Extracellular potassium levels and axon excitability during repetitive action potentials in crayfish.

Abstract

SUMMARY1. Changes in extracellular K+ levels were measured during repetitive stimulation of the excitor axon of the opener muscle of the crayfish walking leg.2. Mesaxon channels, through which K+ might diffuse away from the periaxonal ('Frankenhaeuser-Hodgkin') space, were examined in electron micrographs; they were seen every 2-10 jam along the axon, and their average (± S.D.) length and width were 3 0 (± 1-6) gsm and 19'8 (± 8 9) nm, respectively.3. Intracellular recordings revealed a 40 ms after-depolarization following an action potential; this was attributed to elevated levels of extracellular K+. During stimulation at 50 Hz, this resulted in a depolarizing shift of the membrane potential between impulses; the average depolarization was 9-3 mV, which corresponds to a 4-3 mM increase in extracellular K+.4. Using K+-selective micro-electrodes, changes in extracellular K+ activity, AaK, were measured at distances ranging from 10 to 50 ,um from the axon; during 50 Hz stimulation, AaK rose within 15 s to a maximum value of 1 1 mm which was maintained at a steady level in most preparations.5. Conduction failure occurred in several preparations after at least 90 s of stimulation; levels of AaK were not abnormally high in these cases.6. Soaking the axon for at least 15 min in saline with extracellular K+ levels at least 18 mm above normal values was necessary to cause blockage in unstimulated nerves.7. Soaking the preparation for 30 min in 10-3 M-ouabain resulted in a 48 % increase in the maximum values of AaK during 50 Hz stimulation.8. It is concluded that K+ accumulates extracellularly during axon stimulation and that the extent of this accumulation is reduced by active uptake mechanisms; however, this accumulation probably cannot directly block action potential conduction, for neither the magnitude nor the kinetics of K+ build-up approach values shown to reduce excitability.

Excitation block in a nerve fibre model owing to potassium-dependent changes in myelin resistance

“…Similar patterns of intermittent failure have been demonstrated by Krnjevic & Miledi [39,40] in the rat. Oscillations of extracellular potassium during intermittent block can be seen in the study of Smith [41], figure 4. This study was performed on an un-myelinated nerve, but the conduction failure must be related to a similar K þ -mediated mechanism, since it takes place where the sheath is thinner and the periaxonal space is reduced [42].…”

Computation of action potential propagation and presynaptic bouton activation in terminal arborizations of different geometries

“…Depending on the interpulse interval, facilitation or depression of synapse activation could be expected. It has been shown that potassium buildup in the periaxonal space during repetitive activation of an axon contributes to the development of conduction failure (Grossman et al, 1979a, b;Smith, 1983a). This mechanism, working on a slow time-scale, would interact with the structural features of the terminal arborizations and the refractory and supernormal periods of the axon membrane.…”

Functions of Invertebrate Glia

“…Similar maximum increments may take place in the leech (Kuffler 1967;Schlue and Walz 1984), crayfish (Smith 1983) and insect compound eye (Coles and Tsacopoulos 1979). A probable increment of about 5 mM takes place around neurones that are active under normal physiological conditions.…”