Activity-dependent changes in the short-term electrical properties of neurites were investigated in the anterior pagoda (AP) cell of leech. Imaging studies revealed that backpropagating Na(+) spikes and synaptically evoked EPSPs caused Ca(2+) entry through low-voltage-activated Ca(2+) channels that are distributed throughout the neurites. Voltage-clamp recordings from the soma revealed a TEA-sensitive outward current that was reduced when Ca(2+) entry was blocked with Co(2+) or when the intracellular concentration of free Ca(2+) was reduced by a high-affinity Ca(2+) buffer. Ca(2+) released in the neurite from a caged Ca(2+) compound caused a hyperpolarization of the membrane potential. These data imply that the AP cell expresses Ca(2+)-activated K(+) conductances, and that these conductances are present in the neurites. When the Ca(2+)-activated K(+) current was reduced through the block of Ca(2+) entry, backpropagating Na(+) spikes and synaptically evoked EPSPs increased in amplitude. Hence, the activity-dependent changes in the intracellular [Ca(2+)] together with the Ca(2+)-activated K(+) conductances participate in the regulation of dendritic signal propagation.