The cross-commissural (CC) cell in the supraesophageal ganglion of the giant barnacle, Balanus nubilus, was stimulated intrasomatically and antidromically in normal saline and 3 X 10(-7) M tetrodotoxin (TTX) saline. The action potential in normal saline contained both sodium and calcium components, each independently capable of propagation. Evidence that the action potential in TTX saline was calcium dependent included: the amplitude of the spike in TTX saline increased monotonically with increasing calcium; it was blocked by the calcium channel blockers La, Ni, Cd and Co; and equimolar substitution of Ba or Sr for Ca in TTX saline supported regenerative activity. Evidence that the calcium component could propagate alone included: the distance over which the calcium action potential traveled exceeded the space constant of the axon; the biphasic nature of the extracellularly recorded action potential, which propagated to the axon in the nerve root, indicated inward regenerative current was occurring on the axon; electrotonically spread potentials were clearly distinguishable from active regenerative potentials. In addition, optical experiments using the calcium indicator dye arsenazo III (28) showed that the relative magnitude of the calcium signal was not diminished along the axon in TTX saline compared with normal saline. The critical external calcium concentration necessary to support the propagating action potential in TTX saline was estimated to be between 1.25 and 5 mM. To our knowledge, this is the first direct observation of a neuron with sodium and calcium channels of apparently normal kinetics where the calcium component alone can propagate in the absence of an outward current blocker. Our results suggest that there is a greater density of calcium channels on the CC axon than on the axons of other neurons.