Stimulation-evoked changes in extracellular K+ and Ca2+ in pyramidal layers of the rat's hippocampus

Abstract

In urethane-anesthetized rats, ion-selective microelectrodes recorded changes in extracellular K+ and Ca2+ concentrations (.DELTA.[K+]o and .DELTA.[Ca2+]o) in pyramidal layers of the hippocampus (mostly in area CA1), which were evoked by fimbrial-commissural stimulation. [K+]o increased linearly with frequency of stimulation up to a critical frequency, in the range of 2-5 Hz, where bursts of population spikes appeared, and then rose rapidly to reach a ceiling of 9-12 mM. During continued stimulation, [K+]o remained well above the resting level of .apprx. 3.0 mM. At the end of stimulation [K+]o returned to the base line with a half time of 4-8 s, and a minor undershoot of .simeq. 0.5 mM was detectable for 1-2 min. When stimulating at frequencies above the critical value, a sharp fall in [Ca2+]o (by an average of 1/3 below the mean resting level of 1.4 mM) consistently started 1-5 s after the onset of the rapid phase of .DELTA.[K+]o. [Ca2+]o typically reached a minimum in 5-10 s and immediately started to return towards the base line. The recovery of [Ca2+]o was often accelerated by an overshoot of up to 0.3 mM; this was followed by a delayed phase of low [Ca2+]o for another 2-3 min. During prolonged stimulation at frequencies near 7 Hz, both [Ca2+]o and [K+]o fluctuated periodically, in time with the appearance and disappearance of bursts of population spikes. Comparable observations were made in area CA2-3 (just external to CA1); in the deeper areas of CA3, in CA4 and in the dentate gyrus, major changes in [K+]o and [Ca2+]o (as well as bursts of population spikes) were evoked only by prolonged fimbrial stimulation at higher frequencies (.simeq. 10 Hz). Although adequate repetitive stimulation of fimbrial-commissural inputs evokes sharp but opposite changes in [K+]o and [Ca2+]o, the fall in [Ca2+]o is consistently much briefer than the rise in [K+]o, presumably because of the evanescent character of postsynaptic Ca2+ spikes.