Efficient Ca(2+) buffering in fast-spiking basket cells of rat hippocampus

Y. Aponte, J. Bischofberger, P.M. Jonas, Journal of Physiology 586 (2008) 2061–75.


Journal Article | Published
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Abstract
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 microm fura-2 indicated that the endogenous Ca(2+)-binding ratio was approximately 200 (kappa(S) = 202 +/- 26 for the loading experiments). The peak amplitude of the Ca(2+) transients measured directly with 100 microm fura-FF was 39 nm AP(-1). At approximately 23 degrees C, the decay time constant of the Ca(2+) transients was 390 ms, corresponding to an extrusion rate of approximately 600 s(-1). At 34 degrees C, the decay time constant was 203 ms and the corresponding extrusion rate was approximately 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.
Publishing Year
Date Published
2008-01-01
Journal Title
Journal of Physiology
Volume
586
Issue
8
Page
2061 - 75
IST-REx-ID

Cite this

Aponte Y, Bischofberger J, Jonas PM. Efficient Ca(2+) buffering in fast-spiking basket cells of rat hippocampus. Journal of Physiology. 2008;586(8):2061-2075. doi:10.1113/jphysiol.2007.147298
Aponte, Y., Bischofberger, J., & Jonas, P. M. (2008). Efficient Ca(2+) buffering in fast-spiking basket cells of rat hippocampus. Journal of Physiology, 586(8), 2061–2075. https://doi.org/10.1113/jphysiol.2007.147298
Aponte, Yexica, Josef Bischofberger, and Peter M Jonas. “Efficient Ca(2+) Buffering in Fast-Spiking Basket Cells of Rat Hippocampus.” Journal of Physiology 586, no. 8 (2008): 2061–75. https://doi.org/10.1113/jphysiol.2007.147298.
Y. Aponte, J. Bischofberger, and P. M. Jonas, “Efficient Ca(2+) buffering in fast-spiking basket cells of rat hippocampus,” Journal of Physiology, vol. 586, no. 8, pp. 2061–75, 2008.
Aponte Y, Bischofberger J, Jonas PM. 2008. Efficient Ca(2+) buffering in fast-spiking basket cells of rat hippocampus. Journal of Physiology. 586(8), 2061–75.
Aponte, Yexica, et al. “Efficient Ca(2+) Buffering in Fast-Spiking Basket Cells of Rat Hippocampus.” Journal of Physiology, vol. 586, no. 8, Wiley-Blackwell, 2008, pp. 2061–75, doi:10.1113/jphysiol.2007.147298.

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