Photoreceptor Spectral Sensitivities Research Articles

The Visual Ecology of Avian Photoreceptors

The spectral sensitivities of avian retinal photoreceptors are examined with respect to microspectrophotometric measurements of single cells, spectrophotometric measurements of extracted or in vitro regenerated visual pigments, and molecular genetic analyses of visual pigment opsin protein sequences. Bird species from diverse orders are compared in relation to their evolution, their habitats and the multiplicity of visual tasks they must perform. Birds have five different types of visual pigment and seven different types of photoreceptor-rods, double (uneven twin) cones and four types of single cone. The spectral locations of the wavelengths of maximum absorbance (lambda(max)) of the different visual pigments, and the spectral transmittance characteristics of the intraocular spectral filters (cone oil droplets) that also determine photoreceptor spectral sensitivity, vary according to both habitat and phylogenetic relatedness. The primary influence on avian retinal design appears to be the range of wavelengths available for vision, regardless of whether that range is determined by the spectral distribution of the natural illumination or the spectral transmittance of the ocular media (cornea, aqueous humour, lens, vitreous humour). Nevertheless, other variations in spectral sensitivity exist that reflect the variability and complexity of avian visual ecology.

Optical and developmental constraints on colour vision with lens eyes

Longitudinal chromatic aberration (LCA) is present in all animal lens eyes and is a limiting factor for colour vision. It is discussed how natural evolution has dealt with the problem of chromatic defocus in ways entirely different from technical solutions. Adaptations to LCA are present in the spectral sensitivities of photoreceptors, the architecture of the retina, the lens and the shape of the pupil. These adaptations raise interesting questions in developmental and cell biology, as well as regarding the evolution of lens eyes and colour vision. It is suggested that LCA has been a limiting factor in the evolution of the human visual system.

Visual Ecology and Perception of Coloration Patterns by Domestic Chicks

This article suggests how we might understand the way potential predators see coloration patterns used in aposematism and visual mimicry. We start by briefly reviewing work on evolutionary function of eyes and neural mechanisms of vision. Often mechanisms used for achromatic vision are accurately modeled as adaptations for detection and recognition of the generality of optical stimuli, rather than specific stimuli such as biological signals. Colour vision is less well understood, but for photoreceptor spectral sensitivities of birds and hymenopterans there is no evidence for adaptations to species-specific stimuli, such as those of food or mates. Turning to experimental work, we investigate how achromatic and chromatic stimuli are used for object recognition by foraging domestic chicks (Gallus gallus). Chicks use chromatic and achromatic signals in different ways: discrimination of large targets uses (chromatic) colour differences, and chicks remember chromatic signals accurately. However, detection of small targets, and discrimination of visual textures requires achromatic contrast. The different roles of chromatic and achromatic information probably reflect their utility for object recognition in nature. Achromatic (intensity) variation exceeds chromatic variation, and hence is more informative about change in reflectance – for example, object borders, while chromatic signals yield more information about surface reflectance (object colour) under variable illumination.

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.

Tuning of Photoreceptor Spectral Sensitivities by Red and Yellow Pigments in the Butterfly Papilio xuthus

The compound eye of the Japanese yellow swallowtail butterfly, Papilio xuthus, consists of different types of ommatidia characterized by the pigmentation around the rhabdom. About 75% of the ommatidia harbor red pigment, whereas the other 25% contain yellow pigment. We find that the pigments function as spectral filters for the proximal photoreceptor cells. Intracellular recordings of the proximal cells yielded spectral sensitivities peaking in the red (λmax = 600 nm) and in the green (λmax = 520 nm), respectively. Staining of the recorded cells and subsequent histology demonstrated that the red receptors contain red pigment and that the green receptors contain yellow pigment. The sensitivity spectrum of the red receptors was considerably narrower compared to the absorption spectrum of a visual pigment peaking at 600 nm. The sensitivity spectrum can be calculated with an optical model for the butterfly rhabdom by incorporating measured absorbance spectra of the red pigments, yielding that the cell contains a visual pigment peaking at about 575 nm. The model also indicated that the spectral sensitivity of the green receptors is produced by the combination of the yellow lateral filter and a visual pigment peaking at 515 nm.

Photoreceptor spectral sensitivities: Common shape in the long-wavelength region

Previous measurements of mammalian photoreceptor spectral sensitivity have been analysed, with particular attention to the long-wavelength region. The measurements selected for study come from rod and cone systems, and from human, monkey, bovine and squirrel sources. For the spectra from photoreceptor electrophysiology and from psychophysical sensitivity, the frequency scaling applied by Mansfield (1985, The visual system, pp. 89–106. New York: Alan Liss) provides a common shape over a range of at least 7 log 10 units of sensitivity, from low frequencies (long wavelengths) to frequencies beyond the peak. The same curve is applicable to the absorbance spectrum of bovine rhodopsin, although the absorbance can only be measured down to about 2 log 10 units below the peak. At the longest wavelengths the results exhibit a common limiting slope of 70 log 10 units (or 30.4 log 10 units) per unit of normalized frequency. A simple equation is presented as a generic description for the α-band of mammalian photoreceptor spectral sensitivity curves, and it seem likely that the equation may be equally applicable to retina 1-based pigments in other species. Despite the lack of a theoretical basis, the equation has the correct asymptotic behaviour at long wavelengths, and it provides an accurate description of the peak. It also accounts accurately for the experimentally observed “yellowing” of long-wavelength lights that occurs beyond 700 nm.

Spectral sensitivities of photoreceptors and lamina monopolar cells in the dragonfly, Hemicordulia tau

Five spectral types of photoreceptors with peak sensitivities at 330 nm, 410 nm, 460 nm, 525 nm and 630 nm were recorded from the ventral eye of the dragonfly, Hemicordulia tau. Often the 525 nm photoreceptors presented broader, and the 630 nm photoreceptors narrower, spectral sensitivities than would be excepted of a photopigment with the same peak sensitivity. Four types of lamina monopolar cells (cell types 1–4) were recognised from their dark-adapted spectral sensitivities and their anatomy. The anatomical identification allows tentative assignation to the monopolar cell classification from Sympetrum rubicundulum obtained using Golgi staining (Meinertzhagen and Armett-Kibel 1982). When dark-adapted, the monopolar cells had peak spectral sensitivities that were similar to single photoreceptors or appeared to pool receptor outputs, but in some cases spectral sensitivity changed markedly upon adaptation to white and to chromatic light, in one case (cell type 2) apparently ‘switching off’ a UV-sensitive input.

Spectral sensitivity of single photoreceptors and color vision in the stingless bee, Melipona quadrifasciata

1. The spectral sensitivities of the photoreceptors in the compound eye of the stingless bee, Melipona quadrifasciata (Hymenoptera, Apoidea), was determined by the spectral scanning method. Three spectral receptor types were found with λmax at 356 nm, 424 nm, and 532 nm (Fig. 1). Intracellular markings confirmed one morphological type of green receptor (svf 1) and one type of UV receptor (1vf 1) whose axon morphology resembles that of the corresponding spectral receptor types in the honeybee, Apis mellifera (Fig. 2). 2. Training experiments with a large number of color signals were performed at the hive entrance and the feeding place under natural daylight conditions (Figs. 4–6). The tests were either dual (2 alternative color signals) choice tests or multiple (12 simultaneously presented alternative color signals) choice tests. Melipona discriminates colors very well in both behavioral contexts, but discrimination is generally better at the feeding place (Fig. 7). A comparison with Apis shows that Melipona discriminates colors in the bluish green better than Apis, and that Apis discriminates all other colors better. 3. The spectral properties of the receptor types were used to construct a color space in which all the color signals tested in the behavioral experiments are represented at particular loci (Fig. 3). A receptor model of color vision as proposed by Backhaus and Menzel (1987) for the honeybee is used to calculate the perceptual distance between the colors corresponding to the loci of the color stimuli. This model interprets the perceptual distance between two color stimuli as the number of just noticeable difference steps in the corresponding receptor voltage signals. The predicted distances are highly correlated with the discrimination values of the behavioral tests (Fig. 12).

Seasonal variation in cone sensitivity and short-wave absorbing visual pigments in the rudd Scardinius erythrophthalmus

Microspectrophotometric and electroretinographic investigation of photoreceptor spectral sensitivity in the rudd Scardinius erythrophthalmus has revealed four spectral classes of cone with peak sensitivity in the ultra-violet, violet, green and red regions of the spectrum. These peak sensitivities were found to vary seasonally, and in response to artificial illumination, as a result of a change in the ratio of A1 to A2-based visual pigment in the cells. Short daylengths favoured the A2 pigment whereas long daylengths favoured the A1 analogue. Both the ultra-violet and violet-sensitive pigments have not previously been reported for the rudd. Evidence is presented supporting the hypothesis that the ultra-violet class of cells is not present in older fish.

Spectral Sensitivity of Photoreceptors and Colour Vision in the Solitary Bee, Osmia Rufa

ABSTRACT The spectral sensitivity of single photoreceptors of Osmia rufa was determined by a fast voltage-clamp technique. Three receptor types were found whose spectral sensitivity functions followed a rhodopsin-like photopigment absorption function with λmax values at 348nm (ultraviolet receptor), 436nm (blue receptor) and 572nm (green receptor). The λmax of the green receptor in Osmia rufa is shifted to much longer wavelengths compared with other insect species. Discrimination of colour signals was tested after training a bee at the entrance to its nest. The colour signals were filter discs (70 mm in diameter) with a hole (10 mm in diameter) in the centre and the bees quickly learned to use the coloured disc as a marker of the nest entrance. Tests were dual forced-choice tests with two coloured discs closely positioned next to each other. 94 different tests were each repeated 5–15 times and were performed after training to 12 different colour signals. A photoreceptor model was used to calculate the loci of the colour signals in a three-dimensional colour space and in a chromaticity diagram. The perceptual distance between the colour loci was calculated as line elements (minimum number of just noticeable difference, jnd-steps), which were based on the noise properties of the photoreceptors. The discrimination determined by the behavioural tests correlated very well with the jnd-steps. The correlation was better for the line elements in the colour plane than in the colour space. Osmia rufa was compared with the honeybee Apis mellifera and the stingless bee Melipona quadrifasciata. There is no difference in colour selection between Osmia and Apis, whereas Melipona discriminates less well in the violet-blue region. The model calculation was used to compare the chromaticity diagrams and the spectral discrimination functions of the three species. It is concluded that the receptor model used in this study predicts the discrimination behaviour of the three bee species very well. Therefore, comparative studies on colour vision in flower visiting insects may be based on spectral measurements of the photoreceptors, and in many cases this reduces the extent of laborious behavioural studies.

Spectral sensitivity of photoreceptors in insect compound eyes: Comparison of species and methods

Three different methods were used to determine the spectral sensitivity of retinula cells in the compound eyes of three species of hymenopteran insects (Apis mellifera, Melipona quadrifasciata, Osmia rufa). The conventional flash method gives the least reliable results. Sensitivity is extremely sensitive to small fluctuations of the resting potential and long lasting changes induced by preceding test flashes. The ramp method, which speeds up a spectral scan to about 1 min and keeps effective illumination constant at every flash, determines S(λ) much more reliably. The best results are obtained with the spectral scan method, which provides the experimenter with aS(λ) function of high spectral resolution within 20 s. Using this method we demonstrate that the high observed variability inS(λ) of individual receptors is the result of the inadequacy of the flash method, which was the only method used in earlier studies. Double microelectrode experiments and variations of the stimulus conditions reveal that field potentials and return flow of electric current produced by activated neighboring cells have no effect in the bee eye. We conclude that the model of Shaw (1975, 1981) of current flow in the locust and fly eye does not apply to the bee eye. Very rare recordings (about 1%) of UV receptors with hyperpolarizing responses to long wavelength light are interpreted as having a synaptic inhibitory connection to green receptors. The improvement of spectral measurements of single receptors allows us for the first time to model the spectral input to a color-coding network with great precision.

Spectral sensitivity of photoreceptors in the compound eye of the locust

Intracellular recordings have shown that there are three types of receptors in the retina of the locust with lambda max = 360, 430 and 530 nm. Their spectral sensitivity curves are considerably wider than the absorption curves of the corresponding pigments. On the basis of spectral sensitivity curves obtained and assuming that each receptor contains only one pigment, possible coefficients of electrical coupling between receptors with different spectral characteristics are calculated. They correspond to coefficients of electrical coupling obtained by Shaw and Lillywhite in the locust. Thus the observed broadening of spectral sensitivity curves as compared with the absorption curves of pigments may be caused by electrical coupling between receptors.

Spectral sensitivities of seven morphological types of photoreceptors in the retina of the turtle, Geoclemys reevesii.

Spectral sensitivities of photoreceptors in the turtle (Geoclemys) retina were studied by intracellular recording, and each cell was filled with Lucifer yellow (LY). Photoreceptors were classified into seven morphological types: rod, four types of single cones, and two members of a double cone. Single cones contained one of four different oil droplets: red, pale-green, orange, and clear. Double cones consisted of two apposed cones; principal members contained yellow oil droplets, while accessory members contained no oil droplet. Spectral sensitivities recorded from these seven types of photoreceptors were classified into one type of rod and three chromatic types of cones. Rods (n = 19) showed peak sensitivity at 520 nm. Single cones containing either a red (n = 51) or a pale-green (n = 9) oil droplet were red-sensitive (lambda max at 620 nm). Single cones containing an orange oil droplet (n = 14) were green-sensitive (lambda max at 540 nm). Single cones containing a clear oil droplet (n = 3) were blue-sensitive (lambda max at 460 nm). Both members of the double cone, principal (n = 22) and accessory (n = 15), were red-sensitive (lambda max at 620 nm). No diffusion of LY was detected between the apposed members of double cones. Red-sensitive cones, therefore, consisted of four different morphological types of cones, and they occupy about 70% of the photoreceptor mosaic in the turtle retina.

Polarization and spectral sensitivity of single photoreceptors of the domestic cricket

The polarization and spectral sensitivity of single photoreceptors ofAcheta domesticus L. was measured. The morphological characteristics of the cricket rhabdome satisfy the conditions for a symmetrical model, for which the polarization sensitivity of a single photoreceptor is identically equal to the dichroism of a single microvillus. Characteristic curves of spectral sensitivity of all photoreceptors measured (24 cells) were similar and had two maxima: the principal at 500 nm and a secondary peak at 360 nm, characteristic of a pigment such as rhodopsin in the rods of the vertebrate retina. The mean value of polarization sensitivity measured was 2.28 ± 0.85 (mean ± standard deviation, 70 cells), suggesting the existence of slight preferential orientation of the dipole moments of the rhodopsin molecules along the axes of the microvilli.

On-line computation of photoreceptor spectral sensitivity—A low-cost solution with a programmable pocket calculator

The knowledge of the function of photoreceptors has gained much from studies of invertebrate retinae. In particular, the determination of the spectral properties has led to new concepts of the transduction of light into biologically relevant information (e.g. Laughlin, 1976; Wasserman, 1973; Menzel, 1975). Invertebrate photoreceptors respond with graded depolarizing potentials to an increase of light intensity (Fig. 1A). The size of the receptor potentials depends on the number of light quanta absorbed. Both the wavelength and the number of absorbed quanta of the stimulating light determine the response size. The spectral sensitivity of a photoreceptor is measured by determining the number of absorbed quanta, which produce a constant receptor response for different wavelengths. To measure the spectral sensitivity of a photoreceptor, one has to stimulate the eye with diff’erent intensities of monochromatic light. As it is not always possible to measure intracellular responses of a cell over many minutes, the calculation ot’ spectral sensitivity is often difficult or even impossible.