In the cilia of amphibian olfactory receptor neurons, odorants elicit a receptor current that has two components: a cationic current through cAMP-gated channels and a Cl- current. Here, a cascade of ciliary currents that accounts for the total receptor current is demonstrated. In isolated olfactory cilia, cAMP sequentially activates two currents. The first is a primary cationic current through channels directly gated by cAMP. Part of this current is carried by Ca2+, which in turn activates a Cl- current. This secondary current is eliminated by the presence of Cl- channel inhibitors, replacement of Cl- with methanesulfonate-, removal of external Ca2+, or blockers of the cAMP-gated cationic channels. When cytoplasmic Ca2+ buffering is low, small cationic currents can activate Cl- currents that are 20 times larger.