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

Authors:
  • KKK. Krnjević
    K. Krnjević
  • MMM. E. Morris
    M. E. Morris
  • RRR. J. Reiffenstein
    R. J. Reiffenstein

Abstract
In urethane-anaesthetized rats, ion-selective microelectrodes recorded changes in extracellular K+ and Ca2+ concentrations (Δ[K+]o and Δ[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 about 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 [ ] was detectable for 1–2 min. When stimulating at frequencies above the critical value, a sharp fall in [Ca2+]o (by an average of one-third below the mean resting level of 1.4 mM) consistently started 1–5 s after the onset of the rapid phase of Δ[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 ([ ]). Thus, 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.