[Current views on vision of mammals].

In the review, research data are presented on mammals' vision including visual pigments, color and contrast vision, and visual behaviour in different species. It is shown that in course of evolution mammals were gradually losing the elements of daylight cone vision system that are typical of other vertebrates. In monotremes, visual pigments SWS2 (cone blue-sensitive 2) and MWS/LWS (green/red-sensitive) are still present, as well as rod RH1. Theria, except some primates, also have two cone visual pigments: SWS1 (ultraviolet/violet or blue-sensitive 1) and MWS/LWS along with rod RH1. Humans and some other higher primates evolved the new visual pigment, MWS, and acquired trichromatic vision. Marine mammals (cetaceans and pinnipeds) and some species of other orders have lost also the visual pigment SWS1, probably due to specificity of processing the information received by these cones. Current view on mammals' vision with two cone pigments and rods is presented. Data on maximum spectral sensitivity of visual pigments in different species and orders are given along with data on spatial contrast sensation. High visual acuity has been acquired by ungulates, artiodactyls, and primates, while the highest one--by humans with their specialized fovea.

Spectral sensitivity of four species of fiddler crabs (Uca pugnax, Uca pugilator, Uca vomeris and Uca tangeri) measured by in situ microspectrophotometry.

Fiddler crabs have compound eyes that are structurally fairly well understood. However, there has been much debate regarding their spectral sensitivity and capacity to enable colour discrimination. We examined the visual pigments of two North-American species (Uca pugnax and U. pugilator), one species from the Indo-West Pacific (U. vomeris) and the only Eastern-Atlantic species (U. tangeri) of fiddler crabs using in situ microspectrophotometry of frozen sections of dark-adapted eyes. Only one spectral class of visual receptor was found in the larger (R1-7) retinular cells of each species, with maximum absorption peaking between 508 nm and 530 nm (depending upon species). The R8 retinular cell, that might contain a short-wavelength sensitive photopigment and provide a basis for colour vision, was too small to analyze by these methods. Rhabdoms were lined with screening pigment which strongly influenced each species' spectral sensitivity, sharpening the peak and shifting the maximum towards longer wavelengths, on occasion to as far as the 600 nm region. We hypothesize that sensitivity to longer wavelengths enhances contrast between background (blue sky or tall vegetation) and the male major claw during the waving display.

L and M cone proportions in polymorphic New World monkeys.

Platyrrhine monkeys typically have only a single X-chromosome opsin gene. Alleles of this gene code for multiple versions of middle- to long-wavelength cone photopigments. X-chromosome inactivation provides heterozygous females with a retinal mosaic of cones containing either of two types of M and L pigment, thus establishing the photopigment basis for trichromatic color vision. This study examined the proportions of L and M cones created by this process. For that purpose, electroretinogram flicker photometry was used to obtain complete spectral sensitivity functions from 60 heterozygous female monkeys drawn from seven genera of platyrrhine monkeys. To obtain estimates of cone proportions, these functions were subsequently fit with linear combinations of L and M cone fundamentals that were derived from similar recordings made on conspecific animals having only one type of M/L pigment. Consistent with a random X-chromosome inactivation process, the average L:M cone weighting across the sample was close to unity. At the same time, there were significant individual variations in L:M cone proportions. The genesis of this variation and its implications for seeing are discussed.

Ommatidial type-specific interphotoreceptor connections in the lamina of the swallowtail butterfly, Papilio xuthus.

The eye of the butterfly Papilio xuthus contains a random array of three types of ommatidia (types I-III), each bearing nine photoreceptors, R1-R9. Of the six spectral classes of photoreceptors identified, types I, II, and III ommatidia contain four, three, and two classes, respectively: the ommatidia are thus spectrally heterogeneous. The photoreceptors send their axons to the lamina where, together with some large monopolar cells (LMCs), the nine from a single ommatidium contribute to a module called a lamina cartridge. We recently reported that among different photoreceptor axon terminals visualized by confocal microscopy, the number and length of axon collaterals differ for different spectral receptors, suggesting that lamina circuits are specific for each ommatidial type. Here we studied the distribution of synapse-like structures in the cartridges, first characterizing a photoreceptor by measuring its spectral sensitivity and then injecting Lucifer yellow (LY). We subsequently histologically identified the type of ommatidium to which the injected photoreceptor belonged, cut serial ultrathin sections of the entire lamina, labeled these with anti-LY immunocytochemistry, and then localized synapse-like structures. We found numerous interphotoreceptor contacts both within and between cartridges, the combination of which was again specific for the ommatidial type. R3 and R4, which are green-sensitive photoreceptors in all ommatidia, have thick axons lacking collaterals. We found that these cells exclusively make contacts with LMCs and not with photoreceptors. We therefore presume that R3 and R4 construct a system for motion vision, whereas other randomly distributed spectral types provide inputs for color vision.

Morphology, characterization, and distribution of retinal photoreceptors in the Australian lungfish Neoceratodus forsteri (Krefft, 1870).

The Australian lungfish Neoceratodus forsteri (Dipnoi) is an ancient fish that has a unique phylogenetic relationship among the basal Sarcopterygii. Here we examine the ultrastructure, histochemistry, and distribution of the retinal photoreceptors using a combination of light and electron microscopy in order to determine the characteristics of the photoreceptor layer in this living fossil. Similar proportions of rods (53%) and cones (47%) reveal that N. forsteri optimizes both scotopic and photopic sensitivity according to its visual demands. Scotopic sensitivity is optimized by a tapetum lucidum and extremely large rods (18.62 +/- 2.68 microm ellipsoid diameter). Photopic sensitivity is optimized with a theoretical spatial resolving power of 3.28 +/- 0.66 cycles degree(-1), which is based on the spacing of at least three different cone types: a red cone containing a red oil droplet, a yellow cone containing a yellow ellipsoidal pigment, and a colorless cone containing multiple clear oil droplets. Topographic analysis reveals a heterogeneous distribution of all photoreceptor types, with peak cone densities predominantly found in temporal retina (6,020 rods mm(-2), 4,670 red cones mm(-2), 900 yellow cones mm(-2), and 320 colorless cones mm(-2)), but ontogenetic changes in distribution are revealed. Spatial resolving power and the diameter of all photoreceptor types (except yellow cones) increases linearly with growth. The presence of at least three morphological types of cones provides the potential for color vision, which could play a role in the clearer waters of its freshwater environment.

Photoreceptor projection reveals heterogeneity of lamina cartridges in the visual system of the Japanese yellow swallowtail butterfly, Papilio xuthus.

The compound eye of the butterfly Papilio xuthus is composed of three types of spectrally heterogeneous ommatidia. The ommatidia, which contain nine photoreceptor cells, R1-9, bear four (type I), three (type II), or two (type III) classes of spectral receptors in fixed combinations. The photoreceptors send their axons to the lamina, the first optic ganglion, where the R1-9 axons originating from a single ommatidium, together with some second-order neurons, form a neuronal bundle, called a lamina cartridge. We investigated the axonal structure of photoreceptors in the lamina to determine whether the cartridge structure is different between the three ommatidial types. We first characterized a photoreceptor by measuring its spectral sensitivity and then injected Lucifer Yellow. We subsequently identified the type of ommatidium of the injected photoreceptor via histological sections. We further observed the axonal structure of the photoreceptor in the lamina by laser confocal microscopy. We found that the number and length of axon collaterals markedly differ between the spectral receptors. Those having the most extensive axon collaterals, which extend into six or more surrounding cartridges, are violet receptors (R1 and R2 of type II ommatidia). UV receptors (R1 or R2 of type I ommatidia) also send collaterals into two to four neighboring cartridges. Blue receptors (R1 or R2 of type I ommatidia, R1 and R2 of type III ommatidia) have short collaterals restricted to their own cartridges. We thus conclude that the neuronal circuit of the lamina cartridge differs between the three types of ommatidia.

Temporal shifts in visual pigment absorbance in the retina of Pacific salmon.

The visual pigments and photoreceptor types in the retinas of three species of Pacific salmon (coho, chum, and chinook) were examined using microspectrophotometry and histological sections for light microscopy. All three species had four cone visual pigments with maximum absorbance in the UV (lambda(max): 357-382 nm), blue (lambda(max): 431-446 nm), green (lambda(max): 490-553 nm) and red (lambda(max): 548-607 nm) parts of the spectrum, and a rod visual pigment with lambda(max): 504-531 nm. The youngest fish (yolk-sac alevins) did not have blue visual pigment, but only UV pigment in the single cones. Older juveniles (smolts) had predominantly single cones with blue visual pigment. Coho and chinook smolts (>1 year old) switched from a vitamin A1- to a vitamin A2-dominated retina during the spring, while the retina of chum smolts and that of the younger alevin-to-parr coho did not. Adult spawners caught during the Fall had vitamin A2-dominated retinas. The central retina of all species had three types of double cones (large, medium and small). The small double cones were situated toward the ventral retina and had lower red visual pigment lambda(max) than that of medium and large double cones, which were found more dorsally. Temperature affected visual pigment lambda(max) during smoltification.

The photoreceptor localization confirms the spectral heterogeneity of ommatidia in the male small white butterfly, Pieris rapae crucivora.

The compound eye of Pieris rapae crucivora contains ventrally three types of histologically distinct ommatidia. An ommatidium contains nine photoreceptors, four of which (R1-4) construct the distal tier of the rhabdom. We determined the sensitivity spectra of the R1-4 distal photoreceptors in each type of ommatidia by intracellular electrophysiology and identified UV, blue, double-peaked blue, green, and a green receptor with depressed sensitivity in the violet. We localized these receptors in each type of ommatidia by injecting dye after the recording. In type I ommatidia the R1 and R2 cells are UV and blue receptors. When R1 is UV sensitive, R2 is always blue sensitive, or vice versa. R3 and R4 in type I are both green receptors. In type II, R1 and R2 are both double-peaked blue receptors and R3 and R4 are both green receptors with depressed sensitivity in the violet. In type III, R1 and R2 are both UV, and R3 and R4 are green receptors. The double-peaked blue, and green receptors with depressed sensitivity in the violet in type II ommatidia have depressed sensitivity at 420 nm, which is probably due to the filtering effect of a fluorescing material present in the type II ommatidia. Spectral heterogeneity of ommatidia seems to be a common design of insect compound eyes.

The roles of receptor noise and cone oil droplets in the photopic spectral sensitivity of the budgerigar, Melopsittacus undulatus.

Individual budgerigars (Melopsittacus undulatus) were taught to detect narrow bands of wavelengths under ambient illumination of known spectral composition. Because the cone pigments of this species of bird have been identified and data on carotenoid absorbance present in the cone oil droplets are available, predictions of the Vorobyev-Osorio equations can be calculated with reasonable confidence. Based on more than 27,600 individual choices made by several birds at 10 wavelengths, the photopic sensitivity (i.e., color thresholds) of these birds is found to be consistent with the hypothesis that threshold discrimination of colored targets is limited by receptor noise and that high sensitivity to near-ultraviolet wavelengths is in harmony with the relatively small number of ultraviolet cones present in the retina. The pronounced fine structure of the sensitivity spectrum is caused by the absorption of cone oil droplets. Under natural sunlight, containing more energy in the near-ultraviolet than is present in artificial indoor lighting, the birds' peak of sensitivity in the ultraviolet should be much less prominent than it is in laboratory experiments.

Vision in the ultraviolet.

Sensitivity to ultraviolet light (UV) is achieved by photoreceptors in the eye that contain a class of visual pigments maximally sensitive to light at wavelengths <400 nm. It is widespread in the animal kingdom where it is used for mate choice, communication and foraging for food. UV sensitivity is not, however, a constant feature of the visual system, and in many vertebrate species, the UV-sensitive (UVS) pigment is replaced by a violet-sensitive (VS) pigment with maximal sensitivity between 410 and 435 nm. The role of protonation of the Schiff base-chromophore linkage and the mechanism for tuning of pigments into the UV is discussed in detail. Amino acid sequence analysis of vertebrate VS/UVS pigments indicates that the ancestral pigment was UVS, with loss of UV sensitivity occurring separately in mammals, amphibia and birds, and subsequently regained by a single amino acid substitution in certain bird species. In contrast, no loss of UV sensitivity has occurred in the UVS pigments of insects.

Fundus pigmentation and equiluminant moving phantoms.

Visual phantoms are a perceptual completion illusion wherein contours and surfaces are seen where none physically exist. The visibility of moving phantoms was measured with equiluminant and near equiluminant chromatic inducing gratings for observers having a fundus classified as either darkly or lightly pigmented. Phantom visibility was greatest for observers with a lightly compared to a darkly pigmented fundus with the two groups showing differences in visibility as a function of background luminance. The results are discussed relative to equiluminant stationary phantom findings and a proposed relationship between phantom visibility and magnocellular pathway activity.

Evolution of visual pigments and related molecules.

The molecular phylogenetic tree of vertebrate visual pigments, constructed on the basis of amino acid sequence identity, suggests that the visual pigments can be classified into five groups (L, ML, MS, S and Rh) and that their genes have evolved along these five gene lines. Goldfish has a UV-sensitive visual pigment (S group) localized in miniature single cone cells. Medaka has one type of rod cell containing rhodopsin (Rh group) and four types of cone cells, each of which contains a specific visual pigment with an absorption maximum that differs from those of the others. Frogs have a violet-sensitive visual pigment (S group) in small single cone cells and a blue-sensitive visual pigment (MS group) in green rod cells. Although nocturnal and diurnal geckos have rod- and cone-based retinas, respectively, they have phylogenetically closely related visual pigments. The pigments in each line may have restricted absorption maxima. We have cloned cDNAs encoding molecules involved in the phototransduction system of visual cells, such as phosphodiesterase, opsin kinase and arrestin. We then constructed phylogenetic trees of these molecules with the deduced amino acid sequences. The resulting phylogenetic trees show that these molecules are classified into two groups; one is expressed in cones and another in rods, suggesting that rods and cones contain homologous molecules with different amino acid sequences. These differences may result in the different light responses of rods and cones.

Phylogenetic relationships among vertebrate visual pigments.

Genomic DNA fragments in exon 4 of chicken, goldfish and salmon visual pigments were amplified by polymerase chain reaction, using oligonucleotide mixtures as primers, and hypothetical phylogenetic trees were drawn up from the deduced amino acid sequences. The results suggest that vertebrate visual pigments have evolved along at least five lines, and that these lines diverged from an ancestral gene before the bony fishes diverged from the rest of the higher vertebrates.

The novel ion pump rhodopsins from Haloarcula form a family independent from both the bacteriorhodopsin and archaerhodopsin families/tribes.

Extreme halophiles newly collected from Argentine salt flats were characterized, in one of which, Haloarcula (sp. arg-1), light-driven retinal protein ion pumps were found. The proton pump, cruxrhodopsin-1, shows amino acid sequence homologies of 52% to bacteriorhodopsin and 48% to archaerhodopsin-1. The anion pump, cruxhalorhodopsin-1, identified partially as a 394bp polymerase chain reaction product, shows homologies of 70% to halorhodopsin, and 72% to pharaonis halorhodopsin. The ion pumps (and possibly sensors still to be found) in Haloarcula sp. arg-1, which constitute the cruxrhodopsin-1 family, are distinct from the bacteriorhodopsin and the archaerhodopsin families/tribes.

Molecular characterization of a blue visual pigment gene in the fish Astyanax fasciatus.

We report here the isolation and sequence determination of a gene closely linked to the Astyanax red visual pigment gene. Reverse transcription polymerase chain reaction assays show that this new gene (B23 Af) and the previously characterized red and green visual pigment genes of Astyanax are all expressed in the eye. Phylogenetic analysis shows that B23Af belongs to the group consisting of short wavelength-sensitive pigment genes from different species and is most closely related to the goldfish blue visual pigment gene.