The firing of a train of action potentials in hippocampal pyramidal neurons is terminated by an afterhyperpolarization (AHP) that displays two main components; the medium AHP (I(mAHP)), lasting a few hundred milliseconds and the slow AHP (I(sAHP)), that has a duration of several seconds. It is unclear how much of I(mAHP) is dependent on the entry of calcium ions (Ca(2+)), whereas it is accepted that I(sAHP) is caused by activation of Ca(2+)-activated potassium channels. There has been controversy regarding the subcellular localization and mechanism of activation of these channels. Whole-cell recordings from CA1 neurons in the hippocampal slice preparation showed that inhibition of L-type, but not N-, P/Q-, T- and R-type Ca(2+) channels, reduced both I(mAHP) and I(sAHP). Inhibition of both AHP components by L-type Ca(2+) channel antagonists was not complete, with I(sAHP) being significantly more sensitive than I(mAHP). Somatic extracellular ionophoresis of BAPTA during I(sAHP) caused a transient inhibition, but had no effect on I(mAHP). Cell-attached patch recordings from the soma of CA1 neurons within a slice displayed channels that produced an ensemble waveform reminiscent of I(sAHP) when the patch was subjected to a train of action potential waveforms. The channels were Ca(2+)-activated, exhibited a limiting slope conductance of 19 pS and were not observed in dendritic membrane patches. These data demonstrate that the I(sAHP) is somatic in origin and arises from continued Ca(2+) entry through functionally co-localized L-type channels.