Comparison of Spontaneous and Evoked Activity of CA1 Pyramidal Cells and Dentate Gyrus Granule Cells of the Hippocampus at an Increased Extracellular Potassium Concentration

Abstract

In this work the effect of changing extracellular potassium concentration ([K⁺]_o) on spontaneous and evoked burst activity of glutamatergic neurons in the mouse hippocampus was investigated using the whole-cell patch clamp technique. It was shown that the increase of [K⁺]_o from 3 to 8.5 mM (potassium load): (1) induced spontaneous tonic and pacemaker burst activity in CA1 pyramidal cells (20% and 10% of total cells, respectively) but did not result in the emergence of pacemaker granule cells in the dentate gyrus (DG). (2) Similarly, potassium load increased the evoked burst activity of CA1 pyramidal cells and, paradoxically, suppressed the burst activity of DG granule cells over the entire range of current steps from 10 to 200 pA. (3) Potassium load caused a rightward shift of the current–voltage (I/V) curves in both cell types, decreasing the reversal potential E_rev and increasing the slope of the I/V curves (amplitudes of inward currents at voltages from –100 mV to –70 mV) in the CA1 and DG neurons 2–3- and 4–5-fold, respectively. (4) Potassium load produced an opposite effect on outward currents, causing a significant increase in current amplitude in pyramidal cells and a decrease in granule cells (at membrane voltages above 0 mV). The inward and outward currents of DG neurons were 4–4.5 times higher than those of CA1 neurons. The possible involvement of potassium-activated and other potassium-conducting channels in different excitability responses of glutamatergic CA1 and DG neurons under potassium load is discussed. The high sensitivity of CA1 pyramidal cells to potassium load compared to DG granule cells may play an important role in hyperexcitation of neuronal networks during epileptogenesis.