www.ivis.org Proceeding of the SEVC Southern European Veterinary Conference Oct. 17-19, 2008 Barcelona, Spain http://www.sevc.info Reprinted in the IVIS website with the permission of the SEVC www.ivis.org
Other Companion Animals Evaluating the Reptilian Eye Dr.D.Mader Marathon Veterinary Hospital, USA Abnormalities and pathology of the orbit and adnexa are commonplace in reptile patients. Evaluating the reptilian eye for pathology requires a knowledge of the normal anatomy. The myriad of species encountered, with tremendous diversity in the types of visual systems, can make diagnosis and treatment of these problems complex. Thus, it is imperative to know the normal before abnormal conditions can be identified and corrected. General Features of the Reptilian Eye The eye develops in all vertebrates as a composite of structures. The eyeball or globe sits within its orbit. The two orbits are separated from one another by a cartilaginous interorbital septum in lizards, crocodilians and turtles or by bone (frontal, parietal, and parasphenoid bones) in snakes. The eye is organized by layers making up its wall, the lens, and the vitreous body centrally (vitreous chamber). The eyeball s outer layer is the sclera (a fibrous outer capsule to which extrinsic eye muscles attach). The inner portion may be supported by cartilage in turtles and lizards and outwardly by a ring of small bony plates, the scleral ossicles. Snakes lack scleral ossicles and cartilage in the eye wall6 and crocodilians have a cartilaginous layer within the sclera. The middle layers of the eye are collectively the uvea and include the choroid (a nutritive layer), the tapetum lucidum, a reflective material in the choroid (most fully developed in animals that live in low light conditions or those which are nocturnal), the ciliary body and the iris. The iris is controlled by smooth muscles in most vertebrates. However in reptiles it is striated muscle that controls the iris. This is significant since common topically applied mydriatics will not work to dilate the pupils of a reptile. The inner layer of the eye is the retina, organized in three layers, the photosensitive cells (rods and cones), interneurons (horizontal and bipolar cells) and a layer of ganglion cells and amacrine cells1,2,3. The photosensitive cells are rods and cones. Rods detect light at low levels but not color. Cones detect colors and are active in bright light. Turtles have rods and cones. Crocodilians have retinas formed of both rods and cones (however there are more rods). Nocturnal lizards and snakes have rods and cones (the latter may be secondarily derived from rods)6,7. Diurnal lizards have all-cone retinae2. Most, if not all, diurnal reptiles can see color. The peak sensitivity to colors varies with species, and sometimes with age. However, behavioral assays indicate whether color is perceived. Lizards have one or two foveas (concavities in the retinal wall housing areas of concentrated cones that provide greater acuity)6. Turtles and snakes lack foveas. Turtles have areas (e.g. area centralis, or area temporalis) or visual streaks which are sections of the retinae that are especially sensitive to detail, edges, or movement. Areas may achieve sensitivity through increased numbers of cones, rods, or ganglion cells. Snakes supplement vision with acute chemical sensitivity and, in some cases infrared radiation detection3. In the optic disk is the region in the retina of the eye where nerve fibers from the retina exit to become part of the optic nerve. Arising from the optic disk is a papillary cone (conus papillaris) that extends into the vitreous body. It is often melanic and highly vascular. It is believed to function in providing supplementary nutrition to deep ocular tissues. It is present in lizards, many snakes, and crocodilians, but not in chelonians4,6.
Eye Movement and Extrinsic Eye Muscles Turtles, crocodilians, and most lizards (except Heloderma) have mobile eyes. Snakes do not6. Six extrinsic eye muscles (Table 1) insert on the outside of the eye and move it within the orbit. The extrinsic eye muscles are characterized by fine movement control. Table 1. Extrinsic eye muscles, their innervations and actions3,6. The innervations are conservative. Because of speciesspecific differences in muscle insertion position, these actions are given in the most general terms. There are retractor oculi and protractor oculi (= levator bulbi) muscles inserting on the sclera adjacent to the optic nerve that move the eye inward and outward within the socket. These are weakly developed in crocodilians and many lizards with akinetic skulls (those lacking hinged snouts and/or hinged braincases). They tend to be strongly developed lizards with kinetic skulls (those having hinged braincase and/or snout), as well as in chameleons, most chelonians and in snakes. Innervation is by Cranial Nerve VI (CN VI) (abducens), and possibly CN VII (facial). Intrinsic Muscles Pupil diameter (pupillary reflex) is controlled by the oculomotor nerve (CN III). The pupillary sphincter is formed from striated muscle or a combination of smooth and striated muscle in reptiles (as in some birds, e.g. chickens). This arrangement differs from the purely smooth muscle sphincter found in mammals. Striated ciliary muscles shape the lens and cornea in most reptiles, except in snakes. These muscles are innervated by CN VI and, in some cases, CN VII. Pupils Pupil shape differs among reptilian taxa and with various behaviors. While turtles and many colubrid snakes tend to have round pupils, many nocturnal hunters such as geckos tend to have slits or indented slits. Snakes may have slit or round pupils. The crocodilian pupil is a vertical slit. Diurnal lizards usually have round pupils. The shape of the pupil can have a profound effect on the retinal image because pupil shape can influence the characteristics of light reaching the retina6,7. Glands Lizards generally have three orbital glands which may be compact or have extended portions. Most lizards have well-developed lacrimal glands posterior, dorsal and ventral to the eye (absent in chameleons, calotes, some geckos, and Australian snake-lizards). Harderian glands anterior to each eyeball drain via a duct onto the inner surface of the nictitating membrane. The Harderian ducts extend from the lower lid and empty into the palate. A small mucous gland (sometimes termed the conjunctival gland) opens onto the outer surface of the nictitating membrane.
Snakes have well-developed Harderian glands, which lubricate the spaces between the spectacle and the cornea. A second duct drains this fluid into the Jacobson s organ in the dorsal region of the oral cavity. Harderian glands are located dorsally and nasally. In turtles, lacrimal glands vary in size with taxon. They are very large in marine turtles but small in freshwater species. There is a single lacrimal duct in turtles located posterior to the globe. The Harderian gland is present dorsally and nasally in all turtles. Crocodilians have three kinds of glands associated with the eye: lacrimal, Harderian, and conjunctival glands5. The lacrimal gland is an elongated gland that is small relative to the eyeball size and located dorsally within the orbit. The Harderian gland is large, triangular and located anterior and medial to the eye. This gland secretes lubricating fluid via two ducts that drain between the nictitating membrane and the eye. The conjunctival gland is located at the junction of the conjunctiva and the eyeball within the lower lid. It is presumed to be a lubricating gland as well. Lids Generally, the upper lid has mostly smooth muscle and is less mobile than the lower lid with striated muscle. Both upper and lower eyelids are present in lizards (in most cases), all turtles, and crocodilians. The lower lid of lizards contains a cartilaginous support. In crocodilians, the opposite is the case; the upper lid, containing a bony plate, closes the eye5; the lower lid lacks bone or cartilage and moves little. The borders of the upper and lower lids are often rich in goblet cells (secretory7). Reptilian eyelids cover a poorly cornified nictitating membrane along the nasal surface of the eye; the nictitating membrane is a cartilage-supported extension of the conjunctiva. Nictitating membranes are highly developed in crocodilians and turtles. The nictitating membrane, which may be pigmented, is usually largest toward the medial (nasal) part of the eye8. Depending upon species, it may cover all or part of the eye. Lizards generally lack nictitating membranes. Eyelids are modified in a number of species so that they are partially fused, as in chameleons, or reduced as in geckos and snakes. While most lizards have eyelids, most geckos and Australian snake lizards appear to lack them. The cornea is covered by a spectacle formed by fusion of the upper and lower lids. Chameleons have partially fused upper and lower lids and are reported to lack a nictitating membrane. Some skinks, lacertid, and iguanine lizards have a transparent lower eyelid. Snakes lack eyelids and nictitating membranes. The cornea is covered by a transparent spectacle, which is derived from eyelids6. The spectacle does not move and its outer layer is shed with the skin3. For a comprehensive review of reptilian clinical ophthalmology see Lawton.9 Literature Cited 1. Grüninger, H. 2002. Microscopic-anatomical and morphometrical studies in reptilian eyes veterinary thesis. Universität Munich, Germany 2. Kawamura, S. and S. Yokoyama. 1997. Expression of visual and nonvisual opsins in American chameleon. Vision Res. 1997 36:2797-2804. 3. Kardong, K. V. 2002. Vertebrates: Comparative Anatomy, Function, Evolution. WCB/McGraw-Hill, Boston. 747 pp. 4. Reese, S. and H.-G. Liebich. 2002. Zur Ultrastruktur des Kapillarendothels im Pecten oculi von Vögeln. Institut für Tieranatomie I, Ludwig-Maximialians- Universität Munich, Germany. 5. Reese, A. M. 1915. The Alligator and Its Allies. G. P. Putnam and Sons, New York and London (The Knickerbocker Press). 229 pp. 6. Underwood, G. 1970. The eye. Pp. 1-97. In. C. Gans and T. Parsons, eds. The Biology of the Reptilia. Vol. 2. Morphology B. Academic Press. New York. 274 pp.
7. Walls, G. L. 1942. The Vertebrate Eye and its Adaptive Radiation. Cranbrook Institute of Science, Bloomfield Hills, Mich 785 pp. 8. Wyneken, J. 2001. The Anatomy of Sea Turtles. U.S. Department of Commerce NOAA Technical Memorandum NMFS-SEFSC-470, 172 pp. 9. Lawton, MPC. Reptilian Ophthalmology. In Mader DR. Reptile Medicine and Surgery. Elsevier. St. Louis, MO. 323-342.2006.