The effect of synaptic activation on the extracellular potassium concentration in the hippocampal dentate area, in vitro

Abstract

Excitatory synaptic inputs to the granule cells of the dentate area elicit first of all EPSPs and then action potentials in the cells, giving rise to the characteristic extracellular field potentials referred to as the synaptic wave and population spike 13. The excitability of the cell population is easily altered by prior conditioning shocks or trains of shocks 1-~,9,13, though the mechanisms of these alterations are not fully understood. It is possible that potassium (K +) etttux from the granule cells might account for some of the alterations in excitability. It is already known that large increases in extracellular potassium concentration can accompany states of abnormal cortical function such as spreading depression 7,1°,17 and epilepsy 6. In this study we have used K+-sensitive microelectrodes 18 to show that there are detectable changes in the K + concentration around the dentate granule cells of the guinea pig hippocampus after synaptic activation of a well defined afferent pathway. We are not at present able to say whether such changes in fact account for changes in excitability of the cell population. Slices from the ventral surface of the hippocampus of guinea-pig brains were cut approximately 500 #m thick and maintained at 20-23 °C in vitro, cut surface uppermost, at the surface of an oxygenated saline solution (NaC1 124 mM, NaHCO3 24 mM, NaH2POa 1.25 mM, KC1 6 mM, CaCI2 4 mM, MgSOa 2 mM, glucose 10 mM) under an atmosphere of moist 95 ~o 02-5 ~ COz. The bath K + concentration is approximately twice that of brain extracellular fluidS,n; this high level has been employed by previous workers using similar techniques 4,15,~9, and in our hands it favours the occurrence of synaptic activation comparable to that seen in the intact hippocampus. Some nerve fibres do, however, behave abnormally in 6 mM potassium in vitro and normally in 3 mM potassium s. In the present experiments the pO2 is higher than in vivo and the temperature lower: both these conditions favour the survival of relatively thick slices with the least damage to cells. In view of the various