Distinct Frequency-Dependent Regulation of Nerve Terminal Excitability and Synaptic Transmission by IA and IK Potassium Channels Revealed by Drosophila Shaker and Shab Mutations

Abstract

Regulation of synaptic efficacy by nerve terminal excitability has not been extensively studied. We performed genetic and pharmacological dissections for presynaptic actions of K+ channels in Drosophila neuromuscular transmission by using electrophysiological and optical imaging techniques. Current understanding of the roles of the Shab IK channel and its mammalian Kv2 counterparts is relatively poor, as compared with that for Shaker IA channels and their Kv1 homologues. Our results revealed the striking effect of Shab mutations during high-frequency synaptic activity, as well as a functional division in synaptic regulation between the Shaker and Shab channels. Shaker channels control the basal level of release, indicated by a response to single nerve stimulation, whereas Shab channels regulate repetitive synaptic activities. These observations highlight the crucial control of nerve terminal excitability by Shaker and Shab channels to confer temporal patterns of synaptic transmission and suggest the potential participation of these channels, along with the transmitter release machinery, in activity-dependent synaptic plasticity.