Transient extracellular potassium accumulation produced prolonged depolarizations during synchronized bursts in picrotoxin-treated cockroach CNS

Exposure of the isolated cockroach central nervous system (CNS) to picrotoxin (10^-5 M) results in an increase in spontaneous synaptic activity recorded from giant interneurons (GIN). After 5-7 min, spontaneous synaptic potentials recorded from the nerve cord tend to organize into distinct bursts. During these bursts, prolonged depolarizations (PD) are intracellularly recorded from the GIN. PDs are associated with a conductance increase, which can be entirely accounted for by membrane rectification. Measurements of the action potential afterhyperpolarization (AHP) indicate that during the PD, the extracellular potassium concentration ([K⁺](o)) in the periaxonal space is elevated. Direct measurement of [K⁺](o) with ion-sensitive microelectrodes reveals a transient increase of up to 3 mM. The results demonstrate that the PDs recorded from the giant axons are a consequence of increased [K⁺](o) due to synchronized activity of many fibers. However, the membrane depolarization of the GIN is larger than that expected from the observed change in the potassium equilibrium potential. Several mechanisms that may account for this phenomena are discussed.