Reports 587. Vascularity in the reptilian spectacle. AL- REFERENCES
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1 Volume 15 Number 7 Reports 587 sensitivity curve for ms. flashes on a white background may be a rather precise indicator of the functioning of the opponent-color system. 7 Thus, although J. T. believed that his right eye was normal, the corresponding spectral sensitivity curve (continuous curve, Fig. 3) lies near the limit of the normal range, indicating that his right eye may have been partially affected by a similar defect. There is no evidence for any response from the blue-sensitive cones of J. T.'s left eye and, in this respect, the subject's defect may be classified as a tritan type. However, it may also be possible to interpret this finding in terms of a general loss of opponent-color function, since it is thought that the blue cones signal mainly through the opponent-color system. IJ The opponent-color cells in the primate retina have axons with lower conduction velocities than the luminance cells 10 and it is thus likely that the opponent-color axons are relatively fine. For this reason, it is possible that the proposed defect of the subject's opponent-color system may be related to selective loss or damage to small fibers or neurons. From the Ophthalmic Optics Department, UMIST, Manchester, England. This work was supported by a grant from the Royal Society and by S.R.C. research grant B/RG/ Submitted for publication Oct. 8, Reprint requests: Dr. P. E. King-Smith, Ophthalmic Optics Department, UMIST, P.O. Box 88, Manchester, M60 1QD, England. Key words: acquired color defect, opponent-color and luminance systems, cone mechanisms, spectral sensitivity, photopic luminosity. REFERENCES 1. Grutzner, P.: Acquired color vision defects, In Jameson, D., and Hurvich, L. M., editors: Handbook of Sensory Physiology, Berlin, 1972, Springer-Verlag, vol. VII/4, p Hurvich, L. M., and Jameson, D.: An opponent-process theory of color vision, Psychol. Rev. 64: 384, Gouras, P.: Identification of cone mechanisms in monkey ganglion cells, J. Physiol. (Lond.) 199: 533, Stiles, W. S.: Colour vision: The approach through increment threshold sensitivity, Proc. Natl. Acad. Sci. 45: 100, Mane, M.: Versuch einer quantitativen Analyse erworbener Farbsehenstorungen. Wiener Ophthal. Ges. (Wien) 14: April, De Lange, L. S.: Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light. II. Phase shift in brightness and delay in colour perception, J. Opt. Soc. Am. 48: 784, King-Smith, P. E.: Visual detection analysed in terms of luminance and chromatic signals, Nature 255: 69, Bender, B. G., and Ruddock, K. H.: The characteristics of a visual defect associated with abnormal responses to both colour and luminance, Vision Res. 14: 383, Cuth, L. S., Donley, N. J., and Marroco, R. T.: On luminance additivity and related topics, Vision Res. 9: 537, Gouras, P.: Antidromic responses of orthodromically identified ganglion cells in the monkey retina, J. Physiol. 204: 407, Vascularity in the reptilian spectacle. AL- DEN W. MEAD. Vascnlarization of the spectacle or brille of the reptile was demonstrated by biomicroscopy, histology, fluorescein (in vivo), and Microfl silicone rubber (in situ) injections. This unusual vascularity provides new evidence for reassessment of the origin and development of this structure, and a useful tool with which to do so. All snakes and those lizards without eyelids possess a permanent immovable transparent membrane totally covering the exposed anterior portion of the eye. This structure is the reptilian spectacle or brille. 1-3 This structure is thought to have evolved from either fusion of the eyelids, 2 ' i < 5 or less popularly the nictitating membrane. 3 The primary purpose of the spectacle is protection. The study of the reptilian spectacle as an indication of the evolution of the reptilian eye and possibly the evolution of the reptile itself has been a subject of extensive discussion and investigation in the scientific literature, most especially in the field of visual science. 6 " 9 Review of the literature by this investigator as well as a personal communication with Duke-Elder 10 has failed to uncover evidence of previous observation of the vascularity of this structure in the English literature and mention by only one investigator in the German. 11 The purpose of this report is to present clearly demonstrated evidence of the vascularity of the reptilian spectacle. The study of this vascularity is suggested as a basis for re-evaluating previous information concerning the evolution of the reptilian spectacle and offer this evidence as a tool for further investigation of variations in this structure. Materials and methods. Twenty-four reptiles, representing seven of the major families of snakes and two of the spectacle bearing lizard families were studied (Table I). Animals were anesthetized with sodium pentobarbital 25 mg. per kilogram intraperitoneally. Biomicroscopic examination was done with a Haag Streit slit lamp on all animals. Two animals of each species were in-
2 588 Reports Investigative Ophthalmology July 1976 Table I. Description and number of species examined Boidae Family Xenopellidae Acrochordidae A niliidae Elapidae Viperidae Colubridae Gekonidae Xantusidae Species (scientific name) Python molurus Python reticulata Boa constrictor Xenopeltus unicolor A crochordus javanicus Cylindrophis rufus Naja naja kauothia Agkistrodon contortrix mokasen Crotalus viridis helleri Bitis nasicornis Natrix sipedon sipedon Thamnophis siritalis siritalis Leptodeira annulatta Gecko gecko Klauberina riversiana Species (common name and number) Indian python Reticulated python Boa constrictor Sunbeam snake Java wart snake Malayan pipe snake Siamese cobra Northern copperhead Pacific rattlesnake African rhinoceros viper Northern water snake Eastern garter snake Cat-eyed snake Gecko lizard Island night lizard (4) (4) jected with microsilicone (Microfil) through the common carotid artery or its analogous structure. To allow complete perfusion of the ocular structures a suitable vein was opened for drainage. Two animals each of two species of snakes were examined by fluorescein angiography and histologically by light microscopy. Horizontal and vertical sections of whole decalcified heads were made for histological examinations. Results. Microsilicone injections clearly demonstrate the vascularity of the spectacle. The microarchitectural configuration of these vessels seems to be species-dependent. There are clearly definable pattern distinctions between major families (Figs. 1 through 4). Fluorescein angiography demonstrates the same evidence and shows the vessels to fill without any obvious directional priority in the anesthetized animal. By biomicroscopy, these vessels are seen to traverse the middle or stromal layer of the spectacle. This is interesting since this layer is not replaced during normal reptilian shedding of the skin. Visualization with the slit lamp is possible only at a power of x32 or greater due to the small size of the vessels and the relative transparency of their walls. These vessels are then only visible due to the reflection of red blood cells circulating through them in rouleau formations. Histological examination confirmed these findings. In at least one species of lizard (Gecko gecko; Fig. 1) there is a close anastomosing relationship between the vessels of the spectacle and some intraocular vessels. Discussion. The observation of organized vascularity in the reptilian spectacle is information not previously applied to the phylogeny of the animal or the origin and development of its ocular structures. Examination and comparison of many species may establish a sequentially evolving modification of these vessels useful in the investigation of this area. There is vertical orientation of these vessels in some families of snakes and circumferential orientation in other families with degrees between them. Study and comparison of these patterns would provide valuable, additional phylogenetic information. Preliminary investigation indicates that these vessels are also found in the spectacle of at least some fish, the toadfish being one example. A comparison between these vessels with those of the reptilian spectacle would certainly be of interest. Perhaps the most interesting point of this work is the ability of the reptilian spectacle to maintain a vascular network and still be a tissue with a high degree of transparency comparable to the cornea or lens. This is the only example of such a phenomena as the nictitating membrane, which is also vascular, has a much lesser degree of transparency in even its most sophisticated forms. This structure would, therefore, make an interesting model for the study of compatibility between vascularity and transparency in tissue. The author thanks Professors Marvin L. Sears, William Miller, and Daniel Albert for their continued interest and encouragement of this work and Mr. Kenneth Kostuk for his excellent photography. From the Department of Ophthalmology and Visual Science, Yale University School of Medicine, New Haven, Conn This work was supported in part by United States Public Health Service Grants EY and EY Submitted for publication Jan. 14, Reprint requests: A. W. Mead, Yale University School of Medicine, Department of Ophthalmology and Visual Science, 333 Cedar St., New Haven, Conn Key words: spectacle, brille, snake, lizard, microsilicone, vascularity, transparency.
3 Fig. 1. Microsilicone injected eye of a lizard (Gecko gecko) of the family Gekonidae demonstrating vascularity of the spectacle. The vessels are circumferentially oriented and reticulated in pattern. (x60.) Fig. 2. Microsilicone injection of the eye of the copperhead snake (Agkistrodon contortiix mokasen) of the family Viperidae demonstrating triangulated circumferentially oriented vessels of the spectacle. (x60.) Fig. 3. The microsilicone injected eye of a snake of the Colubrid family, the Northern water snake (Natrix sipedon sipedon) showing quite vertically oriented vessels in a rectilinear pattern. (xl50.) Fig. 4. Specimen of a Siamese cobra (Naja naja kaouthia), an Elapid snake, demonstrating an intricate network of numerous vessels semi-vertically oriented. (x96.)
4
5 Volume 15 Number 1 Reports 591 REFERENCES 1. Rochon-Duvigneaud, A.: La protection de la cornee chez les vertebres qui rampent (serpentes et poissons anguiforms), Ann. Oculist. 154: 633, Bellairs, A. d'a, and Boyd, J. D.: The lachrymal apparatus in lizards and snakes. I. The brille, the orbital glands, lachrymal caniliculi and origin of the lachrymal duct, Proc. Zoo. Soc. Lond. 117: 81, Johnson, C. L.: Contributions to the comparative anatomy of the reptilian and amphibian eye, chiefly based on ophthalmological examination, Philos. Trans. Roy. Soc. B 215: 315, Schwarz-Karsten, H.: Uber Entwicklung und Bau der Brille der Ophidien, Lacertilien, und die Anatomie ihrer Thranenwege, Gegenbaur's Morph. Jahrb. 72: 499, Neher, E. M.: The origin of the brille in Crotalus confluentus, Trans. Am. Ophthalmol. Soc. 33: 535, Bellairs, A. d'a, and Underwood, C: The origin of snakes, Biol. Rev. 26: 193, Walls, G. L.: The vertebrate eye and its adaptive radiation, Cranbrooke Institute of Science, Bull. 19, Walls, G. L.: The significance of the reptilian "spectacle," Am. J. Ophthalmol. 17: 1045, Walls, G. L.: Ophthalmological implications for the early history of snakes, Copeia, 1: 8, Duke-Elder, S.: Personal communication. November, Ludicke, M.: Die Kapillarnetze der Brille, der Iris, des Glaskorpers, und der Chorioidea des Auges, Z. Morph. Tiere 64: 373, 1969.
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