Differential Contributions of Shaker and Shab K+ Currents to Neuronal Firing Patterns in Drosophila

Different K+ currents participate in generating neuronal firing patterns. The Drosophila embryonic “giant” neuron culture system has facilitated current- and voltage-clamp recordings to correlate distinct excitability patterns with the underlying K+ currents and to delineate the mutational effects of identified K+ channels. Mutations of Sh and Shab K+ channels removed part of inactivating IA and sustained IK, respectively, and the remaining IA and IK revealed the properties of their counterparts, e.g., Shal and Shaw channels. Neuronal subsets displaying the delayed, tonic, adaptive, and damping spike patterns were characterized by different profiles of K+ current voltage dependence and kinetics and by differential mutational effects. Shab channels regulated membrane repolarization and repetitive firing over hundreds of milliseconds, and Shab neurons showed a gradual decline in repolarization during current injection and their spike activities became limited to high-frequency, damping firing. In contrast, Sh channels acted on events within tens of milliseconds, and Sh mutations broadened spikes and reduced firing rates without eliminating any categories of firing patterns. However, removing both Sh and Shal IA by 4-aminopyridine converted the delayed to damping firing pattern, demonstrating their actions in regulating spike initiation. Specific blockade of Shab IK by quinidine mimicked the Shab phenotypes and converted tonic firing to a damping pattern. These conversions suggest a hierarchy of complexity in K+ current interactions underlying different firing patterns. Different lineage-defined neuronal subsets, identifiable by employing the GAL4-UAS system, displayed different profiles of spike properties and K+ current compositions, providing opportunities for mutational analysis in functionally specialized neurons.