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The axons of dentate gyrus granule cells form synapses in the hilus. Ca2+ signaling was investigated in the boutons of these axons using confocal fluorescence imaging. Boutons were loaded with various concentrations of the Ca2+indicator Oregon Green BAPTA-1 by patch-clamping the cell bodies and allowing the dye to diffuse into the axon. Resting free [Ca2+] started at 74 nm, rose to ∼1 μm immediately after an action potential, and then decayed to rest with a time constant of 43 msec (all extrapolated to a dye concentration of zero). Action potential-induced [Ca2+] rises were smaller in larger boutons, consistent with a size-independent Ca2+ channel density of 45/μm2. Action potential-induced [Ca2+] changes varied with dye concentration in a manner consistent with κE ∼20 for the ratio of endogenous buffer-bound Ca2+ to free Ca2+. During trains of action potentials, [Ca2+] increments summed supralinearly by more than that expected from dye saturation. The amount of endogenous Ca2+ buffering declined as [Ca2+] rose, and this saturation indicated a buffer with a dissociation constant of ∼500 nm and a concentration of ∼130 μm. This is similar to the dissociation constant of calbindin-D28K, a Ca2+-binding protein that is abundant in dentate granule cells. Thus, calbindin-D28K is a good candidate for the Ca2+ buffer revealed by these experiments. The saturation of endogenous buffer can generate short-term facilitation by amplifying [Ca2+] changes during repetitive activity. Buffer saturation may also be relevant to the presynaptic induction of long-term potentiation at synapses formed by dentate granule cells.

Calcium Dynamics, Buffering, and Buffer Saturation in the Boutons of Dentate Granule-Cell Axons in the Hilus