TEA‐ and apamin‐resistant K Ca channels in guinea‐pig myenteric neurons: slow AHP channels

The patch‐clamp technique was used to record from intact ganglia of the guinea‐pig duodenum in order to characterize the K + channels that underlie the slow afterhyperpolarization (slow AHP) of myenteric neurons. Cell‐attached patch recordings from slow AHP‐generating (AH) neurons revealed an increased open probability ( P o ) of TEA‐resistant K + channels following action potentials. The P o increased from < 0.06 before action potentials to 0.33 in the 2 s following action potential firing. The ensemble averaged current had a similar time course to the current underlying the slow AHP. TEA‐ and apamin‐resistant Ca 2+ ‐activated K + (K Ca ) channels were present in inside‐out patches excised from AH neurons. The P o of these channels increased from < 0.03 to approximately 0.5 upon increasing cytoplasmic [Ca 2+ ] from < 10 n m to either 500 n m or 10 μ m . P o was insensitive to changes in transpatch potential. The unitary conductance of these TEA‐ and apamin‐resistant K Ca channels measured approximately 60 pS under symmetric K + concentrations between −60 mV and +60 mV, but decreased outside this range. Under asymmetrical [K + ], the open channel current showed outward rectification and had a limiting slope conductance of about 40 pS. Activation of the TEA‐ and apamin‐resistant K Ca channels by internal Ca 2+ in excised patches was not reversed by washing out the Ca 2+ ‐containing solution and replacing it with nominally Ca 2+ ‐free physiological solution. Kinetic analysis of the single channel recordings of the TEA‐ and apamin‐resistant K Ca channels was consistent with their having a single open state of about 2 ms (open dwell time distribution was fitted with a single exponential) and at least two closed states (two exponential functions were required to adequately fit the closed dwell time distribution). The Ca 2+ dependence of the activation of TEA‐ and apamin‐resistant K Ca channels resides in the long‐lived closed state which decreased from > 100 ms in the absence of Ca 2+ to about 7 ms in the presence of submicromolar cytoplasmic Ca 2+ . The Ca 2+ ‐insensitive closed dwell time had a time constant of about 1 ms. We propose that these small‐to‐intermediate conductance TEA‐ and apamin‐resistant Ca 2+ ‐activated K + channels are the channels that are primarily responsible for the slow AHP in myenteric AH neurons.