The visual pigments of a deep-sea teleost, the pearl eye Scopelarchus analis (original) (raw)
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The Journal of Comparative Neurology, 2006
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 Ϯ 2.68 m ellipsoid diameter). Photopic sensitivity is optimized with a theoretical spatial resolving power of 3.28 Ϯ 0.66 cycles degree Ϫ1 , 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 Ϫ2 , 4,670 red cones mm Ϫ2 , 900 yellow cones mm Ϫ2 , and 320 colorless cones mm Ϫ2 ), 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.
Grouped retinae and tapetal cups in some Teleostian fish: Occurrence, structure, and function
Progress in Retinal and Eye Research, 2014
This article presents a summary and critical review of what is known about the 'grouped retina', a peculiar type of retinal organization in fish in which groups of photoreceptor cell inner and outer segments are arranged in spatially separated bundles. In most but not all cases, these bundles are embedded in light-reflective cups that are formed by the retinal pigment epithelial cells. These cups constitute a specialized type of retinal tapetum (i.e., they are biological 'mirrors' that cause eye shine) and appear to be optimized for different purposes in different fishes. Generally, the large retinal pigment epithelial cells are filled with light-reflecting photonic crystals that consist of guanine, uric acid, or pteridine depending on species, and which ensure that the incoming light becomes directed onto the photoreceptor outer segments. This structural specialization has so far been found in representatives of 17 fish families; of note, not all members of a given family must possess a grouped retina, and the 17 families are not all closely related to each other. In many cases (e.g., in Osteoglossomorpha and Aulopiformes) the inner surface of the cup is formed by three to four layers of strikingly regularly shaped and spaced guanine platelets acting as an optical multilayer. It has been estimated that this provides an up to 10fold increase of the incident light intensity. In certain deep-sea fish (many Aulopiformes and the Polymixidae), small groups of rods are embedded in such 'parabolic mirrors'; most likely, this is an adaptation to the extremely low light intensities available in their habitat. Some of these fishes additionally possess similar tapetal cups that surround individual cones and, very likely, also serve as amplifiers of the weak incident light. In the Osteoglossomorpha, however, that inhabit the turbid water of rivers or streams, the structure of the cups is more complex and undergoes adaptation-dependent changes. At dim daylight, probably representing the usual environmental conditions of the fish, the outer segments of up to 30 cone cells are placed at the bottom of the cup where light intensity is maximized. Strikingly, however, a large number of rod receptor cells are positioned behind each mirroring cup. This peculiar arrangement (i) allows vision at deep red wavelenghts, (ii) matches the sensitivity of rod and cone photoreceptors, and (iii) facilitates the detection of low-contrast and color-mixed stimuli, within the dim, turbid habitat. Thus, for these fish the grouped retina appears to aid in reliable and quick detection of large, fast moving, biologically relevant stimuli Abbreviations: INL, inner nuclear layer; ONL, outer nuclear layer; OLM, outer limiting membrane; OS, outer segment(s); RGCs, retinal ganglion cells; RPE, retinal pigment epithelium.
Frontiers in Ecology and Evolution, 2016
Marine hatchetfishes, Argyropelecus spp., are one of the 14 genera of mesopelagic teleosts, which possess tubular eyes. The tubular eyes are positioned dorsally on the head and consist of a main retina, which subtends a large dorsal binocular field, and an accessory retina, which subtends the lateral monocular visual field. The topographic distribution of photoreceptors in the retina of Argyropelecus sladeni, Argyropelecus affinis, and Argyropelecus aculeatus was determined using a random, unbiased and systematic stereological approach, which consistently revealed a region of high density (area centralis) in the central region of the main retina (up to a peak of 96,000 receptors per mm 2) and a relatively homogeneous density of photoreceptors in the accessory retina (of ∼20,000 receptors per mm 2). The position of the area centralis in the main retina indicates this retinal region subserves greater spatial resolution in the center of the dorsal binocular visual field. Light microscopy and transmission electron microscopy also revealed the presence of multiple photoreceptor types (two rod-like and one cone-like) based on the size and shape of the inner and outer segments and ultrastructural differences in the ellipsoidal region. The presence of multiple photoreceptor types in these tubular-eyed, mesopelagic hatchetfishes may reflect the need for the visual system to function under different lighting conditions during vertical migratory behavior, especially given their unique dorsally-facing eyes.
Specialization of retinal function in the compound eyes of mantis shrimps
Vision Research, 1994
Visual function and its specialization at the level of the retina were studied in 13 species of stomatopod crustaceans, representing three superfamilies: ~~a~~idea, L~Uoidea, and Squilloidea. We measured a~en~~on and h-radiance spectra in the-~~on~nt of each species, at the actual depths and times of activity where we observed individuals. We also characterized the intrarbabdomal illters of all study species and determined tbe absolute spectral sensitivity functions and approximate photon capture rates of all photoreceptor classes below the level of the 8th retinular cell in seven of these species. Sballow-water gouodactyloid species have four distinct classes of intrarhabdomal illters, producing photoreceptors that are relatively h&sensitive but which have the broadest spectral coverage of all. Deep-water go~a~~~ and all Iy~~~Uoi~ have filters that are spectrally less diverse. These species often discard the proximal filter classes of one or more receptor types. As a result, their retinas are more sensitive but have reduced spectral range or diversity. The single squilloid species has the most sensitive photoreceptors of any we observed, due to the lack both of hrtrarhabdomal illters and tiered photoreceptors. Photon absorption rates, at the times of animal activity, were similar in most photoreceptor classes of all species, whether the receptors were tiered or untiered, or filtered or unfiltered. Tlms, the retinas of stomato~ are specialized to operate at similar levels of ~ulation at the times and depths of actual use, while evidently untying the greatest possible potential for spectral coverage and discrimination.
Visual Neuroscience, 2004
The dorso-laterally located eyes of the southern hemisphere lampreyMordacia mordax(Agnatha) contain a single morphological type of retinal photoreceptor, which possesses ultrastructural characteristics of both rods and cones. This photoreceptor has a large refractile ellipsosome in the inner segment and a long cylindrical outer segment surrounded by a retinal pigment epithelium that contains two types of tapetal reflectors. The photoreceptors form a hexagonal array and attain their peak density (33,200 receptors/mm2) in the ventro-temporal retina. Using the size and spacing of the photoreceptors and direct measures of aperture size and eye dimensions, the peak spatial resolving power and optical sensitivity are estimated to be 1.7 cycles deg−1(minimum separable angle of 34′7′′) and 0.64 μm2steradian (white light) and 1.38 μm2steradian (preferred wavelength or λmax), respectively. Microspectrophotometry reveals that the visual pigment located within the outer segment is a rhodopsin w...
Frontiers in Ecology and Evolution, 2016
Lungfishes are the closest living relatives of the ancestors to all terrestrial vertebrates and have remained relatively unchanged since the early Lochkovin period (410 mya). Lungfishes, therefore, represent a critical stage in vertebrate evolution and their sensory neurobiology is of considerable interest. This study examines the ultrastructure of the retina of two species of lungfishes: the South American lungfish, Lepidosiren paradoxa and the spotted African lungfish, Protopterus dolloi in an attempt to assess variations in photoreception in these two ancient groups of sarcopterygian (lobe-finned) fishes. In juvenile P. dolloi, the retina contains one rod and two cone photoreceptor types (one containing a red oil droplet), while only one rod and one cone photoreceptor type is present in adult L. paradoxa. Both species lack double cones. The large size and inclusion of oil droplets in both species apart from one of the cone photoreceptor types in P. dolloi suggests that L. paradoxa and P. dolloi are adapted for increasing sensitivity. However, the complement of photoreceptor types suggests that there may be a major difference in the capacity to discriminate color (dichromatic and monochromatic photoreception in P. dolloi and L. paradoxa, respectively). This study suggests that the visual needs of these two species may differ.
Retinal projections in teleost fishes: Patterns, variations, and questions
Comparative Biochemistry and Physiology Part A: Physiology, 1993
l. Variations in the pathways of fibers and in the morphology of nuclei in the central nervous system can be used to infer evolutionary changes. 2. Within the large and diverse radiation of ray-finned fishes, variations in the visual system-including the paths of ipsilaterally projecting fibers, the distribution of retinopetal cells, the geometry of homologous nuclei relative to topographically mapped projections, the relative size of homologous nuclei, the structure of the optic tectum, and even an evolutionarily novel nucleus-have been found.