Screening Pigment Migration Research Articles

Photoreceptors and diurnal variation in spectral sensitivity in the fiddler crab Gelasimus dampieri.

Colour signals, and the ability to detect them, are important for many animals and can be vital to their survival and fitness. Fiddler crabs use colour information to detect and recognise conspecifics, but their colour vision capabilities remain unclear. Many studies have attempted to measure their spectral sensitivity and identify contributing retinular cells, but the existing evidence is inconclusive. We used electroretinogram (ERG) measurements and intracellular recordings from retinular cells to estimate the spectral sensitivity of Gelasimus dampieri and to track diurnal changes in spectral sensitivity. G. dampieri has a broad spectral sensitivity and is most sensitive to wavelengths between 420 and 460 nm. Selective adaptation experiments uncovered an ultraviolet (UV) retinular cell with a peak sensitivity shorter than 360 nm. The species' spectral sensitivity above 400 nm is too broad to be fitted by a single visual pigment and using optical modelling, we provide evidence that at least two medium-wavelength sensitive (MWS) visual pigments are contained within a second blue-green sensitive retinular cell. We also found a ∼25 nm diurnal shift in spectral sensitivity towards longer wavelengths in the evening in both ERG and intracellular recordings. Whether the shift is caused by screening pigment migration or changes in opsin expression remains unclear, but the observation shows the diel dynamism of colour vision in this species. Together, these findings support the notion that G. dampieri possesses the minimum requirement for colour vision, with UV and blue/green receptors, and help to explain some of the inconsistent results of previous research.

Red-shift of spectral sensitivity due to screening pigment migration in the eyes of a moth, Adoxophyes orana

BackgroundWe have found that the spectral sensitivity of the compound eye in the summer fruit tortrix moth (Adoxophyes orana) differs in laboratory strains originating from different regions of Japan. We have investigated the mechanisms underlying this anomalous spectral sensitivity.MethodsWe applied electrophysiology, light and electron microscopy, opsin gene cloning, mathematical modeling, and behavioral analysis.ResultsThe ERG-determined spectral sensitivity of dark-adapted individuals of all strains peaks around 520 nm. When light-adapted, the spectral sensitivity of the Nagano strain narrows and its peak shifts to 580 nm, while that in other strains remains unchanged. All tested strains appear to be identical in terms of the basic structure of the eye, the pigment migration in response to light- and dark-adaptation, and the molecular structure of long-wavelength absorbing visual pigments. However, the color of the perirhabdomal pigment clearly differs; it is orange in the Nagano strain and purple in the others. The action spectrum of phototaxis appears to be shifted towards longer wavelengths in the Nagano individuals.ConclusionsThe spectral sensitivities of light-adapted eyes can be modeled under the assumption that this screening pigment plays a crucial role in determining the spectral sensitivity. The action spectrum of phototaxis indicates that the change in the eye spectral sensitivity is behaviorally relevant.

Circadian rhythms affect electroretinogram, compound eye color, striking behavior and locomotion of the praying mantis Hierodula patellifera.

Many behaviors and physiological processes oscillate with circadian rhythms that are synchronized to environmental cues (e.g. light onset), but persist with periods of ~24 h in the absence of such cues. We used a multilevel experimental approach to assess whether circadian rhythms modulate several aspects of the visual physiology and behavior of the praying mantis Hierodula patellifera. We used electroretinograms (ERGs) to assess compound eye sensitivity, colorimetric photographic analyses to assess compound eye color changes (screening pigment migration), behavioral assays of responsiveness to computer-generated prey-like visual stimuli and analyses of locomotor activity patterns on a modified treadmill apparatus. Our results indicate that circadian clocks control and/or modulate each of the target behaviors. Strong rhythms, persisting under constant conditions, with periods of ~24 h were evident in photoreceptor sensitivity to light, appetitive responsiveness to prey-like stimuli and gross locomotor activity. In the first two cases, responsiveness was highest during the subjective night and lowest during the subjective day. Locomotor activity was strongly clustered around the transition time from day to night. In addition, pigment migration and locomotor behavior responded strongly to light:dark cycles and anticipated the light-dark transition, suggesting that the circadian clocks modulating both were entrained to environmental light cues. Together, these data indicate that circadian rhythms operate at the cellular, cellular systems and organismal level in H. patellifera. Our results represent an intriguing first step in uncovering the complexities of circadian rhythms in the Mantodea.

Eye development in southern calamary, Sepioteuthis australis, embryos and hatchlings

Eye development, optical properties and photomechanical responses were examined in embryos and hatchlings of the southern calamary, Sepioteuthis australis. This species occurs in shallow coastal waters in Australia and New Zealand, and the egg masses were collected in October and December 2004 from Great Oyster Bay, Tasmania. At the earliest developmental stage the eye of the squid was comprised of a hemispherical cup of undifferentiated neural retina, while presumptive iris cell layers and lentigenic precursor cells enclosed a posterior eye chamber. Differentiation of the proximal and distal processes was observed in correspondence with the cornea development and lens crystallization, and occurred before differentiation of the neural retina, which was complete prior to hatching. Longer photoreceptor distal processes were first observed just prior to hatching in the dorsal-posterior retina. After hatching, this difference was much more evident and higher photoreceptor density was found in the central retina. This indicates that the eye of S. australis at this age uses different retina areas for different visual tasks. Optical sensitivity and resolution suggest that juvenile S. australis are diurnal. This study also found functional photomechanical responses of visual screening pigment migration and pupil constriction in S. australis embryos, although complete functionality of the pupil at this stage was uncertain. However, the pupils of squid aged 2 days closed almost completely under bright conditions, showing that photomechanical responses were highly developed in the juvenile squid. These findings indicate that squid embryos are able to perceive visual stimulation, suggesting an early reliance on vision for survival after hatching.

Light-regulated translocation of signaling proteins in Drosophila photoreceptors

Illumination of Drosophila photoreceptor cells induces multi-facet responses, which include generation of the photoreceptor potential, screening pigment migration and translocation of signaling proteins which is the focus of recent extensive research. Translocation of three signaling molecules is covered in this review: (1) Light-dependent translocation of arrestin from the cytosol to the signaling membrane, the rhabdomere, determines the lifetime of activated rhodopsin. Arrestin translocates in PIP 3 and NINAC myosin III dependent manner, and specific mutations which disrupt the interaction between arrestin and PIP 3 or NINAC also impair the light-dependant translocation of arrestin and the termination of the response to light. (2) Activation of Drosophila visual G protein, DGq, causes a massive and reversible, translocation of the α subunit from the signaling membrane to the cytosol, accompanied by activity-dependent architectural changes. Analysis of the translocation and the recovery kinetics of DGq α in wild-type flies and specific visual mutants indicated that DGq α is necessary but not sufficient for the architectural changes. (3) The TRP-like (TRPL) but not TRP channels translocate in a light-dependent manner between the rhabdomere and the cell body. As a physiological consequence of this light-dependent modulation of the TRP/TRPL ratio, the photoreceptors of dark-adapted flies operate at a wider dynamic range, which allows the photoreceptors enriched with TRPL to function better in darkness and dim background illumination. Altogether, signal-dependent movement of signaling proteins plays a major role in the maintenance and function of photoreceptor cells.

Role of FMRFamide in the reproduction of Octopus vulgaris: molecular analysis and effect on visual input

As a part of continuous research on the neurobiology of the cephalopods in general, and the neuroendocrine control of reproduction in Octopus vulgaris in particular, the presence, the molecular analysis and the effect of FMRFamide on the screening-pigment migration in the visual system have been analysed. FMRFamide immunoreactive fibres are present in the outer plexiform layer of the retina as well as in the plexiform zone of the deep retina. These fibres presumably come from optic and olfactory lobes. We isolated an incomplete Octopus FMRFamide cDNA which encodes an amino terminal truncated precursor containing several FMRFamide-related peptides (FaRPs) showing a high degree of identity with the FaRPs encoded in the precursor of Sepia officinalis, except for the presence of an Rpamide related peptide, present only in cnidarians. Finally, stimulation of isolated retina demonstrated that the effect of this tetrapeptide, coupled with dopamine, is the induction of an extreme adaptation of the retina to the light condition. This situation de facto inhibits sexual maturation. Our results on the effect of FMRFamide on the retina confirm the suggested hypothesis that this peptide plays an inhibitory role on the activity of optic gland.

Neurotransmitter regulation of circadian structural changes in the fly's visual system.

The visual system of the fly's compound eye undergoes a number of cyclical day/night changes that have a circadian basis. Such responses are seen in the synaptic terminals of the photoreceptors and in their large monopolar-cell interneurons in the first optic neuropile, or lamina. These changes include, in the photoreceptor terminals, rhythms in the numbers of synapses and the vertical migration of screening pigment; and, in the monopolar cells L1 and L2, a rhythm in the transients of the electroretinogram and in the cyclical swelling of L1 and L2 lamina axons, as well as of the epithelial glia that surround these. Some of these changes are seen in both the housefly and the fruit fly, but the time-course of such changes differs between the two species. Many of the changes are influenced by the injection of various transmitter candidates, in a direction that can be reconciled with the possibility of normal endogenous release of two substances, 5HT from the neurites of 5HT-immunoreactive neurons, and pigment dispersing factor peptide from the neurites of PDH cells. Consistent with this interpretation, the immunoreactive varicosities of PDH cells exhibit size changes attributable to their cyclical release of peptide, or to its cyclical synthesis and/or transport from the PDH cell somata. Thus, neurotransmitter substances not only have rapid electrophysiological actions in the optic lobe, but also longer-lasting, presumably indirect, neuromodulatory actions, which are manifest as structural changes among the lamina's neurons and synapses. These actions involve an interplay between aminergic and peptidergic systems, but the exact role and especially the site of action of each has still to be elucidated.

Properties of pupil mechanisms in owl-fly Ascalaphus macaronius (Neuroptera)

Regulation of light flux by pupil mechanisms in the UV-sensitive superposition eye of owl-fly Ascalaphus macaronius (Neuroptera) was studied with a fast reflection microspectrophotometric technique. The spectral sensitivity of pupil reaction, which was calculated on the basis of changes of transient amplitude reflection, was almost identical with the one of Deilephila eye. This indicates that in spite of different life styles and spectral sensitivities of photoreceptors, pupil closing is triggered by the same photosensitive structure in both eyes. By measuring the spectra of reflected light from the Ascalaphus eye between 400 and 700 nm after different dark periods following light stimulation, it was established that the restoration of reflection was much faster in the red than in the blue spectral range. Based on this, we propose that two different pupil mechanisms with different spectral absorption characteristics are involved in light-flux regulation. Fast-reacting pupil is probably represented by screening pigment migration in the secondary pigment cells and a slow blue-absorbing system by the activity in primary pigment cells. The importance of two different pupils for the photoregeneration of visual pigment is discussed.

Neurotransmitters alter the numbers of synapses and organelles in photoreceptor terminals in the lamina of the housefly, Musca domestica.

Various organelles in the lamina terminals of housefly photoreceptors exhibit daily rhythms having a circadian basis. These include changes in the numbers of photoreceptor tetrad and L2 feedback synapses, and longitudinal movements of screening pigment. Circadian information has previously been suggested to spread from the clock to the lamina via widefield cells expressing either 5-hydroxytryptamine or pigment-dispersing hormone-like immunoreactivity. We examined the action of these neuromodulators, and other candidate neurotransmitters, 4 h after injecting either the transmitter or a control into the medulla. We counted electron microscope profiles of organelles that normally exhibit circadian changes, and two types of invagination into photoreceptor terminals, capitate projections and inter-receptor invaginations. No single substance mediated the changes observed. Injected pigment-dispersing hormone peptide decreased the number of pigment granules, implicating this peptide in screening pigment migration, but produced no changes in synapse-related organelles. alpha-Aminobutyric acid exclusively decreased the number of L2 feedback synapses. Responses to other transmitters were specific, and often large, but generally not statistically significant. Histamine, for example, may decrease the number of tetrads, possibly by direct autoregulation. The results suggest that there is likely to be more than one effector in the circadian pathways to the lamina.

The visual ecology of pupillary action in superposition eyes

The two most common mechanisms of pupillary screening-pigment migration in arthropod superposition eyes are the cone and longitudinal pigment migration mechanisms. The dynamics of each were investigated by optical modelling and by determining experimentally the relationship between eye glow brightness and screening pigment position within the eyes of two representative insect species: the noctuid moth Agrotis infusa and the dung beetle Copris elphenor. During dark adaptation, in both mechanisms, the screening pigment is contracted distally to expose the proximal half of each crystalline cone. During light adaptation the pigment migrates proximally and reduces light flux in the retina. In the longitudinal mechanism, pigment migrates into the clear zone of the eye. In the cone mechanism, pigment never enters the clear zone and is instead restricted to the proximal half of each crystalline cone: a migrating sleeve of pigment creates a small aperture at the end of the crystalline cone, the area of which depends on the degree of light adaptation. According to the model, the cone mechanism provides a limited range of light attenuation (ca. 0.6 log units) for which both good spatial resolution and accuracy of control are maintained, and within this range attenuation is controlled very finely. Beyond this range, whilst attenuation is still possible, diffraction at the pigment aperture and increasing coarseness of control worsen visual performance significantly. In contrast, the longitudinal mechanism provides a much larger useful range of light attenuation (up to several log units) and maintains reasonable fineness of attenuation control over the entire range (although not as fine as the cone mechanism). The experimental results support the model. An extensive survey of arthropods with superposition eyes reveals that the cone mechanism is almost exclusively possessed by those animals experiencing a narrow range of light intensities, and the longitudinal mechanism by those experiencing a wide range.

Screening-Pigment Migration in the Octopus Retina Includes Control by Dopaminergic Efferents

ABSTRACT The extent of screening-pigment (SP) migration in the intact octopus retina and the amplitude of the early receptor potential (ERP) correspond with the degree of adaptation to light or darkness. The light-adapted retina has SP granules concentrated in an apical layer, at the tips of the photoreceptor rhabdoms and supporting cells, and the ERP is barely detectable. In the fully dark-adapted retina, the SP granules are mostly at the base of the rhabdoms, and the ERP is at its maximum. Retinae at intermediate stages, between the fully dark-and light-adapted states, show corresponding intermediate stages of SP migration and ERP amplitude. A series of experiments demonstrates the effects on SP migration of the efferent nerves, which form a subset of fibres in the optic nerves. When the optic nerves to one half of the retina have been severed, there is a dramatic difference in the distribution of SP in areas of the retina (of the dark-adapted eye) connected with severed or intact nerves: apical versus basal, respectively. On incubation of a light-adapted retina with 5 μmol l−1 dopamine, but not with other catecholamines or other putative neurotransmitter substances, SP migrates basally and the ERP is significantly larger than for controls. In octopuses treated with reserpine, SP stays in an apical location and the ERP remains very small, regardless of the state of adaptation and of whether the optic nerves are intact. It is concluded that dopaminergic efferents from the optic lobes effect dark-adaptational SP migration in the cephalopod retina. The arrival in the retina of efferent signals that effect adaptational changes through the mediation of dopamine is a remarkable analogue of the vertebrate system.

Ethanol-induced extension of screening-pigment migration range in crayfish photoreceptors

1. Ethanol 5–10% extends the normal range of screening-pigment migration along the photoreceptors of crayfish compound eyes, the effect being accounted for by a supramaximal pigment aggregation in the dark. 2. Excised eyes incubated in the presence of ethanol showed a faster and enhanced pigment aggregation to the dark-Actapted position, whereas the kinetics of the reverse movement in response to illumination was little affected. Methanol and propanol also facilitated pigment aggregation, although not with the same effectiveness as ethanol at equivalent concentrations. 3. The ethanol-induced facilitation of pigment aggregation persisted for some time after thorough washing of the eyes, and counteracted the inhibition of dark-Actaptation normally caused by an increaScin temperature. 4. Two possible explanations for this peculiar effect of ethanol are discussed: (a) alterations in photoreceptor membrane permeability that, in turn, may affect the ionic mechanisms controlling pigment position; and (b) promotion of local release of neurotransmitters involved in the modulation of light/dark adaptation.

Screening pigment, aperture and sensitivity in the dung beetle superposition eye

Sensitivity to light was investigated in the refracting superposition eye of the dung beetle Onitis alexis using electrophysiological measurements and optical modelling. Intracellular recordings were made from single retinula cells over 24-h periods, with cells light and dark adapted, in order to measure the response/intensity (V-LogI) functions. The combined effects of a circadian rhythm and light adaptation allow the determination of the relative contributions of screening-pigment migration and transduction gain to changes in sensitivity in the eye. Between the extremes of dark adaptation at night and light adaptation during the day, the maximum sensitivity change possible is at least 4 log units, of which approximately 2 log units can be accounted for by changes in the transduction gain and at least 2 log units by screening-pigment migration. The role of the superposition aperture (the number of facets that contribute light to one rhabdom) in 3 species of dung beetle was investigated with an optical ray-tracing model of the eye. The facets of the superposition aperture do not contribute light equally to the target rhabdom; except in one species, the greatest contribution comes from facets located away from both the centre and periphery of the aperture. Light adaptation increases the optical density of the superposition aperture and decreases its size.

Requirements for screening pigment migration in the eye of Ephestia kuehniella Z.

The influence of colchicine, cytochalasin B, calcium concentration, ouabain, 2,4-dinitrophenol, epinephrine, octopamine, and low temperature on the migration of pigment granules induced by light or darkness in the superposition eye of Ephestia kuehniella was investigated using the size of the eye glow to indicate the position of the granules. Colchicine, low extracellular calcium concentration, 2,4-dinitrophenol, and low temperature inhibit the aggregation of the granules in the secondary pigment cells from the dispersed state, and cause aggregated granules to disperse in darkness. Cytochalasin B inhibits aggregation from the dispersed state, but does not induce dispersal. Ouabain and high extracellular calcium concentration cause a light-induced inhibition of aggregation. The neurotransmitters, epinephrine and octopamine, have no effects on granule position. Dispersion is inhibited only by cytochalasin B. The requirements for aggregation and dispersion are discussed.

A remote sensing method for the estimation of light-trap efficiency

AbstractA description is given of the use of a video camera to estimate light-trap efficiency in the field. This camera relies on the extra light sensitivity provided by the Newvicon detector tube to enable insect track discrimination. Recorded insect flight tracks were classified into three distinct categories, new arrivals, passers by and local flights, the numbers of which were compared to the moth catch in a Robinson mercury vapour light-trap. Calculations of efficiency were made using two methods, the best-estimate efficiency, obtained by comparing the new-arrival tracks to the light-trap catch, and the worst-estimate efficiency, obtained by comparing new-arrival tracks plus passer-by tracks to the light-trap catch. Preliminary results indicate that efficiency varies with windspeed but with a maximum of 39%, obtained in virtually calm conditions, suggesting that some aspect of moth behaviour limits trapping efficiency. It is suggested that the speed of migration of screening pigment from the dark-adapted state to the light-adapted state in superposition eyes may have a bearing on the catching mechanism of a light-trap.

Screening pigment migration in a sphingid moth is triggered by light near the cornea

It is possible to project a horizontal line of light onto a moth's cornea and simultaneously a vertical line onto the retina (Fig. 1). In the dark adapted eye of a sphingid moth (Theretra latreilli) this resulted in the appearance of a horizontal line of pigment across the eye (Fig. 2). This proves that the trigger for pigment migration is near the cornea, presumably in the pigment cells themselves, and not in the receptors.

The Effect of Screening Pigment Migration on Spectral Sensitivity in a Crayfish Reflecting Superposition Eye

ABSTRACT In crayfish, there is some evidence that visual pigments in the eye affect the spectral sensitivity, both at the receptor level (Goldsmith & Fernandez, 1968; Kong & Goldsmith, 1977) and in the optic fibres (Woodcock & Goldsmith, 1970). However, there is a discrepancy between the absorption spectrum of rhodopsin as measured by microspectrophotometry (λmax is 530–550 nm, Goldsmith, 1978) and published measurements of spectral sensitivity [e.g. electroretinogram (ERG) peaks of 565–570 nm (Kennedy & Bruno, 1961) and intracellular recordings of 556 nm and 600–620 nm (Nosaki, 1969) and 538–634 nm (Waterman & Fernandez, 1970)]. Woodcock & Goldsmith (1970) suggested that sensitivity maxima in the orange and red were due to the non-alignment of the stimulating beam with the optical axis of the cell, thereby allowing light to filter obliquely through red and brown proximal screening pigment surrounding the rhabdom. Goldsmith (1978) showed (theoretically) that the red-brown proximal screening pigments of crayfish and lobster are indeed capable of shifting the effective absorption of the rhabdoms enough to account for the discrepancy between the absorption peak of the visual pigment and the published measurements of spectral sensitivity. However, the effect on spectral sensitivity of the migration of the proximal screening pigment has not been documented.

Ultra-violet and blue induced migration of screening pigment in the retina of the mothDeilephila elpenor

1. The present study concerns the migration of the screening pigment in the compound eye of the mothDeilephila elpenor and its relation to the activity of the visual cells. Movements of the screening pigment were determined by microphotometric measurement, and the electroretinogram (ERG) was used as an index of retinal activity. 2. A light stimulus caused a reflectance change that proceeded in three phases: an initial increase in reflectance, followed by a decrease and a final slow increase. The amplitude of the decrease, i.e. of the pigment dispersion, was found to be determined by the total number of light quanta incident on the eye. The reflectance decrease could be approximated by a first order photochemical reaction with a maximal summation time of at least 80 s. 3. The spectral efficiency of the reflectance change between 338 and 530 nm differed from the spectral efficiency of the dark adapted retina recorded electrophysiologically, but was similar to the efficiency recorded during selective light adaptation of the green sensitive visual cells. Highest sensitivity was recorded in response to UV stimuli. Correspondingly, there was no distinct correlation between the amplitude of the ERG and the amplitude of the simultaneously recorded decrease in reflectance after UV, blue-violet or green light. The green stimulus elicited the largest ERG response but the smallest pigment dispersion. These results indicate that the contribution of the green sensitive visual cells to the pigment dispersion is small. 4. The screening pigment was observed by transmission microscopy in preparations consisting of only the screening pigment cells, dioptric structures, and small visual cell rests kept in a depolarizing, high extracellular potassium concentration. UV and blue-violet light stimuli induced pigment dispersion similar to that observed in intact eyes. The result suggests that photosensitive pigment(s) are located in some element outside the visual cells, but does not preclude that the visual cells participate in the normal regulation of pigment dispersion.

Do retinula cells trigger the screening pigment migration in the eye of the mothEphestia kuehniella?

Simultaneous recordings of reflectance and the electroretinogram (ERG) of the meal moth superposition eye show a good match between the action spectrum of screening pigment migration and the spectral sensitivity curve (Fig. 5). These spectra correspond with the absorption spectrum of a xanthopsin X530 that has been evidenced in the eye. No correlation was found with the extinction spectrum of the pigment granules themselves (Fig. 7). The results suggest, that the photomechanical reaction is controlled by the visual pigment.

Refractive index gradients subserve optical isolation in a light‐adapted reflecting superposition eye

AbstractThe freshwater shrimp Macrobrachium rosenbergii (de Man) has reflecting superposition compound eyes. Upon adaptation from dark to light conditions, the eye converts from superposition to apposition optics by screening pigment migration. The clear zone, typical of dark‐adapted superposition eyes, persisted after adaptation to 500 lux, when the eye optically behaved like an apposition eye. In this state, optical isolation is maintained by a proximal refractive‐index gradient in the crystalline cone, which only requires the proximal pigment to be in the light‐adapted position around the junction between the cone and rhabdom. Thus, the distal pigment need not invade the clear zone for the eye to convert to apposition optics. This mechanism probably decreases the time required for light adaptation. Furthermore, as a result of total internal reflections in the cone tip, the proximal gradient increases the acceptance angle.