Potassium efflux in heart muscle during activity: extracellular accumulation and its implications.

Abstract

SUMMARY1. Extracellular K+ activity and transmembrane potential were simultaneously monitored with a K+-selective micro-electrode placed in the extracellular space and a standard KCl-filled micro-electrode in the intracellular space of the frog ventricular muscle.2. K+ was found to accumulate during activity and had the approximate magnitude and time course to account for the measured membrane depolarization.3. The magnitude of the K+ accumulation depended on the frequency of stimulation, diameter of the muscle and temperature of the bathing solution.4. The time constants of accumulation and decay were dependent only on the diameter and the temperature of the strip. A Q10 of 2 was measured for the decay of accumulated K+. 5. Double barrelled K+-electrodes were used to monitor the change in K+ activity accompanying a single action potential, since the reference barrel allowed for rapid compensation of the electrical potential fluctuations encountered in the subendothelial space.6. K+ accumulated continuously during the plateau to a level which increased external K concentration by about 1 mm. This increase in the subendothelial space corresponds to about 1-3 ,#A/cm2 or 10-30 pmole/cm2. sec-of net K+ efflux. These values are at least an order of magnitude larger than required to discharge the membrane capacitance.7. There is no direct relation between action potential duration and rate of development or magnitude of K+ accumulation during that action potential.8. Increase in the external K concentration, while shortening the action potential and depolarizing the membrane, does not lead to an increased rate of accumulation of K+. The presence of Ni2+, on the other hand, prolongs the action potential and decreases the rate of K+ accumulation.9. The results suggest that there is a substantial and continuous efflux of K+ during the action potential, which sums during rapid beating, resulting in membrane depolarization and alteration of action potential duration. The change in action potential duration in response to rate may be caused by alteration of EK in the local micro-environments.

Potassium currents in frog ventricular muscle: evidence from voltage clamp currents and extracellular K accumulation.

“…It is therefore reasonable to postulate that the accumulation of K+ during the action potential would have little effect on the shape or the time course of the plateau at the postive membrane potentials. In this respect it has been shown that the rate of K accumulation during the action potential plateau, as measured with K-selective micro-electrodes, does not change when the [K]o was altered (Kline & Morad, 1978). On the other hand, as the plateau repolarizes toward -20 mV the inwardly rectifying K current becomes more dominant and initiates the rapid repolarization.…”

Effects of acid‐base changes on excitation‐‐contraction coupling in guinea‐pig and rabbit cardiac ventricular muscle.

“…They have suggested that such shifts are mediated by accumulations of K+ in the restricted spaces between individual Purkinje cells. There is evidence for a K+ accumulation in the less restricted spaces between ventricular cells (Kline & Morad, 1978), so that any explanation may be common to the two tissues. Brown et al (1978) proposed three ways whereby an acidosis could lead to K+ accumulation: (1) inhibition of the Na+-K+ pump, (2) modification of the sarcolemmal K+ permeability, (3) reduction in the fixed negative charge between the intercellular clefts.…”

The temperature dependence of electrical excitability in fish hearts

“…Thermal modulation of excitation may involve the accumulation of K + ions in the intercellular space and frequency-dependent changes in the amplitude of ion currents (Kline and Morad, 1978), which should be taken into account in experimental procedures. Comparison of results from isolated cells, spontaneously active multicellular preparations (sinoatrial tissues, working whole hearts) and in vivo ECG recordings would help to elucidate the significance of molecular and cellular mechanisms in the thermal response of the whole heart Badr et al, 2016).…”