|Year : 1968 | Volume
| Issue : 1 | Page : 3-11
Retinal vasculature in mammalia
PK Agrawal1, LP Agarwal1, HD Tandon2
1 Dept of Ophthalmology, All-India Institute of Medical Sciences, New Delhi-16, India
2 Dept of Pathology, All-India Institute of Medical Sciences, New Delhi-16, India
|Date of Web Publication||22-Dec-2007|
P K Agrawal
Dept of Ophthalmology, All-India Institute of Medical Sciences, New Delhi-16
Source of Support: None, Conflict of Interest: None
|How to cite this article:|
Agrawal P K, Agarwal L P, Tandon H D. Retinal vasculature in mammalia. Indian J Ophthalmol 1968;16:3-11
The recent digestion technique of K U W A B A R A AND COGAN  has given a new impetus to the study of retinal vasculature. It is interesting to study the different types of vascular patterns encountered in the retina of mammalia, and how the retinal circulation is maintained. The retinal vasculature reported here has been studied in the following mammalia by the digestion techniques with trypsin (KUWABARA AND COGAN,  or with pepsin-trypsin (ASHTON),  and stained by P. A. S. and hcernatoxylin.
The study has been divided into three parts:
I. General disposition of retinal vessels.
II. Study of the capillary network.
III. Study of the cellular elements.
There is a considerable amount of similarity in these studies between the different orders of mammals, at the same time there are several dissimilarities to which we' wish to draw special attention.
| I. GENERAL DISPOSITION OF RETINAL VESSELS|| |
I i. Retinal Vascular Pattern of Rats
The vessels are seen crossing from the center of the disc, 6-7 arteries alternating with veins. The arterioles stain more intensely red (P. A. S. and hoematoxylin) than the veins which are bigger than the arterioles, the difference persisting upto the peripheral area.
The branchings are both dichotomous and side arm. An annular thickening may be noticed at the side arm branchings of the arteries only (not of the veins). They take a darker stain.
The last loops of the retinal capillaries form usually a U-shaped anastomosis to each other at the most peripheral point of the retinal circulatory system and are mostly demarkated as the last wide - caliber capillary arches.
I ii. Retional Vascular Pattern of Cats
There are 3 to 4 pairs of arteries and veins which run to the periphery in a curved fashion, crossing and recrossing each other. Besides these major pairs of vessels are to be seen isolated vessels, 3 to 4 in number, running from the disc to the periphery. At the disc the veins are double the thickness of the arteries but become of almost equal thickness as they approach the periphery. The arteriolar branches are dichotomous and side-arm, the latter often showing a narrowing at the junction due to the presence of an annular thickening of the coat here (annuli), which are not to be found in venules (Plate 9)-[Figure - 9].
I iii Retinal Vascular Pattern of Dogs.
In the dog there are no central retinal vessels. From the margin of the disc emerge 3 or 4 arteries and veins like cilio-retinal vessels. The vessels run tortuously to the periphery and not straight as described in the rat and the cat. The differential staining between arteries and veins, the difference in their sizes, their branchings etc. are of the same pattern as in the case of the rat and the cat. The major veins form an annular vascular area at the periphery where they anastomose with each other and with the wide-caliber capillaries.
I iv Retinal Vascular Pattern of Rabbits.
Plate 4-[Figure - 4] shows the temporal half of the retinal vessels of the rabbit. The main central retinal artery and vein divide into two stems which appear to emerge at the periphery of the medullated nerve fibres on either side of the disc. The artery and the vein cross occasionally. Branchings are mostly dichotomous. Darker staining (PAS positive) spots are where branches arise from the deep surface of the arteries. The branches end peripherally forming terminal capillary loops.
I v Retinal Vascular Pattern of Goats
There are 2 main central retinal vessels, which come out at the disc after passing upwards and downwards. Each vessel arches over towards the periphery branching dichotomously. The temporal vessels are straighter than the nasal ones which describe a curved sweep. The vein at first travelling close to the artery tries to pass in between the arteries.
I vi Retinal Vascular Pattern of Monkeys
The vessels are intra-retinal. There is a central retinal artery and vein.
Two arteries and veins cross from the disc upwards and downwards. After a short variable distance temporal and nasal vessels appear. The latter run a straight course to the periphery. The temporal ones arch with their concavity towards the fovea centralis. Plate 7-[Figure - 7]. Temporal to the fovea the blood vessels coming from above and below interdigitate. The general arrangement is reticular with bisular division and rarely trisular.
| Discussion|| |
In general, there is an axial sys, tern of vascular supply and drainage for the mammalian retina, originating from the centre of the disc. The distribution is radial through 2, 3, 4 or more groups of vessels, arteries alternating with veins, the latter being broader but less deeply staining with P.A.S. and haematoxylin than the arterioles. (Plate 8)-[Figure - 8] The differences in emergence of the vessels, their numbers, size, their tortuosity and branchings are brought out in the different plates for the different orders of mammalia. Except in primates, the retinal arteries end in the form of terminal intercommunicating loops which form a kind of an annular venous sinus at the periphery from which the venous blood returns. In the case of primates the arterioles are end-arterioles.
Both dichotomus and side-arm branchings are seen throughout the course of the vascular tree, in all mammalia. At the point of the sidearm branching, the arterioles show annular thickening (arteolar annuli), (Plate 9)-[Figure - 9] which takes a darker stain. The arteriole becomes narrower at this annulus, which is not present in vessels that branch off acutely (Plate 9)-[Figure - 9] Where branches emerge from the deeper surface of the vessels, the points appear as darker stained areas, because of the arteolar annuli which take a deeper stain. (Plate 4)-[Figure - 4] These thickenings are not present on the corresponding areas of the veins.
The vascular system in the retina of rabbits deserves a special mention as it is markedly different from those of other mammals. (Plate 5)-[Figure - 5] It is described as "merangiotic". The retinal vessels are confined to two wing-shaped areas on the nasal and temporal sides of the disc. The rest of the retina is avascular. The other characteristic is a large area of medullated nerve fibres which run along the vessels to a distance of 8.71 to 8.48 mm (MICHAELSON, 1954). The blood vessels are more preretinal (MICHAELSON) than intra-retinal (SCHULZE 1893; FUCHS 1906) or extraretinal BURNS, 1882). The arteries and veins run more parallel to each other and seldom cross. Other characteristics are the formation of connecting loops between arteries an veins and of connecting loops between arterioles and venules distributed along the medullated fibres from the disc to the periphery. These loops have different shapes and size. Most of them have a U or twisted configuration. The last loops are usually formed by the end arterial capilaries, as they turn back with the vein after looping at the periphery. (Plate 10)-[Figure - 10]
In Primates the shift of the eyes to a more frontal position and consequently the differentiation of a small portion of the temporal retina into the macula and its migration towards the disc brings about changes in the arrangement of the nerve fibres and so also of the vasculature. In them the macula gets surrounded by blood vessels which, coming from above and below arch round it. The upper and lower vessels situated further temporally interdigitate beyond the macula, along the raphe. (Plate 7)-[Figure - 7]
| II. RETINAL CAPILLARIES|| |
This study has been made by the digestion technique mentioned above and staining the specimen with PAS, haematoxylin, eosin.
The pattern of distribution of the capillary network is essentially the same in all mammals except in primates.
The capillaries take up an eosinophilic stain and exhibit a regular lumen. The silver nitrate injected specimens reveal a reticular pattern of the vessels. There is a very dense capillary network at the posterior pole, having extensive anastomosis with each other, indirectly connecting the bigger vessels, which gradually decreases in density towards the equator and the periphery where the isolated loops offer themselves for an easier study. (Plate 10)-[Figure - 10]
There is a capillary free zone traversed by only very few capillaries, on either side of the arterioles, which is less evident near the disc because of the capillary density. Plate 8-[Figure - 8], Plate 11-[Figure - 11] There is no capillary free zone around the venules. Many of the capillaries cross the veins while several capillaries enter directly into the main trunk.
Connecting the capillaries are seen occasional strands of tissue, the intercapillary hands which are stained by P. A. S. and eosin and these apparently have no lumen. (Plate 12)-[Figure - 12] They are as numerous in the periphery as in the central region. These usually connect the nucleated region of the two capillaries which may either be adjacent to each other or Tray even be at a distance from each other. The entrance of these intercapillary bands is guarded at least on one end by a mural cell. These bands may be complete or incomplete and are seen in different stages of atrophy in the adult retinal capillaries.
In the cat, dog and goat in the periphery there is practically a single layer of capillaries with many fibrotic and atrophic capillaries. (Plate 13)-[Figure - 13] The intercapillary bands are similarly very few.
In the rabbit the capillaries do not form a regular net-work but they have an entirely irregular arrangement of their loops in the central areas. These irregularities consist of variation in size, shape, origin and exit. More than one capillary layer appears between the major vessels at the central areas. Several of these capillaries present an overlapping position to one another in that area.
They are usually twisted, rarely straight at the centre but at the periphery, they are generally straight and parallel to each other and point towards the periphery. Very few of the peripheral capillaries have anastomoses or form loops. (See insert Plate 10)-[Figure - 10].
Although the retina of primates resembles in its capillary net-work the system described for other mammals in respect of annular thickenings at side-arm branchings, intercapillary hands and capillary-free periarteriolar spaces, the development and migration of the macula to the temporal side of the disc and a much heavier capillary net-work requiring a higher pressure head to overcome the resistance offered by these capillaries, require a few modifications to fulfil these higher demands of the retinal functions.
Orienting our description from the macula we find a disc-shaped capillary-free central part which is surrounded by a very dense capillary network. Plate 7-[Figure - 7]. It is formed by the breaking up into arterioles of the branches of the temporal arteries that approach the macula from all sides and which after extensive anastomosis again form into vessels which drain into the corresponding veins. On the medial side they run inwards towards the disc and on the temporal. side the upper and lower branches interdigitate at the raphe temporal to the macula.
Besides the layer of capillary network which spreads from the macula all round, there is another layer placed more superficial to the main vessels which forms a lamella of long, arborising channels forming rectangles, triangles and elongated ellipses.
At the disc margin there is only a single layer of capillaries, surrounding which there is this extensive double layer of capillary net-work. The general arrangement is reticular with bisular and rarely trisular divisions.
The following types of capillary networks are seen:
(I) The classical capillary system. The transition from arteries to veins occurs via canaliculi which increase in number as their diameter decreases and nowhere a direct communication between artery and vein with a diameter exceeding that of a capillary is seen in this system.
(II) Chambers-Zweifach network in peripapillary area in which the arterio venous transition is formed by a wider canal with the diameter of an average precapillary upto 20μ. From this transition, very fine capillaries extend in all directions so that the capillary system at this site consists not of a progressive transition from artery to vein, but rather of a network dependent on the wider communication between artery and vein. This wider capillary canal, therefore is localised within the capillary system itself.
(III) Annular type and
(IV) A direct precapillary transmission in the periphery.
An unusual feature of the retinal capillaries is that tiny vessels come off from relatively larger arterioles. The branching and division of arterioles in the central area is mostly at right angles where there is the annular thickening (annulus). Towards the periphery they become more acute angled without the thickening. These features serve to maintain a high pressure-head to meet the higher demands of energy of the retina particularly of primates.
| III. THE CELLULAR ELEMENTS|| |
In the capillaries, situated at fairly regular intervals are the large oval pale staining nuclei of the endothelial cells, situated in an axis parallel to the long axis of the vessels. Equally regularly disposed are the mural cells with rounded hyperchromatic nuclei lying in the walls of the capillaries. (Plate 14)-[Figure - 14].
The endothelial and mural cells are derived from a common parent cell. (AGARWAL, 1965) The process of retraction of capillaries as has been described in developing retinal capillaries, is quite evident even in adult capillaries, thereby, indicating the presence of parent cells in the adult capillaries. These parent cells are constantly transforming into mural cells and endothelial cells. The presence of those cells, however, is very difficult to make out as morphologically, there is very little distinction from endothelial cells.
Partially digested retinal preparations or preparations after water digestion and stained by Wolter Silver staining (1960) reveal the presence of structures stained densely and homogenously by silver. These are of many different sizes and shapes. No nuclei are seen on them. These are irregularly present in arterioles, venules and capillaries. These so called pericytes (WOLTER 1962) are completely digested by trypsin and so are not demonstrable after a retinal vascular mount which is well digested with trypin. (Plate 15)-[Figure - 15]
The cellular structure of the retinal capillaries differs somewhat in rabbits. The main cellular components of the capillaries are endothelial cells, their nuclei vary in shape and size and are usually irregular, oval or flattened and contain many fine dust like light blue chromatin particles.
The second type of cells are the mural cells. They are not easily distinguishable from endothelial cells, as they are in retinal capillaries of other mammals. Close scrutiny, however, does reveal a second type of cell, resembling closely mural cells.
These mural cells resemble more the hyaloid capillary mural cells of rat, frog and fishes than the type seen in the intra-retinal capillaries of rat, dog, cat, monkey etc. The nuclei are rot spherical but vary in shape, usually oval and elongated with two tapering ends. They are slightly darker, smaller and narrower than endothelial nuclei but contain thicker chromatine particles. They do not show a regular distribution on the capillary walls.
The presence of parent cells is very doubtful in the retinal capillaries. The process of retraction was, however, very doubtful in the retinal capillaries.
| Summary|| |
The pattern of retinal vasculature in rats, cats, dogs, rabbits, goats and monkeys as studied after digestion with pepsin - trpasin have been described and compared.
The retinal capillaries, their cellular elements and intercapillary bands with their dispositions are described and discussed.
| References|| |
AGRAWAL, P. K. The Cellular Structure of the Hyaloid System of the rat. Orient A. of Ophth. 2, 279 (1964).
AGRAWAL, P. K. Retinal Vessels in Experimental Ischaemia. Orient. A. of Ophth., :3, 184 (1965).
ASHTON, N. Studies of the Retinal Capillaries in relation to diabetic and other Retinopathies. Brit. J. of Ophth., 47, 521 (1963).
BRUNS L. Comparative Anatomical Studies on the Vascular System of the Retina (German) Zeit f. verglichende, Augenheilk., 1, 77 (1882).
HIS: Comparative study on the vascular system of the Human Retina and that of the Rabbit (Germany) Arch. Anat. u. Entwicker, 224 (180).
KUWABARA, T. AND COGAN, D. G. Arch. Ophth. (Chicago), 71, 93 (1960).
MICHAELSON, I. C. Retinal Circulation in Man and Animals. Publ. Thomas, Springfield, Ill. (1954).
SCIIULTZE, O. On the Development of the Retinal Blood-vessels (German) Anat. des Auges p. 174 (1891).
WOLTER, D. R. The pericytes of the Human Retina. Amer. J. Ophth., 53, 981 (1962).
[Figure - 1], [Figure - 2], [Figure - 3], [Figure - 4], [Figure - 5], [Figure - 6], [Figure - 7], [Figure - 8], [Figure - 9], [Figure - 10], [Figure - 11], [Figure - 12], [Figure - 13], [Figure - 14], [Figure - 15]
[Table - 1]