Development of the retinal tapetum lucidum of the walleye (Stizostedion vitreum vitreum)

The development of the retinal tapetum lucidum within the cells of the retinal pigment epithelium (RPE) has been investigated by both light and electron microscopy in the walleye (Stizostedion vitreum vitreum) in specimens ranging in total length from 25-140 mm. In addition changes in the arrangement of the photoreceptors (both rods and cones) in both light and dark-adaptation have also been studied. At 25 mm no evidence of a tapetum is present. At about 30 mm it makes its initial appearance as granular bodies formed within the apical smooth endoplasmic reticulum (SER) cisternae of the RPE cells in the superior temporal fundus. The developing tapetum then spreads peripherally and continues to thicken in existing areas. By 90 mm it is well established throughout the fundus but always appears better developed in the superior fundus. By 125-140 mm it is essentially adult in appearance. At 60-70 mm the rods and cones begin to form bundles producing macroreceptors of 20-30 photoreceptors. In dark-adaptation the rod bundles are retracted and have one or more cone cells centrally located in each bundle, with the bundles separated from one another by melanosomes. Initially when no tapetal material is present, post-larval walleye are positively phototactic and feed on zooplankton. In the adult condition when a tapetum lucidum and large macroreceptors are present, the walleye is negatively phototactic and feeds almost exclusively on larger organisms such as other fish.     

On the eye of the Goldeye Hiodon alosoides (Teleostei: Hiodontidae)

In the eye of the Goldeye the photoreceptors are arranged in bundles and the pigment epithelium contains a massive reflector or tapetum lucidum. Photoreceptor bundles are arranged in parallel rows, the bundles alternating in position from row to row. Each bundle contains about 60 photoreceptors, of which 30 or so are cones. Rod outer segments lie in the scleral half of the outer retinal region of the light-adapted eye. Processes of the pigment epithelium cells extend vitread almost to the external limiting membrane; they envelop the bundles of rods and cones, and a ring of four processes surrounds each bundle. A process contains two kinds of reflecting crystals (composed of uric acid). A large part of the epithelium cell is packed with small disc-shaped crystals (crystallites) enclosed in thin membranes; the tip of the process, in the region of the photoreceptor bundle, contains orderly arrays of small rod-shaped crystals (rodlets). It is suggested that the crystallites form a diffuse reflector backscattering light into the rods; and that the rodlets reflect light regularly from their surfaces into the photoreceptor bundles. In the light-adapted state, rods are enveloped by pigment and crystallites. The organization is compared with that of other fishes that have photoreceptors in bundles (grouped retinae) and tapeta lucida.     

Fine structure of the tapetum cellulosum of the grey seal (Halichoerus grypus)

The morphology of the tapetum lucidum of the grey seal (Halichoerus grypus) has been studied by light and electron microscopy. The reflective layer in this species is a tapetum cellulosum situated in the choroid and covering the entire effective fundus. Posteriorly the tapetum is composed of 30-35 layers of flattened polygonal cells. This number gradually declines to 15-20 layers in the extreme periphery. Near the retinal epithelial layer the tapetal cells are larger and more regular (brick-like) in arrangement whereas further from the retina the tapetal cells become more irregular in outline and more widely separated by collagen fibrils and connective tissue cells. In this outer region the tapetal cells are gradually replaced by melanocytes of the choroid. Within the tapetal cells a few mitochondria and profiles of smooth endoplasmic reticulum are scattered peripherally while the majority of the cell organelles are clustered near the centrally located vesicular nucleus. The dominant feature of the tapetal cells is, however, an accumulation of numerous electron-dense rodlets of presumed zinc cysteine. These rodlets are the reflective material of the tapetum and are arranged with their long axes perpendicular to the incoming light. The orientation of these rodlets is usually uniform within each tapetal cell but varies between adjacent cells. The diameter (0.10 micron) and spacing (0.15 micron) of these rodlets is consistent with the principles of constructive interference. Blood vessels penetrate the tapetum at right angles to supply the choriocapillaris which is indented into the amelanotic retinal epithelium to give a flat reflective surface to the tapetum.     

Fine structure of the retinal epithelium and tapetum lucidum of the ranch mink Mustela vison

The morphology of the retinal pigment epithelium (RPE), Bruch's membrane (complexus basalis), choriocapillaris and tapetum lucidum has been studied in the eye of the ranch mink (Mustela vison) by light and electron microscopy. The RPE is composed of a single layer of cells joined laterally by apically located junctional complexes. Basally (sclerally) these cells display numerous infoldings whereas apically (vitreally) two types of processes are associated with rod and cone outer segments. Smooth endoplasmic reticulum and mitochondria are abundant in these cells whereas rough endoplasmic reticulum and polysomes, although present, are not plentiful. An occasional wandering phagocyte is noted at the RPE-photoreceptor interface. In the posterosuperior part of the fundus, a degenerative tapetum lucidum is present. The presence of only a few layers of tapetal cells containing but little reflective material and the haphazard arrangement of this material makes it very unlikely that this area functions as an effective tapetum lucidum. The RPE over the aberrant tapetum, however, shows the morphology that is seen when a functioning tapetum cellulosum is present, namely the absence of melanosomes and an indented choriocapillaris. Bruch's membrane in non-tapetal areas is pentalaminate but, over the tapetum and where it is associated with capillary profiles, it is reduced to a single, thickened basal lamina. The choriocapillary endothelium is highly fenestrated and in nontapetal areas these capillaries are not indented into the epithelial layer.     

Histochemical and cytochemical demonstration of zinc cysteinate in the tapetum lucidum of the cat

Summary Zinc cysteinate is shown histochemically and cytochemically in the tapetum lucidum of the cat. Heavy metal is demonstrated in the paraplasmic rods of the tapetal cells with a sulphide silver method whereas no such reaction can be found in the pigmented epithelium of the retina. These rods are also stained with silver methenamine indicating the presence of reducing groups which probably appeared after hydrolization of cysteine.     

RETINAL GANGLION CELL SIZE AND DISTRIBUTION PREDICT VISUAL CAPABILITIES OF DALL'S PORPOISE

The structure of the retina, the distribution of ganglion cells, and the extent of the tapetum lucidum were studied in Dall's porpoise ( Phocoenoides dalli ) with the aim of understanding the role vision plays in this species of cetacean. The basic organization of the retina was similar to that of other vertebrates. Average ganglion cell size was 21.5 μm. The distribution of the ganglion cells in the retina was not even and there were two high-density areas, one in the temporal and one in the rostral part of the retina. Retinal resolving power was estimated using a terrestrial animal model incorporating the density of ganglion cells and other morphological data. The resolving power in the right eyes of two individuals was 2.60 and 2.64 cycles per degree. These values were close to those of other oceanic cetaceans, but inferior to those of terrestrial mammals. On the basis of amino acid analyses, it was shown that the choroid tapetum lucidum in Dali's porpoise contained collagen. The tapetum lucidum was thick at the fundal but thin at the peripheral part of the choroid.     

Retinal structure in Synbranchus marmoratus with observations on two new cone myoid inclusions.

The retina of a South American swamp eel, Synbranchus marmoratus (Synbranchidae), was studied by Golgi impregnation, light and electron microscopy. Its principal features include (1) the presence of a dense matrix, possibly a new type of tapetum lucidum, in the pigment epithelium, (2) a well developed photoreceptor layer containing large rods, single, double and triple cones, and (3) well developped inner nuclear and plexiform layers, with the exception of horizontal cells which are few and relatively small. These and other observations are discussed in relation to the photic environment and habits of this fish. The presence of microfilament bundles and two unusual features, microtubuleladen dense bodies and paracrystalline inclusions, in cone myoids are discussed in terms of their possible involvement in retinomotor responses.     

Hereditary abnormality in tapetum lucidum of the Siamese cats

Summary Gross examination showed a weaker reflection (less shining) of the tapetum lucidum of the Siamese cats compared with common cats. Toluidine blue sections revealed that many tapetal cells were weakly stained and giving vacuolated appearance under high magnification. Further examination with electron microscope showed that those weakly stained cells were filled with disrupted tapetal rods. In these affected cells, the arrangement of the tapetal rods was no longer regular. The membranes of the tapetal rods were either enlarged or disrupted. Some of them appeared to be myelin-like structures. The cores of the tapetal rods were either empty or filled with electron-dense materials which may be the remnant of the original cores. The severity of this type of abnormality or degeneration in the tapetum varied from lavers to layers. Those layers closer to the retina showed a greater number of cells with degeneration. Quantitative analysis of histochemical detection of zinc showed a significantly smaller amount of zinc in tapetal rods of the Siamese cats as compared with common cats. Less zinc and disruption of the regular arrangement of the tapetal rods may result in weaker reflection of light by Siamese cat tapetum. In four of the nine Siamese cats studied, this type of abnormality was observed. It suggests that it is a hereditary disorder of relatively high frequency.     

Electron microscopic study of the occlusible tapetum lucidum of the southern fiddler ray (Trygonorhina fasciata).

The choroidally located tapetum lucidum of the southern fiddler ray (Trygonorhina fasciata) has been examined by light and electron microscopy in both light- and dark-adaptation. In this species, the tapetum consists of a single layer of overlapping cells oriented at an angle of about 30 degrees to the incoming light. These are situated immediately external to the choriocapillaris. These tapetal cells alternate with and are separated from one another by melanocytes which have an inner extension that curves and intervenes between the tapetal cells and the choriocapillaris. The tapetal cells and the melanocytes are flattened cells with their widest dimension facing the retina. Internally the tapetal cells display a peripherally-located, vesicular nucleus with most of the cell organelles in a paranuclear location. The bulk of the cell is packed with regularly-spaced crystals reported to be guanine. The size and spacing of these reflective crystals is commensurate with constructive interference. In light-adaptation the small melanosomes of the melanocytes are widely dispersed and fill the portion of the cell intervening between the tapetal cells and the incoming light. This effectively occludes the tapetum as light is unable to reach the reflective material. In dark-adaptation the melanosomes withdraw from this location, exposing the tapetum to light and allowing it to act as a reflective layer. The retinal epithelium overlying the tapetal area is totally unpigmented so as not to interfere with the passage of light.     

The tapetum lucidum in the eye of the big-eye Priacanthus arenatus Cuvier

The big-eye Priacanthus arenatus Cuvier contains a tapetum lucidum or reflector which lies in the inner region of the choroid. It extends over the entire surface of the fundus, and it consists of several layers of reflecting cells. The cells contain many layers of thin guanine crystals, and there is about 0.5 mg of guanine in a square cm of tapetum. The retina is duplex, and rods are small and very numerous. The tapetum of the big-eye is compared with those of selachians and sturgeons, which it much resembles.     

Retinal epithelial fine structure in the grey seal (Halichoerus grypus)

The morphology of the retinal epithelium and the closely associated choriocapillaris and Bruch's membrane (complexus basalis) has been investigated in the eye of the grey seal (Halichoerus grypus) by electron microscopy. The retinal epithelium is composed of a single layer of cuboidal cells joined laterally by apically-located junctional complexes. Basally (sclerally) these cells display numerous infoldings while apically (vitreally) abundant processes enclose rod outer segments. Internally the large vesicular nucleus is centrally located. Smooth endoplasmic reticulum, mitochondria and lysosome-like bodies are abundant. Rough endoplasmic reticulum and polysomes while present are not plentiful. Phagosomes of outer-segment discs are only occasionally noted in the light-adapted state. As the entire fundus is overlain with a choroidally located tapetum cellulosum, only at the extreme periphery is an occasional melanosome present in these epithelial cells. The choriocapillaris endothelium is highly fenestrated and the profiles of these capillaries are deeply indented into the epithelial layer. Bruch's membrane (complexus basalis) is reduced to a trilaminate structure rather than the typical pentalaminate membrane seen in most mammalian species and when associated with capillary profiles is further reduced to a single thick basal lamina.     

The fine structure of the adepidermal reticulum in the basal membrane of the skin of the newt,Triturus

The fine structure of the tapetum of the cat eye has been investigated by electron microscopy. The tapetum is made up of modified choroidal cells, seen as polygonal plates grouped around penetrating blood vessels which terminate in the anastomosing capillary network of the choriocapillaris. The tapetal cells are rectangular in cross-section, set in regular brick-like rows, and attain a depth of some thirty-five cell layers in the central region. This number is gradually reduced peripherally, and is replaced at the margin of the tapetum by normal choroidal tissue. The individual cells are packed with long slender rods 0.1 micro by 4 to 5 micro. The rods are packed in groups and with their long axes oriented roughly parallel to the plane of the retinal surface. Each cell contains several such groups. Cells at the periphery or in the outer layers of the tapetum are frequently seen to contain both tapetal rods and melanin granules, the latter typical of the choroidal melanocytes. Also melanocyte granules may have intermediate shapes. These observations plus the similar density of the two inclusions lead to the belief that the tapetal rods may be melanin derivatives. A fibrous connective tissue layer lies between the tapetum and the retina. The subretinal capillary network, the choriocapillaris, rests on this layer and is covered by the basement membrane of the retinal epithelium. The cytoplasm of the retinal epithelium exhibits marked absorptive modifications where it comes in contact with the vessels of the choriocapillaris. This fibrous layer and the basement membrane of the retinal epithelium apparently comprise the structural elements of Bruch's membrane.     

Rhythmic daily shedding of outer-segment membranes by visual cells in the goldfish

Goldfish were placed on a daily light cycle of 12 h light and 12 h darkness for 18 days or longer. The visual cells and pigment epithelium of the retina were then examined by microscopy at many intervals throughout the cycle. Goldfish rods and cones follow a rhythmic pattern in eliminating packets of photosensitive membranes from their outer segments. Rods shed membranes early in the light period. The detached membranes are ingested by pigment epithelial cells or by ameboid phagocytes, which degrade them during the remainder of the light period. Cones discard membranes from the ends of their outer segments early in the dark period. During the next several hours, this debris is digested by the pigment epithelium or by ameboid phagocytes. Thus, the disposal phase of the outer-segment renewal process is similar in rods and cones, but is displaced in time by about 12 h. There is evidence that this daily rhythm of membrane disposal in rods and cones is a general property of vertebrate visual cells.     

Electron Microscopy of the Tapetum Lucidum of the Cat

The fine structure of the tapetum of the cat eye has been investigated by electron microscopy. The tapetum is made up of modified choroidal cells, seen as polygonal plates grouped around penetrating blood vessels which terminate in the anastomosing capillary network of the choriocapillaris. The tapetal cells are rectangular in cross-section, set in regular brick-like rows, and attain a depth of some thirty-five cell layers in the central region. This number is gradually reduced peripherally, and is replaced at the margin of the tapetum by normal choroidal tissue. The individual cells are packed with long slender rods 0.1 µ by 4 to 5 µ. The rods are packed in groups and with their long axes oriented roughly parallel to the plane of the retinal surface. Each cell contains several such groups. Cells at the periphery or in the outer layers of the tapetum are frequently seen to contain both tapetal rods and melanin granules, the latter typical of the choroidal melanocytes. Also melanocyte granules may have intermediate shapes. These observations plus the similar density of the two inclusions lead to the belief that the tapetal rods may be melanin derivatives. A fibrous connective tissue layer lies between the tapetum and the retina. The subretinal capillary network, the choriocapillaris, rests on this layer and is covered by the basement membrane of the retinal epithelium. The cytoplasm of the retinal epithelium exhibits marked absorptive modifications where it comes in contact with the vessels of the choriocapillaris. This fibrous layer and the basement membrane of the retinal epithelium apparently comprise the structural elements of Bruch's membrane.     

'Yellow lens' eyes of a stomiatoid deep-sea fish, Malacosteus niger

Bright yellow lenses were found in the eyes of the stomiatoid deep-sea fish, Malacosteus niger Ayres. The optical properties of the yellow lens and the retinal specializations in the eyes were examined. Absorption spectra of the yellow lens revealed two peaks at wavelengths 425 and 460 nm. The photoreceptors were all rods and were arranged in two superimposed layers. An astaxanthin-type retinal tapetum was observed in the pigment epithelium. Some chemical evidence is presented showing that the tapetal material is an astaxanthin ester. The ecological significance of the yellow lens is discussed in connection with that of Malacosteus' orbital light organ which has a reddish filter.     

Fine structure of the retinal epithelium and tapetum lucidum of the opossum (didelphis virginiana)

The fine structure of the retinal epithelium has been studied by electron microscopy in the opossum (Didelphis virginiana). The retinal epithelium, over most of the retina, is typical of that in other vertebrates and consists of a single layer of heavily pigmented, cuboidal cells. These cells display extensive basal (scleral) infoldings and numerous apical (vitreal) processes which enclose photoreceptor outer segments. A semicircular area of the retinal epithelium in the superior fundus is further specialized as a tapetum lucidum. The reflecting material consists of a large quantity of lipoidal spheres scattered throughout the epithelial cells. Centrally in the tapetal area very few or no melanosomes are found, indicating a non-occlusible tapetum. Peripherally in the tapetum, the epithelial cells contain both reflecting material and melanosomes. As in the non-tapetal area, the epithelial cells of the tapetum display large amounts of smooth endoplasmic reticulum and numerous mitochondria. Bruch's membrane everywhere displays the usual pentalaminate structure described for most vertebrates. The choriocapillaris is also typical, in that numerous fenestrations are present in the endothelium bordering Bruch's membrane.     

Guanine-type retinal tapetum and ganglion cell topography in the retina of a carangid fish, Kaiwarinus equula.

A guanine-type retinal tapetum was recorded in the eyes of a carangid fish Kaiwarinus equula (= Carangoides equula), spectrophotometric evidence of such being presented. The total amount of guanine in one eye was about 6.5 mg, the guanine density being ca. 1.3 mg cm(-2) over the retinal surface area. To examine the guanine distribution within the retina, the latter was divided into 21 regions. An area of high guanine density (more than 2.0 mg cm(-2)) was observed in the dorsal fundus of the retina, suggesting that the most sensitive vision was checked downward. Using whole-mount retinal preparations, the distribution of Nissl-stained cells within the retinal ganglion cell layer was examined. The greatest cell density area (area centralis) was observed only in the temporal retina. The visual acuity of the area centralis was 4.3 cycles deg(-1), suggesting that high resolution and binocular vision were directed frontally in this species. The eyes of a related carangid (Pseudocaranx dentex), lacking a tapetum, were also examined for comparison. The possible ecological advantage resulting from the tapetum is discussed in terms of visual threshold.     

Melanopsin and mechanisms of non-visual ocular photoreception

In addition to rods and cones, the mammalian eye contains a third class of photoreceptor, the intrinsically photosensitive retinal ganglion cell (ipRGC). ipRGCs are heterogeneous irradiance-encoding neurons that primarily project to non-visual areas of the brain. Characteristics of ipRGC light responses differ significantly from those of rod and cone responses, including depolarization to light, slow on- and off-latencies, and relatively low light sensitivity. All ipRGCs use melanopsin (Opn4) as their photopigment. Melanopsin resembles invertebrate rhabdomeric photopigments more than vertebrate ciliary pigments and uses a G(q) signaling pathway, in contrast to the G(t) pathway used by rods and cones. ipRGCs can recycle chromophore in the absence of the retinal pigment epithelium and are highly resistant to vitamin A depletion. This suggests that melanopsin employs a bistable sequential photon absorption mechanism typical of rhabdomeric opsins.     

Development of amelanotic retinal pigment epithelium in eyes with a tapetum lacidum: melanosome autophagy and termination of melanogenesis

Bovine eyes of embryos and fetuses were examined to determine the developmental processes involved in establishment of the amelanotic retinal pigment epithelium (RPE) which overlies the tapetum lucidum. Melanogenesis was detectable at the optic vesicle stage (Day 28); premelanosomes were visible by electron microscopy in neuroepithelium temporal to the lens placode. Pigmentation of the eye was visible by light microscopy at the optic cup stage (about Day 30) and spread from the lip of the optic cup throughout the entire fundus by the 40th day. Thereafter, pigmentation of the superior temporal fundus diminished and by the 65th day the adult pattern of amelanotic and melanotic RPE was established. Calculations showed that after the 40th day, growth of the eyeball brought about a 16-fold dilution of those melanosomes which had been synthesized by RPE cells of the presumptive amelanotic zone during the initial wave of pigmentation. Enzyme cytochemical studies showed that the remaining melanosomes became sequestered in autophagic vacuoles. Also, individual premelanosomes of these RPE cells became positive for acid phosphatase and aryl sulfatase. The contents of these autophagosomes were later consolidated into a single macromelanosome which was present in adult eyes and was generally positive for acid hydrolases. In contrast, melanosomes of melanotic areas of RPE were negative for acid hydrolases. Thus, the RPE overlying the tapetum lucidum becomes amelanotic by at least three processes: (1) premature termination of melanogenesis, (2) dilution of preexisting melanosomes, and (3) autophagic digestion (melanolysis) and centralization of the residua of preexisting premelanosomes and melanosomes into a macromelanosome.     

The retinal pigment epithelium and photoreceptor cells light-and electron microscopic studies on monkey eyes

Summary In the perifoveal retina of the monkey, Cercopithecus aethiops, the melanin granules are accumulated in apical cytoplasmatic protrusions of the pigment epithelial cells, facing the end of the cones. The rods are inserted deeper into the pigment epithelium than the cones; they reach the bottom of the infoldings of the apical surface membrane of the pigment epithelial cells. No melanin granules or other inclusions are situated at the end of the rods. The outer extremity of the rods is considerably inclined and in sections often appears as groups of rod discs which are incompletely or completely separated from the main part of the outer segments. This separation is regarded as an artifact caused by the inclination of the rods, and it is therefore not considered to represent phagocytosis of the outer segments by the pigment epithelium.The inclusions of the pigment epithelial cells are classified in five categories which seem to be related to each other owing to their shared structural characteristics. It is suggested that melanin granules are produced, modified and destroyed by the pigment epithelial cells of the adult.Because of the relations between the photoreceptors and the melanin granules it is suggested that light scattered by the melanin granules may pass backwards through the outer segments of the cones, but not of the rods.This investigation was supported in part by the Danish Foundation for the Advancement of Science and by the Danish Medical Research Council.