Filtering and polychromatic vision in mantis shrimps: themes in visible and ultraviolet vision

Stomatopod crustaceans have the most complex and diverse assortment of retinal photoreceptors of any animals, with 16 functional classes. The receptor classes are subdivided into sets responsible for ultraviolet vision, spatial vision, colour vision and polarization vision. Many of these receptor classes are spectrally tuned by filtering pigments located in photoreceptors or overlying optical elements. At visible wavelengths, carotenoproteins or similar substances are packed into vesicles used either as serial, intrarhabdomal filters or lateral filters. A single retina may contain a diversity of these filtering pigments paired with specific photoreceptors, and the pigments used vary between and within species both taxonomically and ecologically. Ultraviolet-filtering pigments in the crystalline cones serve to tune ultraviolet vision in these animals as well, and some ultraviolet receptors themselves act as birefringent filters to enable circular polarization vision. Stomatopods have reached an evolutionary extreme in their use of filter mechanisms to tune photoreception to habitat and behaviour, allowing them to extend the spectral range of their vision both deeper into the ultraviolet and further into the red.     

Modelling oil droplet absorption spectra and spectral sensitivities of bird cone photoreceptors

Birds have four spectrally distinct types of single cones that they use for colour vision. It is often desirable to be able to model the spectral sensitivities of the different cone types, which vary considerably between species. However, although there are several mathematical models available for describing the spectral absorption of visual pigments, there is no model describing the spectral absorption of the coloured oil droplets found in three of the four single cone types. In this paper, we describe such a model and illustrate its use in estimating the spectral sensitivities of single cones. Furthermore, we show that the spectral locations of the wavelengths of maximum absorbance (_max) of the short- (SWS), medium- (MWS) and long- (LWS) wavelength-sensitive visual pigments and the cut-off wavelengths (_cut) of their respective C-, Y- and R-type oil droplets can be predicted from the _max of the ultraviolet- (UVS)/violet- (VS) sensitive visual pigment.     

Spectral sensitivity of photoreceptors in the compound eye of stingless tropical bees

The spectral sensitivity of photoreceptors of the tropical bees Melipona quadrifasciata, M. marginata, and Trigona spinipes were measured on-line with a rapid constant response amplitude method. The results indicate that although these bees forage in different habitats they have the same set of photoreceptors with sensitivity maxima in ultra-violet, blue and green.     

Electrophysiology of the visual system in the cricket Gryllus firmus (Orthoptera: Gryllidae): Spectral sensitivity of the compound eyes

The electroretinographic spectral sensitivity of the cricket compound eyes shows the presence of two receptor types, a dominant one at 520 nm and another in the near-u.v. (λ_max 355 ± 5 nm) under dark- and intense chromatic adaptation conditions (Fig. 3). The waveform of the electrical responses elicited by short-wavelength stimuli differ from those elicited by long wavelength stimuli (Fig. 1).     

Tetrachromacy in a butterfly that has eight varieties of spectral receptors

This paper presents the first evidence of tetrachromacy among invertebrates. The Japanese yellow swallowtail butterfly, Papilio xuthus, uses colour vision when foraging. The retina of Papilio is furnished with eight varieties of spectral receptors of six classes that are the ultraviolet (UV), violet, blue (narrow-band and wide-band), green (single-peaked and double-peaked), red and broad-band classes. We investigated whether all of the spectral receptors are involved in colour vision by measuring the wavelength discrimination ability of foraging Papilio. We trained Papilio to take nectar while seeing a certain monochromatic light. We then let the trained Papilio choose between two lights of different wavelengths and determined the minimum discriminable wavelength difference Deltalambda. The Deltalambda function of Papilio has three minima at approximately 430, 480 and 560nm, where the Deltalambda values approximately 1nm. This is the smallest value found for wavelength discrimination so far, including that of humans. The profile of the Deltalambda function of Papilio can be best reproduced by postulating that the UV, blue (narrow-band and wide-band), green (double-peaked) and red classes are involved in foraging. Papilio colour vision is therefore tetrachromatic.     

Ionic permeabilities of the plasma membrane of isolated intact bovine rod outer segments as studied with a novel optical probe

Summary The permeability properties of the plasma membrane of intact rod outer segments purified from bovine retinas (ROS) were studied with the aid of the optical probe neutral red as described in the companion paper. The following observations were made: (1) Electrical shunting of ROS membranes greatly stimulated Na⁺ and K⁺ transport, suggesting that this transport reflects Na⁺ and K⁺ currents, respectively. The dissipation of a Na⁺ gradient across the plasma membrane occurred with a half-time of 30 sec at 25°C. (2) The Na⁺ permeability was progressively inhibited when the external Ca²⁺ concentration was raised from 1 m to 20mm. A similar Ca²⁺ dependence was observed for H⁺ and Li⁺ transport. The Na⁺ permeability was not affected when the total internal Ca²⁺ content of ROS was varied between 0.1 mol Ca²⁺/mol rhodopsin and 7 mol Ca²⁺/mol rhodopsin, or when the free internal Ca²⁺ concentration was varied between 0.1 and 50 m. (3) The K⁺ permeability was progressively stimulated when the external Ca²⁺ concentration was raised from 0.001 to 1 m, whereas a further increase to 20mm was without effect. A similar Ca²⁺ dependence was observed for Rb⁺ and Cs⁺ transport. (4) At an external Ca²⁺ concentration in the micromolar range the rate of transport decreased in the order: Na⁺>K⁺=H⁺>Cs⁺>Li⁺. (5) Na⁺ fluxes depended in a sigmoidal way on the external Na⁺ concentration, suggesting that sodium ions move in pairs. The concentration dependence of uniport Na⁺ transport and that of Na⁺-stimulated Ca²⁺ efflux (exchange or antiport transport) were very similar.     

Unexpectedly low UV-sensitivity in a bird,the budgerigar

Photoreceptor adaptation ensures appropriate visual responses during changing light conditions and contributes to colour constancy. We used behavioural tests to compare UV-sensitivity of budgerigars after adaptation to UV-rich and UV-poor backgrounds. In the latter case, we found lower UV-sensitivity than expected, which could be the result of photon-shot noise corrupting cone signal robustness or nonlinear background adaptation. We suggest that nonlinear adaptation may be necessary for allowing cones to discriminate UV-rich signals, such as bird plumage colours, against UV-poor natural backgrounds.     

Ultraviolet vision in birds: the importance of transparent eye media

Ultraviolet (UV)-sensitive visual pigments are widespread in the animal kingdom but many animals, for example primates, block UV light from reaching their retina by pigmented lenses. Birds have UV-sensitive (UVS) visual pigments with sensitivity maxima around 360–373 nm (UVS) or 402–426 nm (violet-sensitive, VS). We describe how these pigments are matched by the ocular media transmittance in 38 bird species. Birds with UVS pigments have ocular media that transmit more UV light (wavelength of 50% transmittance, λ_T0.5, 323 nm) than birds with VS pigments (λ_T0.5, 358 nm). Yet, visual models predict that colour discrimination in bright light is mostly dependent on the visual pigment (UVS or VS) and little on the ocular media. We hypothesize that the precise spectral tuning of the ocular media is mostly relevant for detecting weak UV signals, e.g. in dim hollow-nests of passerines and parrots. The correlation between eye size and UV transparency of the ocular media suggests little or no lens pigmentation. Therefore, only small birds gain the full advantage from shifting pigment sensitivity from VS to UVS. On the other hand, some birds with VS pigments have unexpectedly low UV transmission of the ocular media, probably because of UV blocking lens pigmentation.     

Teleost polarization vision: how it might work and what it might be good for

In this review, we will discuss the recent literature on fish polarization vision and we will present a model on how the retina processes polarization signals. The model is based on a general retinal-processing scheme and will be compared with the available electrophysiological data on polarization processing in the retina. The results of this model will help illustrate the functional significance of polarization vision for both feeding behaviour and navigation. First, we examine the linkage between structure and function in polarization vision in general.     

Single-channel study of the cGMP-dependent conductance of retinal rods from incorporation of native vesicles into planar lipid bilayers

Summary Unitary currents through cGMP-dependent channels of retinal rods are observed following incorporation into planar lipid bilayers of native vesicles from purified rod outer segment membranes washed free of soluble and peripheral proteins. The influence of the concentration of cGMP, inhibitors (cis-diltiazem, tetracaine and Ag⁺) and divalent cations (Ca²⁺, Mg²⁺, and Co²⁺) on the conductance and open probability of the channel is described, as well as the voltage dependence of these effects. The cGMP dependence suggests the existence of four binding sites for cGMP and reveals that sequential binding of four cGMP molecules corresponds to the opening of four discrete conductance levels. Finally, we provide conclusive evidence that activated G-protein does not directly inactivate the cGMP-dependent channels of bovine retinal rods.     

Visual modelling suggests a weak relationship between the evolution of ultraviolet vision and plumage coloration in birds

Birds have sophisticated colour vision mediated by four cone types that cover a wide visual spectrum including ultraviolet (UV) wavelengths. Many birds have modest UV sensitivity provided by violet‐sensitive (VS) cones with sensitivity maxima between 400 and 425 nm. However, some birds have evolved higher UV sensitivity and a larger visual spectrum given by UV‐sensitive (UVS) cones maximally sensitive at 360–370 nm. The reasons for VS–UVS transitions and their relationship to visual ecology remain unclear. It has been hypothesized that the evolution of UVS‐cone vision is linked to plumage colours so that visual sensitivity and feather coloration are ‘matched’. This leads to the specific prediction that UVS‐cone vision enhances the discrimination of plumage colours of UVS birds while such an advantage is absent or less pronounced for VS‐bird coloration. We test this hypothesis using knowledge of the complex distribution of UVS cones among birds combined with mathematical modelling of colour discrimination during different viewing conditions. We find no support for the hypothesis, which, combined with previous studies, suggests only a weak relationship between UVS‐cone vision and plumage colour evolution. Instead, we suggest that UVS‐cone vision generally favours colour discrimination, which creates a nonspecific selection pressure for the evolution of UVS cones.     

Spectral Sensitivity of the Hawaiian Saddle Wrasse, Thalassoma duperrey, and Implications for Visually Mediated Behaviour on Coral Reefs

Although tropical coral reefs are one of the most spectrally complex habitats, there is relatively little known about colour vision of reef fish. In this study, we measured the spectral sensitivity of an endemic Hawaiian coral reef fish, Thalassoma duperrey (family Labridae), and assessed the possible role of visual sensitivity in mediating intraspecific communication. Electrophysiological recordings of compound action potentials from retinal ganglion cells were used to generate spectral sensitivity curves for specific wavelengths (380–620nm). We found at least 2 sensitivity peaks for the on response (_max=460, 550nm). The off response lacked a short wavelength mechanism but a medium wavelength mechanism (_max=545nm) and a longwave mechanism (_max=570nm) were found. To quantify the visual stimulus provided by a conspecific individual, spectral reflectance from the colour pattern of T. duperrey was measured with a spectroradiometer. Luminance and spectral contrast were computed between colour patches of the pattern and between the patches and natural backgrounds (i.e., water and coral). Reflectance from the blue head and contrast from the blue, green and red patches matched the sensitivity maxima of T. duperrey, although this depended on the type of background. Our results indicate that T. duperrey should be able to visually detect the colour pattern of a conspecific fish and that T. duperrey's visual system is designed to enhance target detection in the coral reef habitat with matched and offset cone mechanisms.