On the role of transient depolarization-activated K+ current in microvillar photoreceptors

Abstract

Photoreceptors in the compound eyes of most insect species express two functional types of depolarization-activated potassium currents: a transient A-type current (IA) and a sustained delayed rectifier current (IDR). The role of Shaker-dependent IA in Drosophila melanogaster photoreceptors was previously investigated by comparing intracellular recordings from Shaker and wild-type photoreceptors. Shaker channels were proposed to be involved in low-frequency signal amplification in dim light and reduction of the metabolic cost of information transfer. Here, I study the function of IA in photoreceptors of the cockroach Panchlora nivea using the patch-clamp method. Responses to Gaussian white-noise stimuli reveal that blockade of IA with 4-aminopyridine has no discernible effect on voltage responses or information processing. However, because open-channel blockers are often ineffective at low membrane potentials, no conclusion on the role of IA could be made on the basis of negative results of pharmacological tests. Using a relatively large set of control data, a physiological variability analysis was performed to discern the role of IA. Amplitudes of the IA window current and half-activation potentials correlate strongly with membrane corner frequencies, especially in dim light, indicating that IA facilitates transmission of higher frequencies. Consistent with voltage-dependent inactivation of IA, these correlations decrease with depolarization in brighter backgrounds. In contrast, correlations involving IDR are comparatively weak. Upon reexamining photoreceptor conductance in wild-type and Shaker strains of D. melanogaster, I find a biphasic voltage dependence near the resting potential in a minority of photoreceptors from both strains, indicating that Shaker channels are not crucial for early amplification of voltage signals in D. melanogaster photoreceptors. Leak current in Shaker photoreceptors at the level of the soma is not elevated. These results suggest a novel role for IA in facilitating transmission of high-frequency signals in microvillar photoreceptors.