Phenotypic plasticity in Periplaneta americana photoreceptors

Abstract

Plasticity is a crucial aspect of neuronal physiology essential for proper development and continuous functional optimization of neurons and neural circuits. Despite extensive studies of different visual systems, little is known about plasticity in mature microvillar photoreceptors. Here we investigate changes in electrophysiological properties and gene expression in photoreceptors of the adult cockroach, after exposure to constant light (CL) or constant dark (CD) for several months. After CL, we observed a decrease in mean whole-cell capacitance, a proxy for cell membrane area, from 362 ± 160 to 157 ± 58 pF, and a decrease in absolute sensitivity. However, after CD, we observed an increase in capacitance to 561 ± 155 pF and an increase in absolute sensitivity. Small changes in the expression of light-sensitive channels and signaling molecules were detected in CD retinas, together with a substantial increase in the expression of the primary green-sensitive opsin (GO1). Accordingly, light-induced currents became larger in CD photoreceptors. Even though normal levels of GO1 expression were retained in CL photoreceptors, light-induced currents became much smaller, suggesting that factors other than opsin are involved. Latency of phototransduction also decreased significantly in CL photoreceptors. Sustained voltage-activated K conductance was not significantly different between the experimental groups. The reduced capacitance of CL photoreceptors expanded their bandwidth, increasing the light-driven voltage signal at high frequencies. However, voltage noise was also amplified, probably because of unaltered expression of TRPL channels. Consequently, information transfer rates were lower in CL than in control or CD photoreceptors. These changes in whole-cell capacitance and electrophysiological parameters suggest that structural modifications can occur in the photoreceptors to adapt their function to altered environmental conditions. The opposing patterns of modifications in CL and CD photoreceptors differ profoundly from previous findings in photoreceptors.

Suppression of Gq and PLC gene expression has a small effect on quantum bumps in vivo in Periplaneta americana

“…6h, i). Although decreased quantum efficiency is consistent with our findings of the relatively low absolute sensitivities in both knockdowns, and also with the previous findings in D. melanogaster (Hardie et al 2002), this effect cannot be separated from the loss of absolute sensitivity associated with what we consider the non-specific changes in the photoreceptor, especially with the reduced C m [the relations between absolute sensitivity and C m are discussed at length in Frolov et al (2018)]. These presumably compensatory changes are similar to those documented previously in other cockroach retinal protein knockdown experiments Saari et al 2017).…”

Changes in electrophysiological properties of photoreceptors in Periplaneta americana associated with the loss of screening pigment

“…3a). Comparable decrease in Cm was also seen when wild-type cockroaches were exposed to constant light (Frolov et al 2018).…”

“…We measured the resting potential, membrane capacitance Cm, absolute sensitivity, and quantum bump properties. Previously, some of these parameters were shown to change when the cockroaches were reared in constant light or dark (Frolov et al 2018). These measurements were performed using patch-clamp on dark-adapted photoreceptors.…”

“…In the present study, we hypothesized that when the white-eyed cockroaches are reared in normal lighting conditions (12 hour light: 12 hour dark) the absence of screening pigment exposes their retinae to a stronger illumination than in wild type cockroaches. This could lead to comparable changes in photoreceptor properties to those found after constant light exposure (Frolov et al 2018). We tested this hypothesis using patch-clamp recordings from photoreceptors in dissociated ommatidia and in vivo intracellular recordings.…”

“…Recently, using patch-clamp experiments, we found that the whole-cell capacitance (a proxy for cell membrane area), absolute sensitivity to light, and light-induced current (LIC) amplitudes decreased strongly in P. americana photoreceptors when the animals were kept in constant light for several months, but constant dark exposure lead to an increase in the same parameters (Frolov et al 2018). These changes suggest adaptive structural modifications in the rhabdom and are different to previous findings in D. melanogaster.…”