Non-inactivating voltage-activated K+ conductances can increase photoreceptor signaling bandwidth beyond the bandwidth set by phototransduction

Abstract

Evolution produced a large variety of rhabdomeric photoreceptors in the compound eyes of insects. To study effects of morphological and electrophysiological differences on signal generation and modulation, we developed models of the cockroach and blow fly photoreceptors. The cockroach model included wide microvilli, large membrane capacitance and two voltage-activated K+ conductances. The blow fly model included narrow microvilli, small capacitance and two sustained voltage-activated K+ conductances. Our analysis indicated that membrane of even the narrowest microvilli of up to 3 μm long can be measured fully from the soma. Attenuation of microvillar quantum bump (QB)-like signals at the recording site in the soma increased with the signal amplitude in the microvillus, due to the decreasing driving force. However, conductance of the normal-sized QBs can be detected in the soma with minimal attenuation. Next, we investigated how interactions between the sustained voltage-activated K+ and light-induced conductances can shape the frequency response. The models were depolarized by either a current injection or light-induced current (LIC) and probed with inward currents kinetically approximating dark- or light-adapted QBs. By analyzing the resulting voltage impulse responses (IR), we found that: (1) sustained K+ conductance can shorten IRs, expanding the signaling bandwidth beyond that set by phototransduction; (2) voltage-dependencies of changes in IR durations have minima within the physiological voltage response range, depending on the activation kinetics of K+ conductance, the presence or absence of sustained LIC, and the kinetics of the probing current stimulus; and (3) sustained LIC lowers gain of IRs and can exert dissimilar effects on their durations. The first two findings were supported by experiments. It is argued that improvement of membrane response bandwidth by parametric interactions between passive, ligand-gated and voltage-dependent components of the membrane circuit can be a general feature of excitable cells that respond with graded voltage signals.