Light adaptation in Drosophila photoreceptors: II. Rising temperature increases the bandwidth of reliable signaling

It is known that an increase in both the mean light intensity and temperature can speed up photoreceptor signals, but it is not known whether a simultaneous increase of these physical factors enhances information capacity or leads to coding errors. We studied the voltage responses of light-adapted Drosophila photoreceptors in vivo from 15 to 30 degrees C, and found that an increase in temperature accelerated both the phototransduction cascade and photoreceptor membrane dynamics, broadening the bandwidth of reliable signaling with an effective Q(10) for information capacity of 6.5. The increased fidelity and reliability of the voltage responses was a result of four factors: (1) an increased rate of elementary response, i.e., quantum bump production; (2) a temperature-dependent acceleration of the early phototransduction reactions causing a quicker and narrower dispersion of bump latencies; (3) a relatively temperature-insensitive light-adapted bump waveform; and (4) a decrease in the time constant of the light-adapted photoreceptor membrane, whose filtering matched the dynamic properties of the phototransduction noise. Because faster neural processing allows faster behavioral responses, this improved performance of Drosophila photoreceptors suggests that a suitably high body temperature offers significant advantages in visual performance.     

Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25 degrees C

Besides the physical limits imposed on photon absorption, the coprocessing of visual information by the phototransduction cascade and photoreceptor membrane determines the fidelity of photoreceptor signaling. We investigated the response dynamics and signaling efficiency of Drosophila photoreceptors to natural-like fluctuating light contrast stimulation and intracellular current injection when the cells were adapted over a 4-log unit light intensity range at 25 degrees C. This dual stimulation allowed us to characterize how an increase in the mean light intensity causes the phototransduction cascade and photoreceptor membrane to produce larger, faster and increasingly accurate voltage responses to a given contrast. Using signal and noise analysis, this appears to be associated with an increased summation of smaller and faster elementary responses (i.e., bumps), whose latency distribution stays relatively unchanged at different mean light intensity levels. As the phototransduction cascade increases, the size and speed of the signals (light current) at higher adapting backgrounds and, in conjunction with the photoreceptor membrane, reduces the light-induced voltage noise, and the photoreceptor signal-to-noise ratio improves and extends to a higher bandwidth. Because the voltage responses to light contrasts are much slower than those evoked by current injection, the photoreceptor membrane does not limit the speed of the phototransduction cascade, but it does filter the associated high frequency noise. The photoreceptor information capacity increases with light adaptation and starts to saturate at approximately 200 bits/s as the speed of the chemical reactions inside a fixed number of transduction units, possibly microvilli, is approaching its maximum.     

Mutation of cGMP phosphodiesterase 6alpha'-subunit gene causes progressive degeneration of cone photoreceptors in zebrafish

In mammals, the blockade of the phototransduction cascade causes loss of vision and, in some cases, degeneration of photoreceptors. However, the molecular mechanisms that link phototransduction with photoreceptor degeneration remain to be elucidated. Here, we report that a mutation in the gene encoding a central effector of the phototransduction cascade, cGMP phosphodiesterase 6alpha'-subunit (PDE6alpha'), affects not only the vision but also the survival of cone photoreceptors in zebrafish. We isolated a zebrafish mutant, called eclipse (els), which shows no visual behavior such as optokinetic response (OKR). The cloning of the els mutant gene revealed that a missense mutation occurred in the pde6alpha' gene, resulting in a change in a conserved amino acid. The PDE6 expressed in rod photoreceptors is a heterotetramer comprising two closely related similar hydrolytic alpha and beta subunits and two identical inhibitory gamma subunits, while the PDE6 expressed in cone photoreceptors consists of two homodimers of alpha' subunits, each with gamma subunits. The els mutant displays no visual response to bright light, where cones are active, but shows relatively normal OKR to dim light, where only rods function, suggesting that only the cone-specific phototransduction pathway is disrupted in the els mutant. Furthermore, in the els mutant, cones are selectively eliminated but rods are retained at the adult stage, suggesting that cones undergo a progressive degeneration in the els mutant retinas. Taken together, these data suggest that PDE6alpha' activity is important for the survival of cones in zebrafish.     

Sex-specific visual performance: female lizards outperform males in motion detection

In animal communication, complex displays usually have multiple functions and, male and female receivers often differ in their utilization and response to different aspects of these displays. The perceptual variability hypothesis suggests that different aspects of complex signals differ in their ability to be detected and processed by different receivers. Here, we tested whether receiver male and female Sceloporus graciosus lizards differ in visual motion detection by measuring the latency to the visual grasp response to a motion stimulus. We demonstrate that in lizards that largely exhibit complex motions as courtship signals, female lizards are faster than males at visually detecting motion. These results highlight that differential signal utilization by the sexes may be driven by variability in the capacity to detect different display properties.     

Fast and slow photoreceptors — a comparative study of the functional diversity of coding and conductances in the Diptera

1. From a comparison of the photoresponses and membrane properties of photoreceptors from 20 species of Diptera, we conclude that coding in the time domain is matched to the dictates of visual ecology. This matching involves the dynamics of phototransduction and the use of an appropriate mix of potassium conductances to tune the photoreceptor membrane.
2. Rapidly flying, manoeuvrable diurnal Diptera from several families have fast photoreceptors, with corner frequencies (the frequency at which signal power falls by a half) of between 50 and 107 Hz. The ponderous and predominantly nocturnal tipulids have slow photoreceptors with fully light adapted corner frequencies of 16 to 19 Hz.
3. Dark adapted fast photoreceptors have a lower gain (as indicated by lower noise levels), a lower sensitivity, and light adapt more rapidly than dark adapted slow photoreceptors. Fast cells also have much lower input resistances and shorter time constants.
4. Fast photoreceptors rectify more strongly in the steady state because of a weakly inactivating delayed rectifier potassium conductance with fast and slow components of activation. Slow photoreceptors rectify less strongly in the steady state because their membrane properties are dominated by strongly inactivating outward currents with reversal potentials in the range — 80 to -90 mV.
5. The differences between potassium conductances match the differing functional requirements of fast and slow photoreceptors. The non-inactivating delayed rectifier promotes the rapid response of fast cells by reducing the membrane time constant. This is an expensive strategy, involving large conductances and currents. Slowly flying nocturnal insects do not require a high speed of response. The potassium conductances in their slow photoreceptors inactivate to avoid costly and unnecessary ion fluxes.
6. Both the dynamics of the photoresponse and photoreceptor membrane properties exhibit sexual dimorphism. Light adapted photoreceptors in the enlarged male dorsal eye of Bibio markii have a corner frequency of 42 Hz, compared with 27 Hz for cells in the smaller female eye. This difference in frequency response correlates with the male's higher spatial acuity and is accompanied by consistent differences in potassium conductance activation rate. We conclude that the divison between fast and slow cells is the product of cellular constraints, metabolic costs and the requirements of coding efficiency at different light levels and retinal image velocities.

     

Photoreceptor processing speed and input resistance changes during light adaptation correlate with spectral class in the bumblebee, Bombus impatiens

Colour vision depends on comparison of signals from photoreceptors with different spectral sensitivities. However, response properties of photoreceptor cells may differ in ways other than spectral tuning. In insects, for example, broadband photoreceptors, with a major sensitivity peak in the green region of the spectrum (>500 nm), drive fast visual processes, which are largely blind to chromatic signals from more narrowly-tuned photoreceptors with peak sensitivities in the blue and UV regions of the spectrum. In addition, electrophysiological properties of the photoreceptor membrane may result in differences in response dynamics of photoreceptors of similar spectral class between species, and different spectral classes within a species. We used intracellular electrophysiological techniques to investigate response dynamics of the three spectral classes of photoreceptor underlying trichromatic colour vision in the bumblebee, Bombus impatiens, and we compare these with previously published data from a related species, Bombus terrestris. In both species, we found significantly faster responses in green, compared with blue- or UV-sensitive photoreceptors, although all 3 photoreceptor types are slower in B. impatiens than in B. terrestris. Integration times for light-adapted B. impatiens photoreceptors (estimated from impulse response half-width) were 11.3 ± 1.6 ms for green photoreceptors compared with 18.6 ± 4.4 ms and 15.6 ± 4.4 for blue and UV, respectively. We also measured photoreceptor input resistance in dark- and light-adapted conditions. All photoreceptors showed a decrease in input resistance during light adaptation, but this decrease was considerably larger (declining to about 22% of the dark value) in green photoreceptors, compared to blue and UV (41% and 49%, respectively). Our results suggest that the conductances associated with light adaptation are largest in green photoreceptors, contributing to their greater temporal processing speed. We suggest that the faster temporal processing of green photoreceptors is related to their role in driving fast achromatic visual processes.     

The 9-methyl group of retinal is essential for rapid Meta II decay and phototransduction quenching in red cones

Cone photoreceptors of the vertebrate retina terminate their response to light much faster than rod photoreceptors. However, the molecular mechanisms underlying this rapid response termination in cones are poorly understood. The experiments presented here tested two related hypotheses: first, that the rapid decay rate of metarhodopsin (Meta) II in red-sensitive cones depends on interactions between the 9-methyl group of retinal and the opsin part of the pigment molecule, and second, that rapid Meta II decay is critical for rapid recovery from saturation of red-sensitive cones after exposure to bright light. Microspectrophotometric measurements of pigment photolysis, microfluorometric measurements of retinol production, and single-cell electrophysiological recordings of flash responses of salamander cones were performed to test these hypotheses. In all cases, cones were bleached and their visual pigment was regenerated with either 11-cis retinal or with 11-cis 9-demethyl retinal, an analogue of retinal lacking the 9-methyl group. Meta II decay was four to five times slower and subsequent retinol production was three to four times slower in red-sensitive cones lacking the 9-methyl group of retinal. This was accompanied by a significant slowing of the recovery from saturation in cones lacking the 9-methyl group after exposure to bright (>0.1% visual pigment photoactivated) but not dim light. A mathematical model of the turn-off process of phototransduction revealed that the slower recovery of photoresponse can be explained by slower Meta decay of 9-demethyl visual pigment. These results demonstrate that the 9-methyl group of retinal is required for steric chromophore–opsin interactions that favor both the rapid decay of Meta II and the rapid response recovery after exposure to bright light in red-sensitive cones.     

An Unexpected Diversity of Photoreceptor Classes in the Longfin Squid,Doryteuthis pealeii

Cephalopods are famous for their ability to change color and pattern rapidly for signaling and camouflage. They have keen eyes and remarkable vision, made possible by photoreceptors in their retinas. External to the eyes, photoreceptors also exist in parolfactory vesicles and some light organs, where they function using a rhodopsin protein that is identical to that expressed in the retina. Furthermore, dermal chromatophore organs contain rhodopsin and other components of phototransduction (including retinochrome, a photoisomerase first found in the retina), suggesting that they are photoreceptive. In this study, we used a modified whole-mount immunohistochemical technique to explore rhodopsin and retinochrome expression in a number of tissues and organs in the longfin squid, Doryteuthis pealeii. We found that fin central muscles, hair cells (epithelial primary sensory neurons), arm axial ganglia, and sucker peduncle nerves all express rhodopsin and retinochrome proteins. Our findings indicate that these animals possess an unexpected diversity of extraocular photoreceptors and suggest that extraocular photoreception using visual opsins and visual phototransduction machinery is far more widespread throughout cephalopod tissues than previously recognized.     

Luring houseflies (Musca domestica) to traps: do cuticular hydrocarbons and visual cues increase catch?

Abstract.  Houseflies ( Musca domestica L.) are a major pest species of livestock units and landfill sites. Insecticide resistance has resulted in an increased emphasis on lure-and-kill control methods, but the success of this approach relies on the effective attraction of houseflies with olfactory or visual stimuli. This study examined the efficacy of olfactory (cuticular hydrocarbons) or visual (colours and groups of flies) attractants in a commercial poultry unit. Despite simulating the cuticular hydrocarbon profiles of male and female houseflies, we found no significant increase in the number of individuals lured to traps and no sex-specific responses were evident. The use of target colours selected to match the three peaks in housefly visual spectral sensitivity yielded no significant increase in the catch rate of traps to which they were applied. This study also demonstrated that male and female flies possess significantly different spectral reflectance (males are brighter at 320–470 nm; females are brighter at 470–670 nm). An experiment incorporating groups of recently killed flies from which cuticular hydrocarbons were either removed by solvent or left intact also failed to show any evidence of olfactory or visual attraction for houseflies of either sex. This study concluded that variations of the most commonly applied methods of luring houseflies to traps in commercial livestock units fail to significantly increase capture rates. These results support commonly observed inconsistencies associated with using olfactory or visual stimuli in lure-and-kill systems, possibly because field conditions lessen the attractant properties observed in laboratory experiments.     

Visual coding in locust photoreceptors

Information capture by photoreceptors ultimately limits the quality of visual processing in the brain. Using conventional sharp microelectrodes, we studied how locust photoreceptors encode random (white-noise, WN) and naturalistic (1/f stimuli, NS) light patterns in vivo and how this coding changes with mean illumination and ambient temperature. We also examined the role of their plasma membrane in shaping voltage responses. We found that brightening or warming increase and accelerate voltage responses, but reduce noise, enabling photoreceptors to encode more information. For WN stimuli, this was accompanied by broadening of the linear frequency range. On the contrary, with NS the signaling took place within a constant bandwidth, possibly revealing a 'preference' for inputs with 1/f statistics. The faster signaling was caused by acceleration of the elementary phototransduction current--leading to bumps--and their distribution. The membrane linearly translated phototransduction currents into voltage responses without limiting the throughput of these messages. As the bumps reflected fast changes in membrane resistance, the data suggest that their shape is predominantly driven by fast changes in the light-gated conductance. On the other hand, the slower bump latency distribution is likely to represent slower enzymatic intracellular reactions. Furthermore, the Q(10)s of bump duration and latency distribution depended on light intensity. Altogether, this study suggests that biochemical constraints imposed upon signaling change continuously as locust photoreceptors adapt to environmental light and temperature conditions.     

雄蝇追逐行为的分析

本文报告了在自由飞行条件下雄蝇追逐的行为实验及其分析的初步结果.其结果如下:1.追逐雄蝇水平方向偏转的角速度dF_1线性地依赖于目标蝇水平方位误差角T_1的大小.当目标在前视场中,即空间误差角|G|<π/4时,线性回归直线的斜率约为37**;而当空间误差角|G|>π/4时,线性回归直线的斜率约为6.7.2.追逐雄蝇俯仰方向偏转角速度dF_2在(-(π/2),π/2)的范围内线性依赖于俯仰误差角T_2的大小,其回归直线的斜率约为14.3.雄蝇追逐行为中,水平方位误差角频数分布的直方图呈现为峰值在零点的对称型分布;而俯仰误差角T_2频数分布的直方图是非对称型的,即仰角出现的频数大大超过俯角出现的频数.4.雄蝇主要利用了两蝇间距离变化dD的信息以及目标误差角来控制向前飞行的速度V.当误差角小时(即目标在前视场中),dD一般为负值,说明两蝇间的距离减小,而雄蝇追逐飞行的加速度A却与dD呈现正的线性关系.当误差角大时(即目标位于后视场中),dD一般为正值,说明两蝇间的距离增加.     

Rod and cone photoreceptors: molecular basis of the difference in their physiology

Vertebrate retinal photoreceptors consist of two types of cells, the rods and cones. Rods are highly light-sensitive but their flash response time course is slow, so that they can detect a single photon in the dark but are not good at detecting an object moving quickly. Cones are less light-sensitive and their flash response time course is fast, so that cones mediate daylight vision and are more suitable to detect a moving object than rods. The phototransduction mechanism was virtually known by the mid 80s, and detailed mechanisms of the generation of a light response are now understood in a highly quantitative manner at the molecular level. However, most of these studies were performed in rods, but not in cones. Therefore, the mechanisms of low light-sensitivity or fast flash response time course in cones have not been known. The major reason for this slow progress in the study of cone phototransduction was due to the inability of getting a large quantity of purified cones to study them biochemically. We succeeded in its purification using carp retina, and have shown that each step responsible for generation of a light response is less effective in cones and that the reactions responsible for termination of a light response are faster in cones. Based on these findings, we speculated a possible mechanism of evolution of rods that diverged from cones.     

Host sex and parasite genetic diversity

Is the genetic diversity of parasites infecting male and female hosts equal or different? This is the question we address in this paper by studying the neutral genetic variability of the plathyhelminth trematode Schistosoma mansoni within males and females of its natural murine host Rattus rattus in the marshy forest focus of Guadeloupe (French West Indies). Using seven microsatellite markers, we demonstrate that parasites from male hosts are genetically more diversified than parasites from female hosts. Three hypotheses are discussed that could explain this pattern: 1) a host sex-specific duration of cercariae recruitment; 2) a difference in the behaviour of male and female hosts that would lead to the exposure of males to a greater diversity of parasites; and 3) a host sex-biased immunocompetence that would lead to the selection of more genetically diversified individuals in male than in female rats. This finding is the first empirical evidence that each host sex may play different roles in the maintenance of parasite genetic diversity and so in their evolutionary dynamics and epidemiology.     

Sex-specific mediation of foraging in the shore crab, Carcinus maenas

Experiments were conducted to investigate the sex-specific differences to feeding responses of the shore crab Carcinus maenas throughout the year. Results demonstrate that female shore crabs exhibit stronger feeding responses than males throughout the year with a significantly reduced feeding response in males during the summer months' reproductive season. We also studied the possible function(s) of the moulting hormone, 20-hydroxyecdysone (Crustecdysone) that has been described as a potential female-produced sex pheromone to initiate male reproductive behaviour in a number of crustaceans. We recently presented evidence that for shore crabs this is not the case and now show that the steroid is instead functioning as a sex-specific feeding deterrent protecting the moulting 'soft' female crabs. Whilst male shore crabs were deterred from prey (Mytilus edulis) and synthetic feeding stimulants glycine and taurine when these feeding stimulants were spiked with crustecdysone, intermoult female crabs were significantly less affected and rarely deterred from feeding. This sex specificity of the moulting hormone, in combination with the female sex pheromone, which has no anti-feeding properties, ensures that male crabs mate with soft-shelled, moulted females rather than engage in cannibalism, such as found frequently in cases when soft-shelled females are exposed to intermoult females.     

The Effect of Timing of Female Vibrational Reply on Male Signalling and Searching Behaviour in the Leafhopper Aphrodes makarovi

Sexual communication in animals often involves duetting characterized by a coordinated reciprocal exchange of acoustic signals. We used playback experiments to study the role of timing of a female reply in the species-specific duet structure in the leafhopper Aphrodes makarovi (Hemiptera: Cicadellidae). In leafhoppers, mate recognition and location is mediated exclusively by species- and sex-specific substrate-borne vibrational signals and a female signal emitted in reply to male advertisement calls is essential for recognition and successful location of the female. In A. makarovi, males have to initiate each exchange of vibrational signals between partners, and in a duet the beginning of a female reply overlaps the end of the male advertisement call. Results of playback treatments in which female replies were delayed and did not overlap with the male call revealed that in order to trigger an appropriate behavioural response of the male, female reply has to appear in a period less than 400 ms after the end of the initiating male call. Results also suggest that males are not able to detect a female reply while calling, since female reply that did not continue after the end of male call triggered male behaviour similar to behaviour observed in the absence of female reply. Together, our results show that vibrational duets are tightly coordinated and that the species-specific duet structure plays an important role in mate recognition in location processes.     

Signal amplification: let's turn down the lights

G protein activation by membrane-bound receptors initiates a chain reaction that amplifies cellular responses to external signals. In retinal photoreceptors, amplification by the phototransduction cascade is regulated by quickly switching off the visual pigment that acts as the receptor for light.     

Membrane filtering properties of the bumblebee (Bombus terrestris) photoreceptors across three spectral classes

Filtering properties of the membrane form an integral part of the mechanisms producing the light-induced electrical signal in insect photoreceptors. Insect photoreceptors vary in response speed between different species, but recently it has also been shown that different spectral photoreceptor classes within a species possess diverse response characteristics. However, it has not been quantified what roles phototransduction and membrane properties play in such diversity. Here, we use electrophysiological methods in combination with system analysis to study whether the membrane properties could create the variation of the response speed found in the bumblebee (Bombus terrestris) photoreceptors. We recorded intracellular responses from each photoreceptor class to white noise-modulated current stimuli and defined their input resistance and linear filtering properties. We found that green sensitive cells exhibit smaller input resistance and membrane impedance than other cell classes. Since green sensitive cells are the fastest photoreceptor class in the bumblebee retina, our results suggest that the membrane filtering properties are correlated with the speed of light responses across the spectral classes. In general, our results provide a compelling example of filtering at the sensory cell level where the biophysical properties of the membrane are matched to the performance requirements set by visual ecology.     

Sex-specific, counteracting responses to inbreeding in a bird

Inbreeding often depresses offspring fitness. Because females invest more than males in a reproductive event, inbreeding is expected to be more costly to mothers than fathers, creating a divergence between the reproductive interests of each sex and promoting sex-specific inbreeding strategies. Males and females may bias the probability of inbreeding by selecting copulation partners, and, in sexually promiscuous species, through male strategic sperm investment in different females and female selection of the sperm of different males. However, these processes are often difficult to study, and the way that different male and female strategies interact to determine inbreeding remains poorly understood. Here we demonstrate sex-specific, counteracting responses to inbreeding in the promiscuous red junglefowl, Gallus gallus. First, a male was just as likely to copulate with his full-sib sister as with an unrelated female. In addition, males displayed a tendency to: (i) initiate copulation faster when exposed to an unrelated female than when exposed to a sister, and (ii) inseminate more sperm into sisters than into unrelated females. Second, females retained fewer sperm following insemination by brothers, thus reducing the risk of inbreeding and counteracting male inbreeding strategies.     

Recoverin improves rod-mediated vision by enhancing signal transmission in the mouse retina

Vision in dim light requires that photons absorbed by rod photoreceptors evoke signals that reliably propagate through the retina. We investigated how a perturbation in rod physiology affects propagation of those signals in the retina and ultimately visual sensitivity. Recoverin is a protein in rods that prolongs phototransduction and enhances visual sensitivity. It is not present in neurons postsynaptic to rods, yet we found that light-evoked responses of rod bipolar and ganglion cells were shortened when measured in recoverin-deficient retinas. Unexpectedly, the effect of recoverin on postsynaptic signals could not be explained by its effect on phototransduction. Instead, it is an effect of recoverin downstream of phototransduction in rods that prolongs signal transmission and enhances visual sensitivity. An important implication of our findings is that the recovery phase of the rod photoresponse does not contribute significantly to visual sensitivity near absolute threshold.     

Metarhodopsin control by arrestin,light-filtering screening pigments,and visual pigment turnover in invertebrate microvillar photoreceptors

The visual pigments of most invertebrate photoreceptors have two thermostable photo-interconvertible states, the ground state rhodopsin and photo-activated metarhodopsin, which triggers the phototransduction cascade until it binds arrestin. The ratio of the two states in photoequilibrium is determined by their absorbance spectra and the effective spectral distribution of illumination. Calculations indicate that metarhodopsin levels in fly photoreceptors are maintained below ~35% in normal diurnal environments, due to the combination of a blue-green rhodopsin, an orange-absorbing metarhodopsin and red transparent screening pigments. Slow metarhodopsin degradation and rhodopsin regeneration processes further subserve visual pigment maintenance. In most insect eyes, where the majority of photoreceptors have green-absorbing rhodopsins and blue-absorbing metarhodopsins, natural illuminants are predicted to create metarhodopsin levels greater than 60% at high intensities. However, fast metarhodopsin decay and rhodopsin regeneration also play an important role in controlling metarhodopsin in green receptors, resulting in a high rhodopsin content at low light intensities and a reduced overall visual pigment content in bright light. A simple model for the visual pigment–arrestin cycle is used to illustrate the dependence of the visual pigment population states on light intensity, arrestin levels and pigment turnover.