K+ accumulation and K+ conductance inactivation during action potential trains in giant axons of the squid Sepioteuthis.

Abstract

1. During action potential trains in giant axons from the squid Sepioteuthis, decline of the peak level of the undershoot potential was observed. The time course of the decline of the undershoot could be fitted with a three‐exponential function with time constants of approximately 25, approximately 400 and approximately 7,000 ms, respectively. 2. When the osmolarity of the external solution was doubled by adding glucose (1.2 M), the fast component of undershoot decline, but not the medium and slow components, was significantly reduced. 3. Under voltage clamp in high osmolarity solutions where K+ accumulation was completely removed, repeated depolarizing pulses at 40 Hz (designed to mimic a train of action potentials) elicited K+ currents whose peak value declined. The decline is consistent with inactivation of the K+ conductance (gK). The decline of gK was fitted by a two‐exponential function with time constants of approximately 400 and approximately 7,000 ms, respectively. 4. Interventions designed to modify Schwann cell physiology, such as high frequency stimulation (100 Hz, 2 min), externally applied ouabain (100‐500 microM), L‐glutamate (100 microM), ACh (100 microM), Co2+ (5mM), Ba2+ (2mM), or removal of external Ca2+ by EGTA, had no significant effects on the fast, medium or slow components of undershoot decline. 5. The results suggest that the fast component of undershoot decline represents K+ accumulation in the space between Schwann cell and axolemma. The medium and slow components are the result of axonal gK inactivation. Schwann cells appear to be involved in K+ clearance only to the extent that they provide an efficient physical pathway for the clearance of K+ by extracellular diffusion.

Computer Model for Action Potential Propagation Through Branch Point in Myelinated Nerves

“…The average thickness of the periaxonal space at the paranodal region is 5 nm in our standard model. Previous theoretical and experimental results provided different values for K clearance in the squid giant axon, ranging from 10 ms (Astion et al 1988) to 25 ms (Inoue et al 1997). In our standard model, the time constant for K clearance was set at 10 ms at 37°C or 20 ms at 20°C…”

Activity‐dependent change in morphology of the glial tubular lattice of the crayfish medial giant nerve fiber

“…These results are to be expected if active transport and glial metabotropic receptors are important in K 1 clearance (Brunder and Lieberman, 1988;Hassan and Lieberman, 1988;Lieberman and Hassan, 1988). In contrast, metabolic poisons or metabotropic receptor agonists were reported to have no effect on K 1 clearance in the experiments reported by Inoue et al (1997). Since the experiments by Inoue et al (1977) were performed at 12°C on the giant fiber from the tropical squid, Sepioteuthis, acclimatized to water temperatures of 30°C, it is possible that glial metabolic processes were slowed leaving them less responsive to metabolic poisons and receptor agonists or antagonists.…”

“…This study focused on a reexamination of the concept that the tubular lattice serves only as a simple ion diffusion pathway with the goal to provide experimental evidence for a structural basis for K 1 clearance from the adaxonal space of axons stimulated at high frequency. Inoue et al (1997) using a pulsed voltage clamp protocol and K 1 current inactivation analysis suggests that K 1 clearance from the adaxonal space can be accounted for by passive diffusion through the inter-glial spaces and glial tubular lattice structures in the squid giant nerve fiber. There are two lines of evidence that make it unlikely that diffusion, alone, can account for K 1 clearance from the crayfish medial giant nerve fiber.…”

“…Reinvestigations of K 1 clearance from both squid and crayfish giant nerve fibers (Shrager et al, 1983;Pichon et al, 1987;Abbott et al, 1988) have shown that K 1 clearance is, in fact, quite rapid (10 ms) in carefully prepared and well-oxygenated nerve fiber preparations. Based on mathematical models of the extracellular space that included the glial tubular lattice as proposed by Brown and Abbott (1993), Inoue et al (1997) used pulsed voltage-clamp to evaluate K 1 current inactivation kinetics and K 1 accumulation resulting from propagated action potentials. Their results led them to argue that diffusion alone can account for rapid clearance of K 1 from the adaxonal space of the squid giant axon.…”

Scalp Acupuncture Effects of Stroke Studied with Magnetic Resonance Imaging: Different Actions in the Two Stroke Model Rats

“…28 If this occurs, K is accumulated in the F-H space. 29 As the neurons are not injured but simply lost the capability of propagating action potentials by the K + depolarisation, the propagation failure can be immediately restored when the F-H space widens by the reduction in vasogenic oedema. This may explain the rapid recovery from neurological dysfunction when the vasogenic oedema was reduced.…”