The avian eye is considered to be “supreme amongst all living creatures” and capable of attaining “an order of excellence unmatched in any other species not excepting man” (Duke-Elder, 1958). Many structural and functional adaptations have become involved in the perfection of visual processes in birds which, according to Pumphrey (1948a) represent the culmination of phylogenetic development toward diurnal vision. This chapter is concerned with several of these adaptations, the most obvious of which are the oil droplet inclusions and glycogen deposits within their photoreceptors, the well-developed areae and foveae within their retina and the highly vascularized pecten within their vitreous body. A detailed description of the avian eye is not intended; excellent sources are available on this subject: Wood (1914), Slonaker (1918), Franz (1934), Walls (1942), Rochon-Duvigneaud (1943), Polyak (1957), Duke-Elder (1958), and Hodges (1974)

The Avian Eye and its Adaptations

The pecten oculi is a convolute of blood vessels in the vitreous body of the avian eye. This structure is well known for more than a century, but its functions are still a matter of controversies. One of these functions must be the formation of a blood-retina barrier because there is no diffusion barrier for blood-borne compounds available between the pecten and the retina. Surprisingly, the blood-retina barrier characteristics of this organ have not been studied so far, although the pecten oculi may constitute a fascinating model of vascular differentiation and barrier maturation: Pectinate endothelial cells grow by angiogenesis from the ophthalmotemporal artery into the pecten primordium and consecutively gain barrier properties. The pectinate pigmented cells arise during development from retinal pigment epithelial cells and subsequently lose barrier properties. These inverse transdifferentiation processes may be triggered by the peculiar microenvironment in the vitreous body. In addition, the question is discussed whether the avascularity of the avian retina may be due to the specific metabolic activity of the pecten.

The Pecten Oculi of the Chicken: A Model System for Vascular Differentiation and Barrier Maturation

An investigation was made of the formation of the pharyngeal arch arteries (PAAs) in developing chick embryos that ranged from Hamburger-Hamilton stage (st) 12 to st44 and 1-day-old chicks after hatching. Corrosion casts of the vasculature were made by injecting resin and examined by scanning electron microscopy. The relationship between the PAAs and associated organs was then demonstrated by computer-aided reconstruction. The ventral aorta connected with the dorsal aorta through a loop in front of the foregut at st12. We named this loop the primitive aortic arch to distinguish it from the true first PAA. The second PAA was found to form at st14 and the third PAA at st15, while the true first PAA to connect the dorsal and ventral aortae was found at st16. The aortic regions anterior to the first PAA then fused. By st19, the first PAA had disappeared and the fourth PAA had appeared. The fifth and sixth PAA were observed as a capillary plexus at st20 and st21. The fifth PAA consisted of a bypass of the sixth PAA during st22 to st25. The second PAA was observed to be very slender at st23 and to rupture by st25. At the same time, the proximal parts of the first and second PAAs and the ventral aorta changed into the primary external carotid artery (ECA) and gave off branches to the upper and lower jaws. Furthermore, the distal part of the second PAA remained to become the two branches of the dorsal aorta giving rise to the stapedial artery and the root of the secondary ECA.(ABSTRACT TRUNCATED AT 250 WORDS)

Formation of the pharyngeal arch arteries in the chick embryo. Observations of corrosion casts by scanning electron microscopy

The pecten oculi of the avian eye is an intriguing structure which, despite intensive study, has defied conclusive functional analysis for over 300 years. The reviews of O'Rahilly and Meyer (1961) and Wingstrand and Munk (1965) summarized research done on the pecten up to 1965. Both of these reviews confirmed the observation of Walls (1942) that although anatomical studies and purely speculative accounts of the function of the pecten abound in the literature, the number of experimental investigations has been small. In his classic study of the vertebrate eye, Walls (1942) marshalled considerable anatomical and circumstantial evidence for the

https://www.jstor.org/stable/info/1368009

The functional significance of the avian pecten: a review.

The microvasculature of the eye of the duckling was studied with microcorrosion casting, scanning electron microscopy, and stereology. Most blood to the eyeball first passes through the arterial ophthalmic rete mirabile, a complex of small arteries which intermixes with a similar complex of veins (venous ophthalmic rete mirabile) at the ventrotemporal angle of the eye. The present study reveals the ultrastructural anatomy and the compact, three-dimensional arrangement of vessels in this rete, which had been shown by previous investigators to function as a countercurrent heat exchanger. Vessels from this rete include the supraorbital and infraorbital arteries, which supply the eyeball anteriorly, and the ophthalmotemporal artery, which supplies the eyeball posteriorly. The internal ophthalmic and ethmoidal arteries, branches of the cerebral carotid artery, anastomose with the ophthalmotemporal artery posteriorly. Blood is distributed to the eyeball anteriorly by two ring arteries: the iridial ring artery, which circumscribes the iris and which receives blood from the long ciliary and infraorbital arteries; and the more peripheral, ciliary ring artery, which receives blood mostly from the infraorbital and ethmoidal arteries. Within the iris is a dense, freely anastomosing bed of capillaries which extends to the edge of the pupil and then loops back beneath the ciliary body. The vasculature of the ciliary body consists of radially arranged plates of anastomosing capillaries of irregular bore which mimic the contours of that organ, but permit changes in pupil diameter. The present study demonstrates the three-dimensional anatomy of the very dense capillary net of the choriocapillaris deep to the retina and the capillary mass of the pecten, and thus supports the finding of earlier investigators that nutrients diffusing from these structures nourish the avascular retina. The pecten consists of a pleated sheet of freely anastomosing capillaries which protrudes into the vitreous body from near the optic nerve. The choriocapillaris and the pecten are supplied by branches of the ophthalmotemporal artery: the former by numerous short posterior ciliary arteries, the latter by two or three arteries which further divide into one or two smaller vessels for each of its folds. Veins of the choroid layer at the periphery of the anterior surface of the eyeball, and to some extent on its lateral walls, are revealed by the corrosion-casting technique as unusual, flattened vessels of large caliber which lie in closely spaced parallel arrays. The large surface area thus created may function in heat dissipation. These veins join with others from the choriocapillaris to form a large dorsal and a large ventral posterior ciliary vein. Blood from the pecten and from the choriocapillaris in the nasal, central, and temporal regions of the posterior surface of the eyeball is drained by the ophthalmotemporal vein. Vascular casts of veins are often distinguishable from those of arteries by bore morphology and by the presence of valves, but also by the shapes of endothelial nuclear depressions left in the plastic. The high resolution obtained with the present technique reveals details of microvasculature and of vessel distribution in the avian eye not previously described. Names for some of these vessels are suggested.

Microvasculature of the avian eye: Studies on the eye of the duckling with microcorrosion casting, scanning electron microscopy, and stereology

The pecten oculi of the domestic chicken was examined with light, scanning and transmission electron microscopy and with freeze-etching techniques. Particular attention has been given to the capillary structure. The capillaries form an extensive anastomotic network. Their endothelial cells have apical (luminal), as well as basal, longitudinally oriented microfolds. It is assumed that the formation of apical differentiations of the endothelial surface is due to haemodynamic influences. Thus, sufficient surface area for membrane bound enzymes is achieved. These enzymes are necessary for active transcellular transport processes that require energy. In freeze-etched material, two different structures of the membrane surface of microfolds can be recognized. These results are discussed in relation to transport functions through capillary endothelial cells of the pecten. It is assumed that the pecten plays an important role in the nourishment of the retina and vitreous body.

C. E. Dieterich

Papers

Fine structural observations of the pecten oculi capillaries of the chicken