The effect of action potentials on the calcium concentration in the somata of chick ciliary neurons ([Ca2+]s) was determined by loading these with the calcium indicator calcium green-1. Following trains of 1-10 impulses (30 Hz) to the postganglionic nerve, the [Ca2+]s increased rapidly and then declined along a single exponential with a time constant of 0.70 +/- 0.04 s (fast phase). After trains of 20 or 50 impulses, the elevated [Ca2+]s declined as the sum of two exponentials, with time constants of 0.78 +/- 0.12 s (fast phase) and 4.0 +/- 0.4 s (moderate phase). After a 600-impulse postganglionic train of impulses, the elevated [Ca2+]s declined quickly over about 1 s, and then as the sum of two exponentials: that of the moderate phase and a slower component with a time constant of 109 +/- 16 s (slow phase). Similar time courses were observed following stimuli to the preganglionic nerve. Caffeine (3 mM) and ryanodine (20 microM) both sped the fast phase and slowed the moderate phase of [Ca2+]s decline. Carbonyl cyanide m-chlorophenyl hydrazone (CCCP, 2 microM) slowed the slow phase, without affecting the other phases of decline. These results are discussed in relation to identifying the mechanisms responsible for these different phases of Ca2+ removal.