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The Journal of Neuroscience, January 19, 2005, 25(3):558-565; doi:10.1523/JNEUROSCI.3799-04.2005

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Cellular/Molecular
Endogenous Ca²⁺ Buffer Concentration and Ca²⁺ Microdomains in Hippocampal Neurons

Andreas Müller,¹ Maria Kukley,¹ Pia Stausberg,¹ Heinz Beck,² Wolfgang Müller,³ and Dirk Dietrich¹

Departments of ¹Neurosurgery and ²Epileptology, University Clinic Bonn, D-53105 Bonn, Germany, and ³Charite, Neurowissenschaftliches Forschungszentrum, D-10117 Berlin, Germany

Ca²⁺-binding proteins are ubiquitously expressed throughout the CNS and serve as valuable immunohistochemical markers for certain types of neurons. However, the functional role of most Ca²⁺-binding proteins has to date remained obscure because their concentration in central neurons is not known. In this study, we investigate the intracellular concentration of the widely expressed Ca²⁺-binding protein calbindin-D_28k in adult hippocampal slices using patch-clamp recordings and immunohistochemistry. First, we show that calbindin-D_28k freely exchanges between patch pipette and cytoplasm during whole cell patch-clamp recordings with a time constant of 10 min. Substituting known concentrations of recombinant calbindin-D_28k in patch pipettes enabled us to determine the endogenous calbindin-D_28k concentration by postrecording immunohistochemistry. Using this calibration procedure, we find that mature granule cells (doublecortin-) contain 40 µM, and newborn granule cells (doublecortin+) contain 0-20 µM calbindin-D_28k. CA3 stratum radiatum interneurons and CA1 pyramidal cells enclose 47 and 45 µM calbindin-D_28k, respectively. Numerical simulations showed that 40 µM calbindin-D_28k is capable of tuning Ca²⁺ microdomains associated with action potentials at the mouth of single or clustered Ca²⁺ channels: calbindin-D_28k reduces the increment in free Ca²⁺ at a distance of 100 and 200 nm by 20 and 35%, respectively, and strongly accelerates the collapse of the Ca²⁺ gradient after cessation of Ca²⁺ influx. These data suggest that calbindin-D_28k equips hippocampal neurons with 160 µM mobile, high-affinity Ca²⁺-binding sites (_S 200) that slow and reduce global Ca²⁺ signals while they enhance the spatiotemporal fidelity of submicroscopic Ca²⁺ signals.

Key words: calcium; calcium binding ratio; adult neurogenesis; confocal laser scanning microscopy; buffered calcium diffusion; single compartment model

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Received Sep 14, 2004; revised November 18, 2004; accepted November 22, 2004.

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