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NEUROSCIENCE |
1 Physiological Institute I, University of Freiburg, Hermann-Herder-Str. 7, D-79104 Freiburg, Germany
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 Ca2+-permeable receptors, Ca2+-binding proteins and Ca2+-dependent signalling molecules, physiological Ca2+ signalling in these interneurons has not been investigated. To study action potential (AP)-induced dendritic Ca2+ influx and buffering, we combined whole-cell patch-clamp recordings with ratiometric Ca2+ imaging from the proximal apical dendrites of rigorously identified BCs in acute slices, using the high-affinity Ca2+ indicator fura-2 or the low-affinity dye fura-FF. Single APs evoked dendritic Ca2+ transients with small amplitude. Bursts of APs evoked Ca2+ transients with amplitudes that increased linearly with AP number. Analysis of Ca2+ transients under steady-state conditions with different fura-2 concentrations and during loading with 200 µM fura-2 indicated that the endogenous Ca2+-binding ratio was
200 (
S = 202 ± 26 for the loading experiments). The peak amplitude of the Ca2+ transients measured directly with 100 µM fura-FF was 39 nM AP–1. At
23°C, the decay time constant of the Ca2+ 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 Ca2+ concentration that was proportional to AP number, whereas more intense stimulation was required to reach micromolar Ca2+ concentrations and to shift Ca2+ signalling into a non-linear regime. In conclusion, dentate gyrus BCs show a high endogenous Ca2+-binding ratio, a small AP-induced dendritic Ca2+ influx, and a relatively slow Ca2+ extrusion. These specific buffering properties of BCs will sharpen the time course of local Ca2+ signals, while prolonging the decay of global Ca2+ signals.
(Received 30 October 2007;
accepted after revision 11 February 2008;
first published online 14 February 2008)
Corresponding author P. Jonas: Physiological Institute I, University of Freiburg, Hermann-Herder-Str. 7, D-79104 Freiburg, Germany. Email: peter.jonas{at}physiologie.uni-freiburg.de
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