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Characteristics of the Ocular Fundus in Primates

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Characteristics of the Ocular Fundus in Primates J. Anat. (1967), 101, 4, pp. 693-699 693 With 16 figures Printed in Great Britain Characteristics of the ocular fundus in primates LEE R. WOLIN AND L. C. MASSOPUST, JR. Laboratory of Neurophysiology, Cleveland Psychiatric Institute, Cleveland, Ohio In recent years we have seen a marked increase in research on the visual system. The last few years in particular have been characterized by an increasing use of primates for vision research. As an aspect of comparative research on the visual system, we have been in- terested in variations of the gross morphology of the retina (Ordy, Massopust & Wolin, 1962). We take routine ocular fundus photographs of each species of animal used. Since we have been able to assemble a collection of fundus photographs of a reasonably representative selection of primates (based on Simpson's Classification, 1945) we felt this would be of interest, as only a limited selection of primate retinal fundus photographs is readily accessible in the literature (Ordy, et al., 1962; Samorajski, Ordy & Keefe, 1966; Smith, Reynolds, Rane & Justice, 1964). The fundus photography is a relatively simple procedure. The pupil is dilated with cyclopentolate hydrochloride (Cyclogyl), following which the animal is anaesthetized, usually with thiamylal sodium (Suritol). The photographs are taken with a Zeiss fundus camera on Kodachrome II film. Species having a highly reflective retina and possibly a tapetum lucidum require insertion of a neutral density filter in the optical path of the camera. Two persons are required for the procedure, one to hold the subject's head and maintain proper orientation of the eye, while the second person mani- pulates the camera. The fundi of primates follow two basic patterns, one showing a clearly defined macular area and fovea and the other a less well-defined central area with no clear macula or fovea (see figures). The tree shrew (Tupaia) which has a controversial taxonomic status does not fit either pattern. Species including New and Old World, monkeys, gibbon and man, and in addition the tarsier, all show the first patterns (Figs. 1-9 and 11). Nerve fibres and blood vessels originating in a circular or oval optic disc (nerve head or papilla) converge on the central area of a retina containing a well-defined macula. The macula is largely free of vessels, differs slightly in pigmentation from the surrounding retina, and is out- lined by a ring light reflex. The foveal depression is readily visualized and often shows a spot reflex with bright light and a deep focus. The choroidal vessels can often be seen. There is considerable variation in the vascular patterns within species and a difference between the representatives of the various species shown here should not be regarded as species specific. The general pattern of arcuate vessels with branches terminating near the macula or central retinal area is characteristic of all primates. According to Johnson (1901) this vascular pattern is also found in many carnivores. Certainly the cat fundus is quite similar in appearance to that of the loris (Fig. 12). The predominantly horizontal orientation of the arterioles in Fig. 1 and the pre- 694 LEE R. WOLIN AND L. C. MASSOPUST Ocular fundus in primates 695 .X- japmo T At -a.. Ho i.s _ .-.M.-.- .S, j.-- -; / A: ....A....0...e..qs__rST_.s- | 696 LEE R. WOLIN AND L. C. MASSOPUST dominantly vertical orientation of the venules in Fig. 3 are strictly individual patterns. Individual variations in pigmentation, within species, are also found. Except in man, coloration of the retina (as viewed and photographed with the Zeiss light sources) in the higher species is from green to greenish blue with the pigment being relatively uniformly distributed over the retina (Figs. 2-9). The area near the macula is close to natural colour in each figure, while the bright blue appearing in Fig. 5, and the purple in Figs. 7, 8 and 15 is artifactual. The major differences to be noted among these species are: size and regularity of the border of macular area, size and shape of the optic disc, apparent 'texturing' of retina, and pigmentation of retina. Species including the aotes, lemurs, lorises and tree shrews (the tarsier being the exception) show a somewhat different appearance (Figs. 10, 12-16). The optic disc and vascular distribution are similar to those in the higher species and the distribu- tion and termination of the arteries and veins define the central retinal area. There is, however, no defined macula or fovea. In some instances (see Fig. 10) there is a shadowing indicative of a slight depression over a broad central area; however, no pigment difference is noticeable nor can any ring reflex be obtained. In those animals apparently having a tapetum, the retina has a spotted and sometimes mosaic ap- pearance (see Figs. 10-13). Such a highly reflecting retina sometimes makes it difficult to photograph the retina, vasculature and nerve head simultaneously, whilst the choroidal vessels are completely obscured (Fig. 12). The retina in these species varies in colour from orange through yellow to greenish yellow, with little of Fig. 1. Man (Homo sapiens). Lightly pigmented (blond) subject. Note light pigmentation of retina, large round nerve head, large slightly oval macula, smooth appearance of retinal surface and termination of vessels outside fovea centralis. Fig. 2. Gibbon (Hylobates lar). Quite similar in appearance to human fundus, nerve head is slightly obscured to higher reflectivity, macula rounder in shape, and generally darker pigmentation of retina. Fig. 3. Baboon (Papio hamadryas). Although the general characteristics are again close to those of human, note deeper (green) pigmentation and slightly textured appearance of retinal surface. Fig. 4. Rhesus monkey (Macaca mulatta). The oval shape of nerve head distinguishes this retina from those preceding. Fig. 5. Patas monkey (Erythrocebus patas). Very much like rhesus fundus. Deep pigmentation made macular ring reflex difficult to obtain although part of it is seen and outline of macular area is easy to determine. Horizontal striations are due to separation of nerve fibres coursing toward optic nerve. This is seen in individuals of many species and has on at least one occasion been misinterpreted as a speciescharacteristic and described as outlining the shape and extent of the macular area. Light coloured (pink) lines are choroidal vessels. Bright blue area at top is photographic artifact. Fig. 6. Colobus monkey (Colobus polykomos). Characteristic higher primate retina. Note relatively lighter pigmentation which in part permitted photography of extremely well defined macular ring reflex. Macular area is quite regular and nerve head is round as in human. Fig. 7. Marmoset (Oedipomidas oedipus). This eye was the smallest (and most difficult to photograph) of all the primate eyes. Macula is determinable by deeper pigmentation although we were unable to photograph, even in part, a ring reflex. The macular and foveal reflexes can however be obtained with an ophthalmoscope. Fig. 8. Cebus monkey (Cebus albifrons). Note relatively large well-defined macular area. Retina shows some texturing which in this photograph is shown by the irregular character of the ring reflex. The purplish haze is an external reflection artefact. Ocular fundus in primates 697 the darker pigments appearing in the more central portion of the retina. The peri- phery of the retina near the ora serrata or ora terminalis has a dense accumulation of melanin sometimes giving an appearance similar to that of retinitis pigmentosa in man. One of the authors (L. R. W.) had the opportunity to examine the fundi of a num- ber of prosimian species not represented here. Some differences in appearance of vasculature, pigmentation and reflectivity of the retina were observed, but all appeared to fall within the range of variation represented in Figs. 10-13. The tarsier is of particular interest as it is the only prosimian in which we have been able to see and photograph a 'macula'. Johnson (1901) states that, "...in Simiae the macula is invariably present, whilst in the Prosimiae it is entirely wanting....' Polyak (1957), on the other hand, refers to the '. central fovea and area of the Night Monkey...', a simian, while describing a '...well-developed yellow spot or "macula" temporal to the disk...' in tarsier, a prosimian. This species has been described as nocturnal in behaviour and certainly has the gross characteristics of a nocturnal animal. The eyes are quite large in proportion to the head. The pupils when fully dilated are almost as large as the visible portion of the eye. The pupil when contracted is elongated rather than round but, in contrast to other nocturnal species observed, the elongation of the tarsier pupil is horizontal rather than vertical. Fig. 9. Squirrel monkey (Saimiri sciureus). This fundus also shows a large macula. 'Texturing' also is apparent not only at the ring reflex but over a much larger area. Blue pigmentation of retina is 'true' colour in this species. Note also extensive appearance of choroidal vessels. Fig. 10. Owl monkey (Aotus trivirgatus). This is the first nocturnal species represented, but is more closely related to Cebus and Saimiri than to other nocturnal species. No macula or fovea can be grossly visualized though a 'foveal' area is found in histological section. Note 'spotted' appearance of retina, which is found in most nocturnal species. Fig. 11. Tarsier (Tarsius syrichta). Highest of the prosiminians here represented. This eye is unique among nocturnal species in revealing a macular ring reflex and foveal spot (the photograph barely does justice to these features which are most distinctly seen with an ophthalmoscope). Note the relatively small nerve head and complex intertwining of vessels as they emerge. The beginning of dense peripheral deposits of pigment can be seen in the temporal and inferior portions of the photograph.
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