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

Immonen, Esa‐Ville; Krause, Stephan; Krause, Yani; Frolov, Roman V.; Vähäsöyrinki, Mikko; Weckström, Matti

doi:10.3389/fphys.2014.00153

Cited by 21 publications

(52 citation statements)

References 49 publications

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“…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.…”

Section: Discussionmentioning

confidence: 99%

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

et al. 2014

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The common backswimmer, Notonecta glauca, uses vision by day and night for functions such as underwater prey animal capture and flight in search of new habitats. Although previous studies have identified some of the physiological mechanisms facilitating such flexibility in the animal's vision, neither the biophysics of Notonecta photoreceptors nor possible cellular adaptations are known. Here, we studied Notonecta photoreceptors using patch-clamp and intracellular recording methods. Photoreceptor size (approximated by capacitance) was positively correlated with absolute sensitivity and acceptance angles. Information rate measurements indicated that large and more sensitive photoreceptors performed better than small ones. Our results suggest that backswimmers are adapted for vision in both dim and wellilluminated environments by having open-rhabdom eyes with large intrinsic variation in absolute sensitivity among photoreceptors, exceeding those found in purely diurnal or nocturnal species. Both electrophysiology and microscopic analysis of retinal structure suggest two retinal subsystems: the largest peripheral photoreceptors provide vision in dim light and the smaller peripheral and central photoreceptors function primarily in sunlight, with light-dependent pigment screening further contributing to adaptation in this system by dynamically recruiting photoreceptors with varying sensitivity into the operational pool.

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Section: Discussionmentioning

confidence: 99%

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

et al. 2014

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“…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.…”

Section: Discussionmentioning

confidence: 99%

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

Section: Elementary Responses To Lightmentioning

confidence: 99%

“…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.…”

Section: Introductionmentioning

confidence: 99%

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

Frolov

Matsushita

Arikawa

2017

Journal of Experimental Biology

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Flying is often associated with superior visual performance, as good vision is crucial for detection and implementation of rapid visually guided aerial movements. To understand the evolution of insect visual systems it is therefore important to compare phylogenetically related species with different investments in flight capability. Here, we describe and compare morphological and electrophysiological properties of photoreceptors from the habitually flying green cockroach Panchlora nivea and the American cockroach Periplaneta americana, which flies only at high ambient temperatures. In contrast to Periplaneta, ommatidia in Panchlora were characterized by two-tiered rhabdom, which might facilitate detection of polarized light while flying in the dark. In patch-clamp experiments, we assessed the absolute sensitivity to light, elementary and macroscopic light-activated current and voltage responses, voltage-activated potassium (K v ) conductances, and information transfer. Both species are nocturnal, and their photoreceptors were similarly sensitive to light. However, a number of important differences were found, including the presence in Panchlora of a prominent transient K v current and a generally low variability in photoreceptor properties. The maximal information rate in Panchlora was one-third higher than in Periplaneta, owing to a substantially higher gain and membrane corner frequency. The differences in performance could not be completely explained by dissimilarities in the light-activated or K v conductances; instead, we suggest that the superior performance of Panchlora photoreceptors mainly originates from better synchronization of elementary responses. These findings raise the issue of whether the evolutionary tuning of photoreceptor properties to visual demands proceeded differently in Blattodea than in Diptera.

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“…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).…”

Section: Electrophysiologymentioning

confidence: 99%

Visual ecology and potassium conductances of insect photoreceptors

Frolov

Immonen

Weckström

2016

Journal of Neurophysiology

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Frolov R, Immonen EV, Weckström M. Visual ecology and potassium conductances of insect photoreceptors. J Neurophysiol 115: 2147-2157, 2016. First published February 10, 2016 doi:10.1152/jn.00795.2015.-Voltage-activated potassium channels (Kv channels) in the microvillar photoreceptors of arthropods are responsible for repolarization and regulation of photoreceptor signaling bandwidth. On the basis of analyzing Kv channels in dipteran flies, it was suggested that diurnal, rapidly flying insects predominantly express sustained K ϩ conductances, whereas crepuscular and nocturnally active animals exhibit strongly inactivating Kv conductances. The latter was suggested to function for minimizing cellular energy consumption. In this study we further explore the evolutionary adaptations of the photoreceptor channelome to visual ecology and behavior by comparing K ϩ conductances in 15 phylogenetically diverse insects, using patch-clamp recordings from dissociated ommatidia. We show that rapid diurnal flyers such as the blowfly (Calliphora vicina) and the honeybee (Apis mellifera) express relatively large noninactivating Kv conductances, conforming to the earlier hypothesis in Diptera. Nocturnal and/or slow-moving species do not in general exhibit stronger Kv conductance inactivation in the physiological membrane voltage range, but the photoreceptors in species that are known to rely more on vision behaviorally had higher densities of sustained Kv conductances than photoreceptors of less visually guided species. No statistically significant trends related to visual performance could be identified for the rapidly inactivating Kv conductances. Counterintuitively, strong negative correlations were observed between photoreceptor capacitance and specific membrane conductance for both sustained and inactivating fractions of Kv conductance, suggesting insignificant evolutionary pressure to offset negative effects of high capacitance on membrane filtering with increased conductance. insect photoreceptor; potassium channels; compound eye; visual ecology

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

Cited by 21 publications

References 49 publications

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

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

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

Visual ecology and potassium conductances of insect photoreceptors

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