The excitability level of pyramidal neurons in the basolateral amygdala (BLA) is greatly increased following muscarinic receptor activation, an effect associated with an increased rate of action potential firing and reduction of the afterhyperpolarization (AHP). We impaled BLA pyramidal neurons in slices of rat ventral forebrain with a single microelectrode to examine the currents underlying the AHP and spike frequency accommodation and determine their sensitivities to muscarinic modulation. In voltage-clamp, depolarizing steps were followed by biphasic outward tail currents, consisting of rapidly decaying (IFast) and slowly decaying (ISlow) current components. These corresponded temporally with the medium and slow portions of the AHP, respectively. The reversal potential for the IFast component of the AHP tail current shifted in the depolarizing direction with increases in the extracellular K+ concentration. The amplitude of IFast was reduced during perfusion of 0-Ca2+ medium or by superfusion of TEA (1-5 mM) or carbachol (10-40 microM). It is suggested that IFast was produced by the rapidly decaying Ca(2+)-activated K+ current (IC) and the muscarinic-sensitive M-current (IM). The ISlow tail current component reversed at the estimated values for EK in medium containing either normal or elevated K+ levels. This component was eliminated by perfusion of 0-Ca2+ medium or inclusion of cyclic-AMP in the recording electrode. It was not blocked by TEA (5 mM) or apamin (50-500 nM), but was reduced by carbachol in a dose-dependent manner (IC50 = 0.5 microM). Electrical stimulation of cholinergic afferent pathways to the BLA produced inhibition of ISlow, an effect which was enhanced by eserine and prevented by atropine. Loss of the ISlow component was always accompanied by similar reductions in accommodation and the slow AHP. It was concluded that this tail current component resulted from the slowly decaying Ca(2+)-activated K+ current, IAHP. Thus, the muscarinic inhibition of IAHP contributes to the enhanced excitability exhibited by BLA pyramidal neurons following cholinergic stimulation.