Whole cell patch and cell-attached recordings were obtained from neurons in intact ganglia of the myenteric plexus of the guinea pig duodenum. Two classes of neuron were identified electrophysiologically: phasically firing AH neurons that had a pronounced slow afterhyperpolarization (AHP) and tonically firing S neurons that lacked a slow AHP. We investigated the properties of the slow AHP and the underlying current ( I AHP) to address the roles of Ca2+ entry and Ca2+ release in the AHP and the characteristics of the K+channels that are activated. AH neurons had a resting potential of −54 mV and the AHP, which followed a volley of three suprathreshold depolarizing current pulses delivered at 50 Hz through the pipette, averaged 11 mV at its peak, which occurred 0.5–1 s following the stimulus. The duration of these AHPs averaged 7 s. Under voltage-clamp conditions, I AHP's were recorded at holding potentials of −50 to −65 mV, following brief depolarization of AH neurons (20–100 ms) to positive potentials (+35 to +50 mV). The null potential of the I AHP at its peak was −89 mV. The AHP and I AHP were largely blocked by ω-conotoxin GVIA (0.6–1 μM). Both events were markedly decreased by caffeine (2–5 mM) and by ryanodine (10–20 μM) added to the bathing solution. Pharmacological suppression of the I AHP with TEA (20 mM) or charybdotoxin (50–100 nM) unmasked an early transient inward current at −55 mV following step depolarization that reversed at −34 mV and was inhibited by niflumic acid (50–100 μM). Mean-variance analysis performed on the decay of the I AHPrevealed that the AHP K+ channels have a mean chord conductance of ∼10 pS, and there are ∼4,000 per AH neuron. Spectral analysis showed that the AHP channels have a mean open dwell time of 2.8 ms. Cell-attached patch recordings from AH neurons confirmed that the channels that open following action currents have a small unitary conductance (10–17 pS) and open with a high probability (≤0.5) within the first 2 s following an action potential. These results indicate that the AHP is largely a consequence of Ca2+ entry through ω-conotoxin GVIA-sensitive Ca2+ channels during the action potential, Ca2+-triggered Ca2+ release from caffeine-sensitive stores and the opening of Ca2+-sensitive small-conductance K+ channels.