Mode switching characterizes the activity of large conductance potassium channels recorded from rat cortical fused nerve terminals

1. Inside-out recordings from rat cortical fused nerve terminals indicate that the most common channel observed was a large conductance K⁺ (BK) channel with characteristics dissimilar to conventional cell body calcium-activated BK (BK_Ca) channels. 2. BK channels exhibit mode switching between low (mode 1) and high (mode 2) activity, an effect not influenced by membrane voltage. Increasing internal Ca²⁺ concentration increased time spent in mode 2 as did application of protein kinase A, an effect not mimicked by protein kinase C or protein kinase G. 3. Mode 1 activity was voltage independent although depolarization increased mode 2 channel activity. Global average channel activity was voltage and Ca²⁺ dependent. 4. Alkaline phosphatase treatment induced channel activity to reside permanently in mode 2, where activity was voltage and Ca²⁺ dependent but unaffected by protein kinases A, G or C. 5. Internal application of tetraethylammonium blocked BK channel activity in a manner identical to that reported for BK_Ca channels. 6. These results indicate that nerve terminal membranes have large conductance K+ channels with significant differences in gating kinetics and regulation of activity compared with BK_Ca channels of other neuronal preparations. The BK channel subtype may play a unique physiological role specific to the nerve terminal.