Characteristics of the ocular fundus in primates

Transcription

1 J. Anat. (1967), 101, 4, pp 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 interested 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 manipulates 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 1 1). 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 outlined 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-

2 694 LEE R. WOLIN AND L. C. MASSOPUST

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4 696 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 distribution 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 appearance (see Figs ). 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.

5 Ocular fundus in primates 697 the darker pigments appearing in the more central portion of the retina. The periphery 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 number 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 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. Fig. 12. Slow loris (Nycticebus). This is the most highly reflective of the primate retinae shown. Use of neutral density filters in order to photograph the major portion of the retina produced blacking out of the optic nerve head. Note small size of nerve head and relatively large distance between nerve head and central retinal area (as defined by terminal pattern of blood vessels). Fig. 13. Lemur (Lemur fulvis). One of the more darkly pigmented retinae among the nocturnal species, this retina has an extremely 'mottled' appearance. Dense accumulation of pigment may be noted just below the nerve head. The periphery of this retina (not shown in plate is) almost black due to the density of the pigment. Fig Tree shrew (Tupaia glis). These three photographs survey the retina from nasal to temporal extremes. Unlike any other eye which we have observed, the vessels radiate in spokelike fashion from the nerve head. Veins and arteries alternate except in the temporal direction where it appears that three arteries extend toward the central visual portion of the retina. Fig. 15 was photographed directly through the centre of the pupil along the apparent optical axis of the eye. Fig. 14 was taken with the camera directed approximately thirty degrees in a nasal direction, while Fig. 16 required an orientation of more than forty-five degrees toward the posterior (temporal) portion of the eye. It is in the posterior part of the retina that an area having the appearance of a central visual area is observed.

6 698 LEE R. WOLIN AND L. C. MASSOPUST The retina of the tarsier has been described by Polyak (1957) as a pure rod retina but showing a clearly defined macula. In this latter respect it differs from all other nocturnal species examined. We have not yet obtained a tarsier eye and so have not determined whether the tarsier has a tapetum lucidum (Polyak does not mention this) but it was apparent while doing the photography that the retina was highly reflective, more reflective than that of any of the diurnal species examined, but less reflective than many of the nocturnal species. Aotes also have a 'fovea' in histological section (Polyak, 1957) but this cannot be seen ophthalmoscopically. Aotes, like the tarsier, have an all rod retina. The aotus, loris, lemur, bushbaby, and galago all show a slightly shadowed central area when viewed under dim illumination, but no macular ring reflex or foveal spot reflex can be elicited. The tree shrew which is reported to have a pure cone retina rather than a pure rod or duplex retina, deviates considerably from the two patterns described above (Figs ). It has been described whether this species should or should not be classified as a primate (Campbell, 1966; Goodman, 1966; Martin, 1966; McKenna, 1966; Van Valen, 1965). It has the appearance of an insectivore with a long narrow snout and with the eyes set in a lateral orientation. The optic disc is located such that if one looks directly into the eye along the optical axis the disc is in the anterior portion of the field (anterior and posterior here refer to the nasal and occipital directions along the median sagittal plane of the head) (Fig. 15). The vessels radiate in a spoke-like fashion (Fig. 14) rather than predominantly vertically as in the other species. The several arteries (three in Figs. 14 and 15) projecting in the posterior direction are somewhat smaller than the others and seem to terminate just anterior to what is probably the 'central retinal area' (Fig. 16). This area is located far in the posterior portion of the eye and, while it appears largely free of blood vessels, shows no evidence of a macula or fovea. The tree shrew looks 'straight ahead' at an object (Sanderson, 1963; author's observation) rather than cocking the head to one side, thus indicating that the central retinal area is in fact in the posterior portion of the eye and that the tree shrew probably employs binocular visual fixation. The controversy concerning the classification of the tree shrew must undoubtedly be based upon a number of considerations. The morphology of the eye of the animal is certainly unlike that of any other primate we have observed. This would be another factor in support of the classification of tree shrews as a separate order of mammals (Martin, 1966; McKenna, 1966; Van Valen, 1965). SUMMARY This report presents colour illustrations of the ocular fundus of fourteen primate species spanning the Order Primates. Both nocturnal and diurnal species are represented. Similarities and differences in the appearance of the fundi, particularly pigment variations, vascular patterns, and the appearance of a macula and fovea are noted. Supported in part by grant FR from the National Institutes of Health. We express our appreciation to Wallace Wendt, D.V.M. for his assistance with

7 Ocular jundus in primates 699 anaesthesia and photography; to L. J. Goss, D.V.M., Ph.D. and Mr R. T. Reuther of the Cleveland Zoological Society for making available to us the colobus monkey; to Dr William Montagna, Director of the Oregon Regional Primate Research centre, and to the many staff members who were most helpful in assisting with the examination of a variety of prosimian species and with the photography of the fundus of the tarsier and lemur; and to Dr Kenneth Swan of the University of Oregon Medical School for making available to us the facilities of the Eye Clinic. REFERENCES CAMPBELL, C. B. G. (1966). Taxonomic status of tree shrews. Science N.Y. 153, 436. GOODMAN, M. (1966). Phyletic position of tree shrews. Science N.Y. 153, JOHNSON, G. L. (1901). Contributions to the comparative anatomy of the mammalian eye, chiefly based on opthalmoscopic examination. Phil. Trans. R. Soc. B, 194, MARTIN, R. D. (1966). Tree shrews: unique reproductive mechanism of systematic importance. Science N. Y. 152, MCKENNA, M. C. (1966). Paleontology and the origin of the primates. Folia primatol. 4, ORDY, J. M., MAssOPUST, L. C., JR. & WOLIN, L. R. (1962). Postnatal development of the retina, electroretinogram, and acuity in the rhesus monkey. Expl Neurol. 5, POLYAK, S. (1957). The Vertebrate Visual System. Ed. H. Kluver. Chicago: University of Chicago Press. SAMORAJSKI, T., ORDY, J. M. & KEEFE, J. R. (1966). Structural organization of the retina in the tree shrew (Tupaia glis). J. Cell Biol. 28, SANDERSON, 1. T. (1963). The Monkey Kingdom. Philadelphia: Chilton Books. SIMPSON, G. G. (1945). The principles of classification and a classification of mammals. Bull. Am. Mus. nat. hist. 85, New York. SMITH, J. L., REYNOLDS, D. H., RANE, L. & JUSTICE, J., JR. (1964). The fundus oculi in the squirrel, owl and marmoset monkey. Am. J. Ophthal. 57, VAN VALEN, L. (1965). Tree shrews, primates, and fossils. Evolution 19,