicated by concomitant changes in the extracellular K + concentration and by possible effects both of the extracellular K + and intracellular Na+ on activation of the Na-K pump.…”

Electrophysiological alternans and restitution during acute regional ischaemia in myocardium of anaesthetized pig.

“…Electrical alternans has been attributed both to alternation in extracellular potassium levels at the start of each action potential (Kline & Kupersmith, 1980), and to incomplete membrane recovery between alternate beats (Hauswirth et al 1972;Boyett & Jewell, 1978). A second, more persistent type of alternans has been identified in the isolated preparation, probably linked to intracellular calcium cycling, and calcium entry into the cell during the action potential (Hirata et al 1980).…”

Interaction of intracellular ion buffering with transmembrane-coupled ion transport.

“…Subsequently the contribution of electrogenic transport to the transmembrane potential was pursued (Gadsby and Cranefield, 1979;Falk and Cohen, 1984); at the same time the influence of rapid voltage-activated current fluxes on the transmembrane ionic balance was considered (Atwell et al, 1979;Kootsey et ai., 1980;Levis et al, 1983). Thus, intracellular sodium and calcium loading (Eisner et al, 1981a;Sheu and Fozzard, 1982;Ellis, 1985;Boyett et al, 1987) and extracellular potassium accumulation and depletion (Cohen and Kline, 1982;Kline and Kupersmith, 1982) were seen as routine consequences of repeated activation of transient transmembrane currents. Subsequent attempts (Deitmer and Ellis, 1980;Ellis and MacLeod, 1985;Piwnica-Worms et al, 1985) to include the role of both single ion and coupled transport systems (electrogenic and nonelectrogenic) analyzed in some detail the interaction of these multiple active and passive transport systems, showing, for example, that ions could be effectively coupled by sharing common cotransport partners even when not actually transported by the same molecular entity (Jacob et al, 1984).…”