Opsin knockdown specifically slows phototransduction in broadband and UV-sensitive photoreceptors in Periplaneta americana

Frolov, Roman V.; Severina, I. Yu.; Novikova, E. S.; Ignatova, Irina I.; Liu, Hongxia; Zhukovskaya, M. I.; Torkkeli, Päivi H.; French, Andrew S.

doi:10.1007/s00359-022-01580-z

Cited by 5 publications

(6 citation statements)

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“…For example, the rhabdom of the crepuscular cockroach P . americana contains a large number of thick (~100 nm in diameter) microvilli [ 4 ]. In contrast, the rhabdom cross-section in the highly aerobatic diurnal muscoid fly Lucilia cuprina contains ~25 short and narrow (~40 nm in diameter) microvilli [ 24 ].…”

Section: Resultsmentioning

confidence: 99%

“…Cockroach photoreceptors vary strongly in their electrophysiological properties [ 11 ]. The cells are large compared to photoreceptors of other insects [ 2 ], with a median C m of 363 pF for broadband photoreceptors [ 4 ]. However, the peak of C m distribution is at 300 pF, and so the membrane area of the cockroach photoreceptor model was made to have a similar size.…”

Section: Resultsmentioning

confidence: 99%

“…The diameters, 40 and 100 nm, delimit the empirically determined range of microvillar diameter variability in species with rhabdomeric photoreceptors. For example, the rhabdom of the crepuscular cockroach P. americana contains a large number of thick (~100 nm in diameter) microvilli [4]. In contrast, the rhabdom cross-section in the highly aerobatic diurnal muscoid fly Lucilia cuprina contains ~25 short and narrow (~40 nm in diameter) microvilli [24].…”

Section: Visibility Of the Rhabdomeric Membrane From The Somamentioning

confidence: 99%

“…In the previous studies, we established dependencies of several electrophysiological properties and signal processing parameters on C m . Photoreceptor sensitivity to light correlates strongly positively with C m in P. americana [4,28,35], Panchlora nivea [37], Corixa punctata [38], Notonecta glauca [39], Gerris lacustris [9], and Carausius morosus [8], presumably because sensitivity of a given cell is proportional to the area of the light-sensitive rhabdomeric membrane, which is reflected in C m . For the same reason, LIC amplitude correlates positively with C m in C. morosus, G. lacustris, C. punctata and P. americana [8,9,35,38].…”

Section: Photoreceptor Size and Functional Parametersmentioning

confidence: 99%

“…For example, in the frontal-dorsal part of the compound eye of the hover fly Volucella pellucens , the microvillus diameter is ~40 nm and length ~1000 nm, with only about ten microvilli of similar length per cross-section of the rhabdomere [ 3 ]. In contrast, in the eye of the crepuscular American cockroach Periplaneta americana , the microvillus diameter is ~100 nm, its length varies from hundreds of nanometers to several micrometers, and the number per cross-section can exceed one hundred [ 2 , 4 ]. Microvilli of big diurnal flies appear to be irreducibly small for a standalone cellular compartment because the diameter of <40 nm accommodates ~7 nm of plasma membrane and a similar measure of the central filament.…”

Section: Introductionmentioning

confidence: 99%

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

Frolov

2023

PLoS ONE

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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.

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Section: Resultsmentioning

confidence: 99%