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.