Calcium transients in subcompartments of the leech retzius neuron as induced by single action potentials

Regional Ca2+ influx into neurons plays an essential role for fast signal processing, yet it is little understood. We have investigated intracellular Ca2+ transients induced by a single action potential (AP) in Retzius neurons in situ of isolated ganglia of the leech Hirudo medicinalis using confocal laser scanning microscopy in the cell body, in different axonal branches, and in dendrites, In the cell body, a single AP induced a Ca2+ transient in submembrane regions, while in central regions no fluorescence change was detected. Burst activity evoked a much larger Ca2+ influx, which elicited Ca2+ signals in central somatic regions, including the cell nucleus. A single AP induced a Ca2+ transient in distal branches of the axon and in dendrites that was significantly larger than in the proximal axon and in the cell body (p < .05), and the recovery of the Ca2+ transient was significantly faster in axonal branches than in dendrites (p < .01). The AP-induced Ca2+ transient was inhibited by Co2+ (2 mM). The P/Q-type Ca2+ channel blocker -agatoxin TK (500 nM) and the L-type Ca2+ channel blocker nifedipine (20 muM) had no effect on the Ca2+ transient, whereas the L-type Ca2+ channel blocker methoxyverapamil (D600, 0.5-1 mM) irreversibly reduced the Ca2+ transient by 37% in axons and by 42% in dendrites. Depletion of intracellular Ca2+ stores following inhibition of endoplasmic Ca2+-ATPases by cyclopiazonic acid (10 muM) decreased the AP-induced Ca2+ transient in the dendrites by 21% (p < .01), but not in axons, and increased the Ca2+ recovery time constant (<tau>) in the axonal branches by 129% (p < .01), but not in dendrites. The results indicate that an AP evokes a voltage-gated Ca2+ influx into all subcompartments of the Retzius neuron, where it produces a Ca2+ signal of different size and/or kinetics. This may contribute to the modulation of electrical excitation and propagation of APs, and to different modes of synaptic and nonsynaptic processes. (C) 2001 John Wiley & Sons, Inc.