Axonal and glial currents activated during the post-tetanic hyperpolarization in non-myelinated nerve

Abstract

Changes in membrane potential and potassium concentration in the extracellular space ([K+]e) of rabbit vagus nerve were measured simultaneously during electrical activity and during the period of recovery using a modified sucrose-gap method and potassium-sensitive microelectrodes. After stimulation for 15 s at 15 Hz the main activity-induced increase in [K+]e reached 16.9 mM. This increase in [K+]e was paralleled by a depolarization of the preparation. The period of activity was followed by a post-tetanic hyperpolarization (PTH) lasting tens of seconds, generated by the axonal electrogenic Na+-K+ pump and to a lesser extent by the pump of the surrounding Schwann cells. The amplitude of the PTH dramatically increased in experiments in which inward currents were blocked by removal of Cl– or after application of Cs+ or Ba2+, indicating that under normal conditions the current generated by the Na+-K+ pump is strongly short-circuited. A pharmacological and kinetic study showed that these currents are: (1) the hyperpolarization-activated current I h, and (2) the inwardly rectifying I KIR current. The results show that the latter originates from Schwann cells. Our data indicate that in non-myelinated nerves there is a subtle association of inward ionic channels which (1) helps the cell to maintain an optimal membrane potential after a period of activity, and (2) contributes to the removal of excess K+ from the extracellular space.

Na+/K+ pump interacts with the h-current to control bursting activity in central pattern generator neurons of leeches

“…The possible interaction between the pump current and the h -current has been suggested by previous studies on slow afterhyperpolarizations (e.g., Robert and Jirounek, 1998; Soleng et al, 2003; Baginskas et al, 2009). For example, when Robert and Jirounek (1998) recorded the slow afterhyperpolarization (described by the authors as a slow posttetanic hyperpolarization), which occurs after a burst of compound action potentials, in the rabbit vagus nerve, they found that blocking the h -current or the inward rectifier K + with Cs + and Ba 2+ , respectively, would increase the amplitude of the slow afterhyperpolarization.…”

“…Previous studies in other systems have suggested that the h -current might counteract the hyperpolarizing effects of the pump current (e.g., Robert and Jirounek, 1998; Soleng et al, 2003; Baginskas et al, 2009). Moreover, Hill et al (2001) developed a canonical model of the oscillator heart interneurons and showed that increasing the h -current conductance decreases the period, which was later supported by dynamic clamp experiments (Sorensen et al, 2004; Olypher et al, 2006).…”

“…For example, when Robert and Jirounek (1998) recorded the slow afterhyperpolarization (described by the authors as a slow posttetanic hyperpolarization), which occurs after a burst of compound action potentials, in the rabbit vagus nerve, they found that blocking the h -current or the inward rectifier K + with Cs + and Ba 2+ , respectively, would increase the amplitude of the slow afterhyperpolarization. Because the slow afterhyperpolarization has been documented to be a product of the pump current, Robert and Jirounek (1998) hypothesized that the h -current and the inward rectifier K + current may serve to counterbalance the effects of the pump current under normal conditions. Such a counterbalancing role by the h -current could explain the previously mentioned paradoxical shortening of the period when we stimulated the pump in the heart interneurons.…”

Beyond faithful conduction: Short-term dynamics, neuromodulation, and long-term regulation of spike propagation in the axon

“…Because the pump exchanges three sodium ions for two potassium ions, strong activation leads to hyperpolarization. There is ample evidence for this type of hyperpolarization for many different types of axons, including invertebrate and vertebrate, myelinated and unmyelinated (Baker, 2000; Barrett and Barrett, 1982; Bostock and Bergmans, 1994; Gordon et al , 1990; Kiernan et al , 2004; Moldovan and Krarup, 2006; Robert and Jirounek, 1998; Scuri et al , 2007; Vagg et al , 1998; Van Essen, 1973). …”

P2 nucleotide receptors in peripheral nerve trunk

“…It has also been argued that Schwann cells might contribute to the d.c. potential [Robert and Jirounek, 1998]. As an alternative, we applied a flexible, stimulus-response data acquisition program with threshold tracking facilities for the study of P2 receptors in isolated peripheral mammalian nerves.…”