Patch-clamp recordings were made from isolated and intact retinal ganglion cells (RGCs) of the ferret to examine the calcium-activated potassium channels expressed by these neurons and to determine their functional role in the generation of spikes and spiking patterns. Single- channel recordings from isolated neurons revealed the presence of two calcium-sensitive potassium channels that had conductances of 118 and 22 pS. The properties of these two channels were shown to be similar to those ascribed to the large-conductance calcium-activated potassium channel (BK(Ca)) and small-conductance calcium-activated potassium channel (SK(Ca)) channels in other neurons. Whole cell recordings from isolated RGCs showed that apamin and charybdotoxin (CTX), specific blockers of the SK(Ca) and BK(Ca) channels, respectively, resulted in a shortening of the time to threshold and a reduction in the hyperpolarization after the spike. Addition of these blockers also resulted in a significant increase in spike frequency over a wide range of maintained depolarizations. Similar effects of apamin and CTX were observed during current-clamp recordings from intact alpha and beta ganglion cells, morphologically identified after Lucifer yellow filling. About 20% of these neurons did not exhibit a sensitivity to either blocker, suggesting the presence of functionally distinct subgroups of alpha and beta RGCs on the basis of their intrinsic membrane properties. The expression of these calcium-activated potassium channels in the majority of alpha and beta cells provides a means by which the activity of these output neurons could be modulated by retinal neurochemicals.
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