Single channel currents in internodes of demyelinated Xenopus axons were measured with the gigaseal patch-clamp technique. Demyelination induced by injected lysolecithin allows the entire internodal axolemma to be accessible to a patch electrode. Four classes of K+ channels in this region were characterized. A Ca(2+)-activated K+ channel [K(Ca)] with a single channel conductance of 235 pS was found. In the presence of 10(-3), 10(-4), 10(-5), and 10(-6) M intracellular free [Ca2+]i, the half-activation voltages are -24.1, -20.8, 30.2, and 111 mV, and the voltage sensitivities are 18.3, 17.2, 23.7, and 21 mV per e-fold change in open probability, respectively. The half-activation Ca2+ concentration at 40 mV is 10(-5) M and the Hill coefficient of Ca2+ binding is 1.7. The K(Ca) channels were sometimes found in clusters, three to six channels in a patch. A 125 pS ATP-sensitive K+ channel was inhibited by the internal application of 2 mM ATP. Its activation was voltage independent. This channel may be important in the regulation of resting potential. A background K+ channel exhibited outwardly rectifying unitary current (176 pS) in symmetrical 115 mM KCl solutions but the ensemble-averaged I-V curve was ohmic. The voltage dependence is very weak, 220 mV per e-fold change in open probability. The nearly symmetrical macroscopic I-V curve of the background channel suggests a role in maintaining the axonal resting potential. A 28 pS delayed- rectifier K+ channel is found to be blocked internally by 2 mM 4- aminopyridine and by 10 mM tetraethylammonium. The half-activation voltage is -41 mV and the voltage sensitivity is 8 mV per e-fold change in open probability.