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We have investigated intracellular Ca<jats:sup>2+<\/jats:sup> transients induced by a single action potential (AP) in Retzius neurons <jats:italic>in situ<\/jats:italic> of isolated ganglia of the leech <jats:italic>Hirudo medicinalis<\/jats:italic> 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 Ca<jats:sup>2+<\/jats:sup> transient in submembrane regions, while in central regions no fluorescence change was detected. Burst activity evoked a much larger Ca<jats:sup>2+<\/jats:sup> influx, which elicited Ca<jats:sup>2+<\/jats:sup> signals in central somatic regions, including the cell nucleus. A single AP induced a Ca<jats:sup>2+<\/jats:sup> transient in distal branches of the axon and in dendrites that was significantly larger than in the proximal axon and in the cell body (<jats:italic>p<\/jats:italic> &lt; .05), and the recovery of the Ca<jats:sup>2+<\/jats:sup> transient was significantly faster in axonal branches than in dendrites (<jats:italic>p<\/jats:italic> &lt; .01). The AP\u2010induced Ca<jats:sup>2+<\/jats:sup> transient was inhibited by Co<jats:sup>2+<\/jats:sup> (2 m<jats:italic>M<\/jats:italic>). The P\/Q\u2010type Ca<jats:sup>2+<\/jats:sup> channel blocker \u03c9\u2010agatoxin TK (500 n<jats:italic>M<\/jats:italic>) and the L\u2010type Ca<jats:sup>2+<\/jats:sup> channel blocker nifedipine (20 \u03bc<jats:italic>M<\/jats:italic>) had no effect on the Ca<jats:sup>2+<\/jats:sup> transient, whereas the L\u2010type Ca<jats:sup>2+<\/jats:sup> channel blocker methoxyverapamil (D600, 0.5\u20131 m<jats:italic>M<\/jats:italic>) irreversibly reduced the Ca<jats:sup>2+<\/jats:sup> transient by 37% in axons and by 42% in dendrites. Depletion of intracellular Ca<jats:sup>2+<\/jats:sup> stores following inhibition of endoplasmic Ca<jats:sup>2+<\/jats:sup>\u2010ATPases by cyclopiazonic acid (10 \u03bc<jats:italic>M<\/jats:italic>) decreased the AP\u2010induced Ca<jats:sup>2+<\/jats:sup> transient in the dendrites by 21% (<jats:italic>p<\/jats:italic> &lt; .01), but not in axons, and increased the Ca<jats:sup>2+<\/jats:sup> recovery time constant (\u03c4) in the axonal branches by 129% (<jats:italic>p<\/jats:italic> &lt; .01), but not in dendrites. The results indicate that an AP evokes a voltage\u2010gated Ca<jats:sup>2+<\/jats:sup> influx into all subcompartments of the Retzius neuron, where it produces a Ca<jats:sup>2+<\/jats:sup> 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. \u00a9 2001 John Wiley &amp; Sons, Inc. 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