Fast network oscillations induced by potassium transients in the rat hippocampus in vitro

Brief pressure ejection of solutions containing potassium, caesium or rubidium ions into stratum radiatum of the CA1 or CA3 regions of the hippocampal slice evoked a fast network oscillation. The activity evoked lasted approximately 3-25 s with the predominant frequency component being in the gamma frequency range (30-80 Hz), although beta frequency (15-30 Hz) and ultrafast (> 80 Hz) components could also be seen. The gamma frequency component of the oscillation remained constant, even when large changes in power occurred, and was synchronous across the CA1 region. Measurements with potassium ion-sensitive electrodes revealed that the network oscillation was accompanied by increases (0.5 to 2.0 mM) in the extracellular potassium concentration [K+]o. Bath application of the N-methyl-D-aspartate (NMDA) receptor antagonists D(-)-2-amino-5-phosphonopentanoic acid (D-AP5; 50 microM) had no significant effect but the alpha-amino-3-hydroxy-5-methyl-4-isooxazolepropionic acid (AMPA)/kainate receptor antagonist 2,3,-dioxo-6-nitro-1,2,3,4-tetrahydrobenzo[f]quinoxaline-7-sulphonamide disodium (NBQX; 20 microM) caused a significant reduction (86.7 +/- 4.5 %) in the power in the gamma frequency range. Residual rhythmic activity, presumably arising in the interneuronal network, was blocked by the GABA(A) receptor antagonist bicuculline. The putative gap junction blocker octanol caused a decrease in the power of the gamma frequency component of 75.5 +/- 5.6 %, while carbenoxolone produced a reduction of only 14 +/- 42 %. These experiments demonstrate that a modest increase in exogenous [K+]o in the hippocampus in vitro is sufficient to evoke a fast network oscillation, which is an emergent property of the synaptically and electrically interconnected neuronal network.