Efficient Ca 2+ buffering in fast‐spiking basket cells of rat hippocampus

Fast‐spiking parvalbumin‐expressing basket cells (BCs) represent a major type of inhibitory interneuron in the hippocampus. These cells inhibit principal cells in a temporally precise manner and are involved in the generation of network oscillations. Although BCs show a unique expression profile of Ca 2+ ‐permeable receptors, Ca 2+ ‐binding proteins and Ca 2+ ‐dependent signalling molecules, physiological Ca 2+ signalling in these interneurons has not been investigated. To study action potential (AP)‐induced dendritic Ca 2+ influx and buffering, we combined whole‐cell patch‐clamp recordings with ratiometric Ca 2+ imaging from the proximal apical dendrites of rigorously identified BCs in acute slices, using the high‐affinity Ca 2+ indicator fura‐2 or the low‐affinity dye fura‐FF. Single APs evoked dendritic Ca 2+ transients with small amplitude. Bursts of APs evoked Ca 2+ transients with amplitudes that increased linearly with AP number. Analysis of Ca 2+ transients under steady‐state conditions with different fura‐2 concentrations and during loading with 200 μ m fura‐2 indicated that the endogenous Ca 2+ ‐binding ratio was ∼200 (κ S = 202 ± 26 for the loading experiments). The peak amplitude of the Ca 2+ transients measured directly with 100 μ m fura‐FF was 39 n m AP −1 . At ∼23°C, the decay time constant of the Ca 2+ transients was 390 ms, corresponding to an extrusion rate of ∼600 s −1 . At 34°C, the decay time constant was 203 ms and the corresponding extrusion rate was ∼1100 s −1 . At both temperatures, continuous theta‐burst activity with three to five APs per theta cycle, as occurs in vivo during exploration, led to a moderate increase in the global Ca 2+ concentration that was proportional to AP number, whereas more intense stimulation was required to reach micromolar Ca 2+ concentrations and to shift Ca 2+ signalling into a non‐linear regime. In conclusion, dentate gyrus BCs show a high endogenous Ca 2+ ‐binding ratio, a small AP‐induced dendritic Ca 2+ influx, and a relatively slow Ca 2+ extrusion. These specific buffering properties of BCs will sharpen the time course of local Ca 2+ signals, while prolonging the decay of global Ca 2+ signals.