Extracellular potassium ion activity and electrophysiology in the hippocampal slice: paradoxical recovery of synaptic transmission during anoxia

Abstract

The relationship between extracellular potassium ion activity and neuronal excitability during anoxia was investigated in hippocampal slices in vitro. Extracellular field potentials and K+ activity were measured with double-barreled ion-selective microelectrodes placed either in the stratum pyramidale or stratum radiatum of field CA1. Orthodromic spike activity of CA1 pyramidal cells and field excitatory postsynaptic potentials (f-EPSPs) failed rapidly after anoxia with little change in potassium ion activity and without failure of the Schaffer collateral prevolley or antidromic responses of pyramidal cells. As [K+]o approached 8-10 mM, f-EPSPs and orthodromic spike activity recovered spontaneously. Continued anoxia resulted in massive release of K+ into the extracellular space and complete electrical silence. Presynaptic activity and antidromically elicited spike activity recovered promptly upon reoxygenation after anoxia, but synaptic transmission remained blocked for many minutes. Spontaneous recovery of f-EPSPs and spike activity suggests that a simple mechanism involving depolarization or hyperpolarization of neuronal elements cannot account for failure of synaptic transmission observed during anoxia. However, continued elevation of [K+]o and the associated loss of pre- and postsynaptic excitability with more prolonged anoxia indicated that depolarization was responsible for the eventual electrical silence as anoxia progressed.