Anatomy of Structures Related to the FundusChapter 1

The first step in examination is to be able to understand the anatomy of the structures being visualized and their normal appearance.

The retina is composed of tissues embryologically arising from the optic vesicle. It consists of the pigment epithelial layer, derived from the outer layer of the optic cup and the sensory retina derived from the inner layer of the optic cup.

The retina is divided into a central and a peripheral part that ends at the ora serrata. The central retina is an area approximately 5 to 6 mm in diameter centered on the fovea that contains the foveola, fovea, and macula. The peripheral retina is divided into the near periphery, midperiphery, far periphery, and ora serrata. Clinically however the peripheral retina is defined as the zone from the equator to the ora serrata and is approximately three to four disk diameters in width. The vortex veins represent the equator (Fig. 1.1). The retina is thickest around the disk, measuring around 0.56 mm. Peripherally the retina thins so that at the equator it is 0.18 mm in thickness and 0.1 mm at the ora serrata.

The RPE cells have a round nucleus that is situated close to the base of the cell. Mitoses have not been observed in the RPE cells and upon cell death adjacent cells slide laterally to fill the space created. The cytoplasm in the outer part of the RPE cells contains mainly mitochondria and the prominent infoldings of the plasma membrane (villi). The cytoplasm in the inner part of the cell contains most of the melanin granules, which often extend into the apical villi around the outer segments of the photoreceptor. In the peripheral retina there is a high concentration of melanin granules that gradually increase with age. The inner part of the pigment epithelial cells also contain a few ribosomes lying freely in small clusters or attached to short segments of rough endoplasmic reticulum. With increasing age, other pigment granules, composed of lipofuscin, are found in the cytoplasm. The increase in lipofuscin is most marked in the first two decades of life but continues to increase with advancing age, particularly in the macular area. Increase in the number of lipofuscin granules can also occur from mild acute or chronic insult caused by choroidal or RPE disease. Phagosomes are also present in the cytoplasm of the RPE cells and are produced by the apical villi by phagocytosis of disks from the outer segments of the rods and cones. Melanin often becomes incorporated into the lysosome of the RPE cells. These phagosomes are gradually digested by enzymes that are derived from organelles in the cytoplasm of the RPE cells, and their products are often cast off into Bruch's membrane or are retained in the cytoplasm to become lipofuscin granules. The degree of lipofuscin accumulation in the retina is assessed by ‘autofluorescence’ imaging.

The RPE has many functions, the most important being storage of vitamin A and its conversion to a form that can be utilized by the photoreceptors for synthesis of rhodopsin. Other functions include the production of glycosaminoglycans that envelope the photoreceptors, phagocytosis and degradation of lamellar disks of the photoreceptors, promotion of retinal adhesion and absorption of scattered light.

The sensory retina is composed of nine layers (Fig. 1.3). The retinal layers are connected to each other by synaptic connections between axons and dendrites in the inner and outer plexiform layers and eventually to the ganglion cells. The connective tissue supporting the neuronal cells comprises the fibers of Muller's cells and the astrocytes in the inner portion of the retina.

Histologically the macula is defined as that portion of the retina temporal to the optic nerve head that contains two or more layers of ganglion cells.

The macular area is divided into foveola, fovea, parafoveal and perifoveal regions (Fig. 1.4). The central portion of the macula contains the fovea and the foveola is a small depression in the internal surface of the retina.

The foveola is located about 4 mm temporal and 0.8 mm inferior to the optic disk. Centrally, the foveola is 0.35 mm in diameter and 0.25 mm deep. The wall of the depression containing the foveola is called the clivus and causes the tiny foveal reflex. In the foveola, the retina is only 0.13 mm thick and comprises of only photoreceptor cells and Muller cell processes. Each cell is united with a single bipolar cell and possibly with a single ganglion cell, thus yielding maximal transmission of the stimulus. No rods exist in the foveola. The external segments of the cones are long and approach the apical side of the RPE cells. The accumulation of a large number of these specialized cones in the foveola causes a forward, bow-shaped configuration termed as Umbo.5

The fovea measures 1.9 mm in diameter. The thickness of the retina in the fovea is one half of what it is elsewhere, measuring about 0.37 mm as most of the layers are absent, being displaced laterally. The only photoreceptors in the central fovea are cones. The central rod-free area within the fovea measures 0.57 mm in diameter and contains about 35,000 cones. The inner nuclear layer is only two cell layers thick at the edge of the fovea and is absent within the fovea. The inner plexiform layer, ganglion cell layer, and nerve fiber layer are also absent in the fovea. The outer plexiform layer is modified to run obliquely and is called the Henle's layer. This causes the fiber arrangement to become loose and delicate allowing the collection of transudates and exudates. The exudates often form a star like pattern due to the radial arrangement of the fibers. The capillary free zone of the macula measures approximately 0.4 mm in diameter. The entire vascular supply to the fovea is via the choriocapillaris.

The parafoveal area is an annular zone 0.5 mm in width. It contains the largest number of nerve cells in the entire retina. The thickness of the photoreceptor layer in this portion of the retina is 40 to 45 µm.

The perifoveal central retina measures 1.5 mm in width beyond the parafoveal retina. The outer boundary of this area is 2.75 mm from the foveal center.

The peripheral retina consists of four regions: near periphery, midperiphery, far periphery, and ora serrata. The near periphery consists of an annular area 1.5 mm in width surrounding the macula. The midperiphery consists of an annular area 3 mm wide surrounding the near peripheral retina. The far peripheral retina extends in width 9 to 10 mm beyond the midperipheral retina temporally and 16 mm nasally. Ganglion cells in this area are quite large and widely spaced.

At the ora serrata the nine layers of the sensory retina resolve themselves into a single layer of cells that continues into the ciliary body as the nonpigmented epithelium. The external segments of the rods and cones disappear and the inner nuclear layer and the outer nuclear layer merge. The ILM becomes thinner and ultimately multilaminar, finally interweaving with the collagenous filaments of the vitreous base. The rod photoreceptors disappear approximately 1 mm posterior to the ora serrata and are replaced by primitive or malformed-appearing cones. The RPE is continuous with the pigment epithelium of the ciliary body.

Clinically the ora serrata is a serrated zone approximately 2 mm wide temporally and 1 mm wide nasally. It is located more anteriorly on the nasal side than on the temporal. There are 20 to 30 dentate processes which produce serrations and are more prominent nasally. They extend into the pars plana and point towards the valleys between the ciliary processes. The average distance from the ora serrata to the optic nerve head is 32.5 mm temporally, 27 mm nasally, and 31 mm superiorly and inferiorly.

The optic nerve head is just nasal to the posterior pole of the eye. Its edge is located about 3.5 mm from the foveola. The optic disk has an average vertical diameter of 1.86 mm and an average horizontal diameter of 1.75 mm. The normal optic nerve head is usually oval with a central depression—the cup, which represents partial or complete absence of axons with exposure of the lamina cribrosa. The tissue between the cup and the disk margins is referred to as the neural rim. The neural rim has a pink color as it represents the bulk of axons and associated capillaries. The physiological healthy rim is typically broadest in the inferior quadrant followed by the superior, and then the nasal, with the temporal rim being the thinnest (ISNT rule).6

The blood supply to the retina is from two sources. The central retinal artery, a branch of the ophthalmic artery supplies the layers internal to the outer plexiform layer. It enters via the optic nerve. These vessels are anatomically arterioles and they are affected by generalized diseases that affect the arterioles all over the body. The main branches of the central retinal artery run in the nerve fiber layer. The veins and arteries frequently cross, with the vein lying deeper than the artery. The two often share a common adventitial sheath. Smaller branches from these vessels then dip into the retinal layers forming a capillary network in the outer aspect of the inner nuclear layer. An additional small ciliary arterial branch may on occasion additionally supply the macular area. In the parafoveal zone the capillary network is well developed into three layers. The peripapillary retina has an additional layer of capillaries making four layers, to support the thick nerve fiber layer. The central 350-400 microns of the fovea is devoid of any capillaries and receives its nutrition entirely from the choriocapillaris.

The layers of the retina, from the retinal pigment epithelium internally to the inner nuclear layer and the fovea receive their blood supply from the choriocapillaris.

The choroid is dark brown in color. It is 0.22 mm thick posteriorly and 0.10-0.15 mm anteriorly. It is loosely attached to the sclera and can be separated easily creating a potential suprachoroidal space. The retinal pigment epithelium is more strongly attached to the choroid than to the sensory retina.

The choroid is made of four layers. The Bruch's membrane is a multilayered connective tissue between the RPE and the choriocapillaris. It has five layers and its thickness increases with age. The innermost layer is actually the basement membrane of the RPE cells. The next layer is the inner collagenous layer followed by a middle elastic layer and the outer collagenous layer. The outermost layer is the basement membrane of the choriocapillaris.

The choriocapillaris is the modified capillary layer of the choroid. Its unique structure is mandatory for its function. These capillaries are larger than normal capillaries, have thinner walls and multiple fenestrations with covering diaphragms. These capillaries are also grouped into lobules with a central precapillary arteriole and venule. This lobular pattern is more prominent at the posterior pole.

The spongy stroma of the choroid consists of a loose framework of collagenous tissue with a variety of cells and plenty of blood vessels. The cells are mainly melanocytes and fibroblasts. The stroma contains two layers of blood vessels comprising of an outer layer of large vessels of Haller and medium sized vessels of Sattler. These vessels are highly entwined and not fenestrated.

The outermost layer of the choroid is the lamina suprachoroidea made of tightly packed collagen fibrils, elastic fibers and cells. It is more densely pigmented. This layer serves as the transition between the spongy stroma and the tough sclera. Blood vessels only pass through this layer.

The choroidal vascular system is peculiar in the sense that the arteries and veins do not run parallel to each other. The ophthalmic artery gives off the medial and lateral posterior ciliary arteries. These vessels divide into a long posterior ciliary artery (LPCA) and several (10-20) short posterior ciliary arteries (SPCA). These then pierce the sclera 3-4 mm from the optic nerve. The LPCAs then course anteriorly through the suprachoroidal space along the horizontal meridian. Near the ora these give off branches posteriorly to supply the choroid upto the equator. The short posterior ciliary arteries pierce the sclera and enter the choroid all around the optic nerve. They then branch and supply the choriocapillaris till the equator. The venous drainage of the choroid is through the vortex veins. The outer choroid is mainly a venous system where the post capillary venules form afferent veins in each quadrant. These then drain into a vortex vein via a wide ampulla. The vortex veins emerge through the sclera posterior to the equator between the rectus muscles. There may be more than one vortex vein per quadrant. They drain into the superior and inferior ophthalmic veins. These veins exit through the superior and the inferior orbital fissures respectively.

The short and long ciliary nerves form the nerve supply of the choroid and are branches of the ciliary ganglion and nasociliary nerves respectively.7

The main function of the choroid is to provide nutrition to the retinal pigment epithelium and the sensory retina upto the inner nuclear layer. In addition it also produces the pigment of the fundus and dissipates heat.

The vitreous occupies two thirds the volume of the eye and constitutes about 4 ml. It is formed by a highly viscous hydrogel. It is mainly made of water. The collagens like fibrils intertwine with the hyaluronic acid to produce the rigidity and viscosity of the vitreous. The vitreous has a few cells called hyalocytes which may belong to the phagocytic system. Other cells that are found are predominantly fibroblasts and macrophages.

The vitreous is attached all around to the adjacent structures but the attachment is stronger at certain points. It is most strongly attached at the vitreous base that straddles the ora. The base includes 2 mm of the pars plana and 1-4 mm of the peripheral retina. It is also relatively well attached to the optic nerve head, fovea-parafoveal area, the posterior surface of the lens and along the major blood vessels. At the back of the lens the circular area of adherence of condensed vitreous is called the capsulohyaloid ligament (Weigert's ligament). There is a potential space in the inner aspect of this space called the Berger's space which is continuous with the Cloquet's canal.

The peripheral vitreous is called the cortex and has more collagen fibrils and hyalocytes. The central vitreous is relatively less dense. There are bundles of fibrils which insert into the cortex in various directions.

The nerve fibers leave the globe through the perforated scleral plate called the lamina cribrosa. The optic nerve head thus shows the end on view of the nerve fibers leaving the eye. The central area is devoid of nerve fibers and is seen as a pale excavation called the cup. Its size depends on the size of the optic disk and the space occupied by the nerve fibers and will be larger if the disk is large or nerve fibers have been lost. Its size also depends on the obliquity of the attachment of the nerve and the degree of the development and regression of the hyaloid artery system. The pinkish color of the neuroretinal rim is due to the presence of numerous capillaries within the nerve fibers. The central retinal vessels emerge from the cup. Sometimes a cilioretinal vessel can be seen to arise from the temporal part of the disk coursing towards the macula for varying distances.

The surface of the optic nerve is supplied by small recurrent branches from the retinal arteries that anastamose with branches from the posterior ciliary vessels. The part of the nerve anterior to the lamina cribrosa is referred to as the pre-laminar portion and receives its blood supply from the branches of the peripapillary choroidal vessels and the short posterior ciliary vessels. The laminar portion is supplied by branches of the short posterior ciliary vessels and pial arteries with occasional branches from the central retinal artery. The retrolaminar portion is supplied by branches of the central retinal artery and perforating branches of the pial plexus which form the main blood supply of the posterior portion of the optic nerve.8

On focusing the retinal details (Fig. 1.7), the first structure to look for is the disk. It is the most striking part of the fundus and easiest to locate. The normal disk (Fig. 1.8) is vertically oval to round in shape with well defined margins lying in the same plane as the rest of the retina. Its color varies from yellowish orange to pink with a pale excavation in the center called the cup. The cup roughly occupies one third the area of the whole disk. It is placed in the center of the disk or slightly eccentric. The surrounding rim is usually thickest inferior to the cup followed by the superior, the nasal and temporal. The peripapillary area is occupied by normal retinal tissue though sometimes there may be a diskolored crescent shaped area adjacent to the temporal rim called the temporal crescent.

The next structures to be examined are the blood vessels (Fig. 1.9). The retinal vessels arise from the center of the disk or slightly nasally. Most commonly they divide into a superior and inferior branch as they emerge on the disk surface. Further division into nasal and temporal branches occurs near the disk margin. The nasal vessels then run straight towards the retinal periphery. The temporal vessels arch above and below the macula forming the vascular arcades. The arterioles are identified by the presence of the streak of a golden yellow reflex. They are reddish in color as compared to the venules which are darker. Venules are also wider, flatter and lack any reflex. The arterioles and venules run alongside for some distance and their branches often cross each other. At these crossings, the arterioles usually coarse over the venules and are encased in a common sheath (Fig. 1.10). Sometimes an additional arteriole is seen arising from the temporal part of the optic disk separate from the retinal vessels. This vessel is derived from the ciliary vessels and is called the cilioretinal artery (Figs 1.11 and 1.12). It supplies the area from the optic nerve to the macula for varying distances.

The rest of the retina has an orangish color which varies with the degree of pigmentation in the pigment epithelium. Some normal variations of the pigment in the RPE can allow the orange stripes of choroidal vessels to be seen giving it a tigroid appearance (Fig. 1.13). These vessels are better seen in the mid-periphery and beyond.

The macula is examined a little late in the examination process as it will cause diskomfort to the patient, due to its sensitivity to light. The macula is located at the posterior pole, temporal to the disk (Fig. 1.14). A small bright yellow reflex denotes the foveola which is the center of the macula. The foveola is surrounded by a dark circular region of approximately 150 microns termed the fovea. The fovea may be surrounded by a faint circular light reflex. Surrounding this, an area upto 5-6 mm from the foveola is the macula. It roughly extends upto the vascular arcades and nasally upto the optic disk. Short branches from the superior and inferior arcades coarse towards the macula and terminate before the fovea.

Angiographically an avascular zone of 350-500 microns is seen at the center of the macula (Fig. 1.15). The fovea often shows a yellowish appearance due to the presence of xanthophyll pigment.

It is possible to examine the peripheral retina better by asking the patient to look in the direction of the examined area. Any lesions found are localized in relation to the vortex ampullae which mark the equator (Fig. 1.16). The equator lies 6-8 mm posterior to the ora serrata. These ampullae are seen as oval orange colored areas into which several choroidal vessels are seen to drain.

It may be possible to see the ora in some patients especially aphakic without indentation (Fig. 1.17) but on most occasions some indentation is required. This brings the retina upto the ora into view and allows a dynamic study of a lesion such as raising the flap of a horseshoe retinal tear. The Ora is recognized by its white edged, serrated appearance formed by the sharp dentate processes and bays. These are more prominent nasally. Invariably there is a strip of small cysts just anterior to the ora called microcystoid degeneration.

The normal vitreous is visualized by biomicroscopy with a bright beam and a narrow slit. The illumination is kept at the maximum angle possible without losing the slit. This shows a black background against which the faintly visible gray bundles of fibrils can be seen (Fig. 1.18). These exhibit gentle movements with movements of the eye. The slit lamp can be moved in to view the deeper vitreous. The posterior vitreous can be examined better by condensing lenses. The vertical slit beam is moved in and out to look for the detached posterior face which is seen as a continuous fine white line. The fibrillar arrangement is seen anterior to this line and clear space behind it. The peripheral vitreous can be examined by indirect ophthalmoscopy or by three mirror examination.