We measured the current activated by cytoplasmic adenosine 3':5'-cyclic monophosphate (cAMP) in olfactory cilia from the frog Rana pipiens. The odorant-induced current in frog olfactory receptor neurons was also measured for comparison. In both cases, recordings were performed near the neuronal resting potential in a variety of extracellular bath solutions. 2. In Ca(2+)-free baths, cAMP activated an inward current in excised olfactory cilia that was carried entirely by cations. As extracellular Ca2+ was increased, the cationic current decreased while a second current, carried by C1-, increased. Total cAMP-activated current decreased with increasing extracellular CA2+. When external Na+ but not Ca2+ was eliminated, only the C1- component of the current persisted. When external Na+ and Ca2+ were both removed, there was no cAMP-activated current. 3. In receptor neurons, the total odorant-induced receptor current varied in a similar way with the extracellular ionic environment. Under conditions favoring the anionic receptor current, the response amplitude decreased and the latency increased. 4. It is known that olfactory receptor currents persist in a wide variety of extracellular environments. This persistence can be sufficiently explained by the balance between cationic and anionic currents demonstrated here.