The occurrence and ionic basis of prolonged plateau depolarizations were studied during intracellular recordings obtained from thirty-nine supraoptic nucleus (s.o.n.) neurosecretory neurones in perfused explants of rat hypothalamus. Replacement of Ca2+ by Ba2+ in the perfusion media enhanced the shoulder on the repolarization phase of the action potentials in all of eleven cells tested. In Ba2+, spike durations increased as the holding membrane potential was made more positive, resulting in plateaux lasting up to 100 s. These plateaux were characterized by a sustained but slowly decaying absolute potential near 0 mV from which there appeared frequent spontaneous hyperpolarizing transients. A membrane resistance decrease of more than 50% was observed at the onset of a plateau, with gradual restoration during the plateau. Injection of Cs+ into twenty-one cells abolished the spike frequency adaptation and after-hyperpolarization associated with current-evoked bursts of action potentials. Mean spike duration after Cs+ injection increased from 2.5 +/- 0.3 ms to 68 +/- 9 ms (S.E. of mean). Addition of 4-5 mM-tetraethylammonium (TEA) to the perfusion media further increased the spike duration of nine Cs+-injected cells to 320 +/- 70 ms. No further increase could be obtained by doubling the concentration of TEA and/or by the addition of 0.2-0.5 mM-4-aminopyridine to the media. Although spike duration was greatly prolonged during such extensive blockade of K+ channels, plateau potentials lasting for longer than 1 s were observed only when Ba2+ was eventually added to the perfusion media. The special property of Ba2+ that leads to the formation of plateau potentials in s.o.n. neurones is therefore not restricted to its ability to reduce K+ conductances but may reside in its reduced effectiveness as a mediator of Ca2+-dependent inactivation of Ca2+ channels. Injection of Cs+ into s.o.n. neurones increased the slope of their current-voltage relationship below -60 mV from 148 +/- 15 to 257 +/- 41 M omega (S.E. of mean) and eliminated the outward rectification present at potentials above -60 mV. K+ currents are presumably active near the resting potential of these cells. Addition of Ba2+ to the perfusion media revealed a Cd2+-sensitive inward rectification above but not below ca. -55 mV. A slowly inactivating Ba2+ current is therefore carried through Ca2+ channels at potentials above -55 mV.(ABSTRACT TRUNCATED AT 400 WORDS)