Characterizing the persistent CA3 interneuronal spiking activity in elevated extracellular potassium in the young rat hippocampus

Abstract

Seizures coincide with an increase in extracellular potassium concentrations [K +] e yet little information is available regarding this phenomenon on the firing pattern, frequency and neuronal properties of inhibitory neurons responsible for modulating network excitability. Therefore, we investigated the effects of elevating [K +] e from 2.5 to 12.5 mM on CA3 rat hippocampal interneurons in vitro using whole-cell patch-clamp recordings. We found that the majority of interneurons (21/25) in artificial cerebral spinal fluid (aCSF) exhibited spontaneous tonic spiking activity. As the [K +] e increased to 12.5 mM, interneurons exhibited a tonic, irregular, burst firing activity, or a combination of these. The input resistance decreased significantly to 59 ± 18% at 7.5 mM K + and did not further change at higher [K +] e while the amount of K +-induced depolarization significantly increased from 5 to 12.5 mM K + perfusion; a depolarization block occurred in 4 of the 12 interneurons at 12.5 mM. Also, as [K +] e increased, a transition from lower (1.3 ± 0.6 Hz) to higher dominant peak frequency (15.0 ± 5.0 Hz) was observed. We found that non-fast spiking (NFS) interneurons represented the majority of cells recorded and exhibited mostly tonic firing activity in raised K +. Fast spiking (FS) interneurons predominately had a tonic firing pattern with very few exhibiting bursting activity in elevated K +. In conclusion, we report that raised [K +] e in amounts observed during seizures increases hippocampal CA3 interneuronal activity and suggests that a loss or impairment of inhibitory function may be present during these events.