Elementary and macroscopic light-induced currents and their Ca2+-dependence in the photoreceptors of Periplaneta americana

Abstract

In a microvillar photoreceptor, absorption of an incident photon initiates a phototransduction reaction that generates a depolarizing light-induced current (LIC) in the microvillus. Although in-depth knowledge about these processes in photoreceptors of the fruitfly Drosophila is available, not much is known about their nature in other insect species. Here, we present description of some basic properties of both elementary and macroscopic LICs and their Ca2+-dependence in the photoreceptors of a dark-active species, the cockroach Periplaneta americana. Cockroach photoreceptors respond to single photon absorptions by generating quantum bumps with about 5-fold larger amplitudes than in Drosophila. At the macroscopic current level, cockroach photoreceptors responded to light with variable sensitivity and current waveform. This variability could be partially attributed to differences in whole-cell capacitance. Transient LICs, both elementary and macroscopic, showed only moderate dependence on extracellular Ca2+. However, with long light pulses, response inactivation was largely abolished and the overall size of LICs increased when extracellular Ca2+ was omitted. Finally, by determining relative ionic permeabilities from reversals of LICs, we demonstrate that when compared to Drosophila, cockroach light-gated channels are only moderately Ca2+-selective.

Large variation among photoreceptors as the basis of visual flexibility in the common backswimmer

“…Importantly, all these species have different visual ecologies: the stick insect Carausius morosus is strictly nocturnal, the water strider Gerris lacustris is strictly diurnal, and the American cockroach Periplaneta americana is active during twilight and night-time. All these species demonstrate strong positive correlations between absolute sensitivity and capacitance [28,31] (P. americana sensitivity and capacitance values were obtained from the dataset as published by Immonen et al [40]). In fact, this was found in all insect species where we addressed this issue, without exception.…”

Not flying blind: A comparative study of photoreceptor function in flying and non-flying cockroaches

“…Transducer noise has three components, which are variations in bump shape ('bump shape noise'), latency ('latency noise') and amplitude ('shot noise'). Statistical analysis of quantum bumps in the cockroach (Immonen et al, 2014b) implies that all three components of the transducer noise are mutually independent and intrinsically stochastic. Unlike the bump shape and latency noises, shot noise is largely inconsequential for information transfer by the membrane because the effect of differing amplitudes of individual bumps constituting an aggregated response to light will be cancelled out by averaging, except perhaps in very dim light when single bumps dominate the response.…”

“…However, unlike in Periplaneta, this variability depended neither on the photoreceptor size, nor on the sensitivity to light (Immonen et al, 2014b). Fig.…”

“…One way to investigate this is to compare electrophysiological properties of related species with overall similar lifestyles but different flying habits (Niven et al, 2007). We have previously characterized photoreceptors in the American cockroach Periplaneta americana (Blattidae) in detail (Heimonen et al, 2012(Heimonen et al, , 2006Immonen et al, 2014b). Periplaneta is able to fly but in laboratory conditions it flies rarely and only at high ambient temperatures.…”

Visual ecology and potassium conductances of insect photoreceptors

“…Part of the data presented in this study were obtained from previously published work on C. morosus , C. punctata (Frolov 2015), D. melanogaster (Krause et al 2008), G. lacustris , G. bimaculatus , N. glauca (Immonen et al 2014a), and P. americana (Immonen et al 2014b). Additional experiments were performed on P. xuthus, generously provided by Prof. Kentaro Arikawa (Sokendai, Hayama, Japan), G. integer, generously provided by Petri Niemelä (Munich, Germany), C. vicina, P. schultei, and G. portentosa, purchased from Blades Biological (Edenbridge, UK), and A. mellifera, E. lapponicus, and M. roeselii, which were caught locally in Oulu (Finland).…”