Filtration angle and aqueous drainage

Aqueous humour is produced by the ciliary epithelium, passes through the pupil and circulates within the anterior chamber supplying the avascular cornea and lens with nutrients. It drains from the eye mainly through the trabecular meshwork into the canal of Schlemm at the iridocorneal (filtration) angle (Figs 40.2, 40.3), formed between the posterior aspect of the corneoscleral limbus and the periphery of the iris.

Fig. 40.2 Meridional section through the anterior eye highlighting the ciliary body and drainage apparatus.

Fig. 40.3 Tissues bordering the anterior chamber angle. The trabecular meshwork is an anulus of tissue spanning the angle: its meshes are shown in transverse section opposite the canal of Schlemm and partly attached to the scleral spur. A single iris process bridges the angle, connecting the trabecular meshwork to the anterior tissues of the iris.

The trabecular meshwork consists of loose trabecular tissue which is continuous anteriorly with Descemet’s membrane and the endothelium of the cornea. Aqueous humour filters from the anterior chamber through interconnected spaces among trabecular fibres. Most of these fibres are attached to the anterior, external aspect of the scleral spur. Of the remainder, most are continuous with longitudinal fibres of the ciliary muscle, some of which attach to the posterior internal aspect of the scleral spur. The trabecular meshwork provides sufficient resistance to aqueous humour outflow to generate an intraocular pressure of approximately 15 mmHg. It also acts as a filter and has the capacity to phagocytose particulate matter, although overloading may contribute to the pathogenesis of various forms of obstructive secondary glaucomas.

The canal of Schlemm (sinus venosus sclerae) is an anular endothelial canal located near the internal surface of the sclera close to the limbus. In section, the canal appears as an oval cleft, with an outer wall that grooves the sclera. Posteriorly, the cleft extends as far as a rim of scleral tissue, the scleral spur, which in section forms a triangle with its apex directed forwards (Figs 40.2, 40.3). The canal of Schlemm may be double or multiple in part of its course, and its walls are constructed of a continuous single thin endothelial layer. Passage of aqueous humour to the canal probably occurs via giant pinocytotic vacuoles, which form on the inner face of the endothelium and discharge into the canal at the outer face, and through intercellular clefts. Aqueous humour passes through a plexus of fine intrascleral vessels which connect the canal of Schlemm with anterior ciliary veins (Fig. 40.4). Normally the canal does not contain blood: pressure gradients prevent the reflux of blood even though the channels between the canal and veins have no valves. However, in venous congestion, blood may enter the canal: the continuous endothelial outer wall of the canal prevents further reflux.

Fig. 40.4 Tissues of the filtration angle in section. The approximate borders of the limbal region are indicated by the solid lines. Aqueous humour drains from the anterior chamber at T through the trabecular meshwork into the canal of Schlemm from where it flows through collector channels either to the intrascleral venous plexus, where it mixes with blood from the ciliary venous plexus, or directly to the surface tissues of the eye as an aqueous vein. The aqueous vein is shown joining an episcleral vein at the surface to form a laminated vessel. Aqueous and blood drain posteriorly in episcleral veins which in turn join anterior ciliary veins.

An alternative route for aqueous outflow, the uveo-scleral pathway, has been described. Since there is no epithelial barrier between the anterior chamber and the ciliary body, aqueous humour is able to enter the loose connective tissue in front of the ciliary muscle and pass between the muscle fibres into the supraciliary and suprachoroidal spaces, where potentially it can be absorbed by vessels that drain the uvea.

Corneal epithelium

The corneal epithelium accounts for approximately 10% of the corneal thickness (50 μm). It usually consists of 5–6 layers of cells (Fig. 40.5B) that protect the ocular surface from mechanical abrasion, form a permeability barrier (to small molecules, water and ions) and prevent the entry of pathogens. The deepest cells are columnar with flat bases, rounded apices, and large round or oval nuclei. Outside these are 2–3 layers of polyhedral (often wing-shaped) cells. In the more superficial layers the cells become progressively flatter, and present a smooth, optically perfect surface. Scanning electron microscopy of surface cells reveals extensive finger-like and ridge-like projections (microvilli and microplicae). A complex network of tight junctions links the superficial cells, consistent with their barrier function.

Anterior limiting lamina (Bowman’s layer)

The anterior limiting lamina lies behind the corneal epithelium. It contains a dense mass of collagen fibrils set in a matrix similar to that of the substantia propria. The lamina is 12 μm thick, is readily distinguishable from the substantia propria because it does not contain fibroblasts, and appears amorphous by light microscopy (Fig. 40.5B).

Substantia propria (stroma)

The substantia propria is approximately 500 μm thick and forms the bulk of the cornea. It is a compact and transparent layer, composed of 200–250 sequential lamellae, each made up of fine parallel collagen fibrils mainly of type I collagen. Flat dendritic interconnecting fibroblasts (keratocytes) form a coarse mesh between the lamellae. Alternate lamellae are typically orientated at large angles to each other (Fig. 40.6). X-ray diffraction studies indicate that they run along two preferred directions, superior-inferior and nasal-temporal, to account for the additional tensile stress exerted by the recti along these meridians (Boote et al 2005). Each lamella is approximately 2 μm thick and of variable width (10–250 μm, or, rarely, more). In the central cornea fibrils within the lamellae have a similar diameter of approximately 31 nm. This increases slightly with age and approaching the limbus. The small size of the fibrils (much smaller than the wavelength of light), along with the regularity of their spacing (maintained by collagen: proteoglycan interactions), and the careful control of corneal hydration, are the principal factors which determine stromal transparency. Light scattered by the collagen fibrils is eliminated by destructive interference in all directions other than forwards.

Fig. 40.6 Stroma of the human cornea showing the geometric precision of the alternation in direction of adjacent layers of fibres.

(By courtesy of John Marshall, St Thomas’ Hospital, London).

Posterior limiting lamina (Descemet’s layer)

The posterior limiting lamina covers the substantia propria posteriorly. It is thin and apparently homogeneous, and is regarded as the basement membrane of the endothelium. It is 4 μm thick at birth, and may increase to 12 μm by the eighth decade.

Endothelium

The endothelium covers the posterior surface of the cornea and consists of a single layer of squamous cells (Fig. 40.5C) with prominent interdigitations between adjacent cells, which are also connected by tight and gap junctions. When viewed en face, the endothelium appears as a mosaic of polygonal (typically hexagonal) cells. As these cells have a limited capacity for mitosis, in response to pathology, trauma, age and prolonged contact lens wear, the endothelial mosaic becomes less regular, and shows a greater variation in cell size and shape, as cells spread to fill gaps caused by cell loss. The numerous mitochondria and prominent rough ER within these cells reflects their high metabolic activity. Thus, for example, active pumping mechanisms largely control the degree of corneal hydration.

Corneal innervation

The cornea is innervated by numerous branches of the ophthalmic nerve (see p. 667) which either form an anular plexus around the periphery of the cornea, or pass directly from the sclera and enter the corneal stroma radially as 70–80 small groups of fibres. Upon entering the cornea, the few myelinated nerves lose their myelin sheaths and ramify throughout the corneal matrix in a delicate reticulum, their terminal filaments forming an intricate subepithelial plexus. Axon bundles from this plexus cross the anterior limiting membrane and form a subbasal plexus from which individual beaded axons pass to more superficial epithelial layers, eventually terminating as free nerve endings. Corneal nerves provide the afferent arm of the blink and lacrimal (see p. 673) reflexes and may also have a neurotrophic function.

Suprachoroid

The suprachoroid covers the external surface of the choroid, is approximately 30 μm thick and composed of delicate non-vascular lamellae, each one a network of fine collagen and elastic fibres, fibroblasts and melanocytes. Ciliary nerves and long posterior ciliary arteries pass forward to the anterior uvea in this layer.

Vessel layer (stroma)

Internal to the suprachoroid lies a layer composed mainly of arteries and veins, but also some loose connective tissue containing scattered pigment cells. These melanocytes limit the passage of light through the sclera to the retina. More importantly, like the retinal pigment epithelium (see p. 689), they also absorb light traversing the retina that is not absorbed by the photoreceptors, so preventing internal reflection.

The blood supply of the choroid, as well as the rest of the uvea, is summarized in Figure 40.10. Short posterior ciliary arteries enter the eye through the sclera near the optic disc and supply the posterior choroid. These vessels branch and gradually decrease in size as they approach the retinal border. The choroidal stroma can be divided into layers based on the change in the calibre of these vessels; an outer layer of larger vessels (Haller’s layer), an inner layer of smaller vessels (Sattler’s layer) which eventually give rise to the choriocapillaris (Fig. 40.7). Long posterior ciliary arteries and recurrent branches of anterior ciliary arteries supply the anterior part of the choriocapillaris.

Fig. 40.10 The vasculature of the uveal tract. The long posterior ciliary arteries, one of which is visible (A), branch at the ora serrata (b) and feed the capillaries of the anterior part of the choroid. Short posterior ciliary arteries (C) divide rapidly to form the posterior part of the choriocapillaris. Anterior ciliary arteries (D) send recurrent branches to the choriocapillaris (e) and anterior rami to the major arterial circle (f). Branches from the circle extend into the iris (g) and to the limbus. Branches of the short posterior ciliary arteries (C) form an anastomotic circle (of Zinn) (h) round the optic disc, and twigs from this (i) join an arterial network on the optic nerve. The vortex veins (J) are formed by the junctions (k) of suprachoroidal tributaries (l). Smaller tributaries are also shown (m, n). The veins draining the scleral venous sinus (o) join anterior ciliary veins and vorticose tributaries.

(By permission from Hogan MJ, Alvarado JA, Weddell JE 1971 Histology of the Human Eye. Philadelphia: WB Saunders.)

Veins within the choroid converge spirally onto four, or very occasionally more, principal vortex veins. These pierce the sclera behind the equator to reach tributaries of the ophthalmic veins.

The vessels of the choroid have a rich autonomic vasomotor supply.

The blood flow through the choroid is high, a feature probably associated with an intraocular pressure of 15–20 mm Hg, which means that a venous pressure above 20 mm Hg is required to maintain circulation. The choroidal perfusion rate exceeds that required to supply nutrients and may serve to cool the retina during exposure to bright light.

Choriocapillaris

The choriocapillaris provides nutrients to the outer five layers of the retina and is composed of large (up to 20 μm thick) densely packed, freely anastomosing, fenestrated capillaries. While pericytes occur mainly on the scleral surface, most fenestrations face the retina. The permeability of choriocapillaris is exceptionally high even compared to other structures invested with fenestrated capillaries.

Lamina vitrea (Bruch’s membrane)

The lamina vitrea lies between the choriocapillaris and the retinal pigment epithelium from both of which it is derived. It appears as a glassy, homogeneous layer, only 2–4 μm in diameter, under the light microscope. It consists largely of an elastic fibre mesh, although some authors include internal and external layers of collagen and the basal laminae of the choriocapillaris and retinal pigment epithelium in this structure. Its function is thought to be related to the passage of fluid and solutes from the choroidal capillaries to the retina. In advancing years, extracellular deposits may accumulate in this membrane (drüsen), which impairs the exchange of gases, nutrients and metabolites between the choroidal blood and the outer layers of the retina, potentially contributing to degenerative disease in the photoreceptor layer of the neural retina.

Ciliary epithelium

The ciliary epithelium is bilaminar, consisting of two layers of simple epithelium which are derived embryonically from the two layers of the optic cup. The superficial layer consists of columnar cells over the pars plana, and cuboidal cells over the ciliary processes of the pars plicata: it becomes irregular and more flattened between the processes. These cells contain little or no pigment. The outer layer of the ciliary epithelium, in contrast contains cuboidal cells which are loaded with melanin. The two layers are normally firmly united, but fluid may separate them pathologically. The pigment layer is attached to the stroma of the ciliary body by its basal lamina, which continues back into the basal lamina of the choroid. As a consequence of the invagination of the optic cup during development, a basal lamina covers the free surface of the bilayer which is continuous with the internal limiting membrane of the retina (see p. 692).

The ciliary epithelium is responsible for the secretion of aqueous humour (see p. 685), while the outer pigmented epithelium additionally contributes to the eye’s ‘black box effect’, like the retinal pigment epithelium, choroidal pigment and posterior iris epithelium, absorbing stray light to enhance image quality.

Ciliary stroma

The ciliary stroma is composed largely of loose bundles of collagen, which form a considerable mass between the ciliary muscle and overlying processes, and extend into both of them. This inner layer of connective tissue contains numerous larger branches of the ciliary vessels. A dense reticulum of large (up to 35 μm diameter) fenestrated capillaries is concentrated in the ciliary processes. This facilitates the passage of substances from the blood plasma during aqueous production (see p. 685). Anteriorly, near the periphery of the iris, the major arterial circle (Fig. 40.10; see also Fig. 40.14) is formed chiefly by long posterior ciliary branches of the ophthalmic artery. These enter the eye some distance behind the ocular equator and pass between the choroid and sclera to the ciliary body. Ciliary veins, also draining the iris, pass posteriorly to join the vortex veins of the choroid.

Fig. 40.14 Meridional section of an iris. The posterior surface is lined with a double epithelium (E, E’): the arrow points to the processes of the anterior layer of the epithelium forming the dilator pupillae muscle. ST, Stroma. C, Collarette. RT, Root. A, Anterior border layer. PF, Folds in anterior surface towards the root. R, Pupillary ruff. S, Sphincter pupillae muscle. P, Pupillary region of the iris. The iris is in a contracted state, as shown by the thickened epithelium opposite the dilator muscle and thinning opposite the sphincter, and by the shortness of the pupillary zone. CM, Ciliary muscle. CP, Ciliary processes. I, Major iridic circle.

Ciliary muscle

Ciliary muscle is composed of smooth muscle cells, most of which are attached to the scleral spur and arranged in three different orientations. The outermost fibres are meridional or longitudinal, and pass posteriorly into the stroma of the choroid. The innermost fibres swerve acutely from the spur to run circumferentially as a sphincter near the periphery of the lens. Obliquely interconnecting radial fibres run between these two muscular strata, frequently forming an interweaving lattice (Figs 40.2, 40.11).

Fig. 40.11 The ciliary muscle and its components. The meridional or longitudinal (1), radial or oblique (2), and circular or sphincteric (3) layers of muscle fibres are displayed by successive removal towards the ocular interior. The cornea and sclera have been removed, leaving the canal of Schlemm (a), collecting venules (b) and scleral spur (c). The meridional fibres (1) often display acutely angled junctions (d) and terminate in epichoroidal stars (e). The radial fibres meet at obtuse angles (f) and similar junctions, at even wider angles (g), occur in the circular ciliary muscle.

(By permission from Hogan MJ, Alvarado JA, Weddell JE 1971 Histology of the Human Eye. Philadelphia: WB Saunders.)

Accommodation reflex

At rest distant objects are focused on the retina in an emmetropic eye (see p. 687). In order to focus closer objects the dioptric power of the eye has to be increased, which is achieved by increasing the curvature of the lens. At rest the lens is under tension from the zonular ligaments and hence flattened. On accommodation, the ciliary muscle contracts, moving the ciliary body forwards and inwards towards the optic axis. All parts of the muscle act in concert, and tension on the zonular ligaments is relaxed. As the lens is covered by an elastic capsule (see p. 686), once tension on it is released it assumes a more convex shape suitable for focusing closer objects. The radius of curvature of the anterior lens surface changes most during accommodation.

Information from the retina passing to the visual cortex does not constitute the afferent limb of a simple reflex in the usual sense of the term, but permits the visual areas to assess the clarity of objects in the visual field. Cortical efferent information passes to the pretectal area and thence to the Edinger–Westphal nucleus, which contains preganglionic parasympathetic neurones whose axons travel in the oculomotor nerve (Fig. 40.12). Efferent impulses pass in the oculomotor nerve to the orbit where they synapse in the ciliary ganglion. Postganglionic fibres (short ciliary nerves) innervate the ciliary muscle causing it to contract. There is also a sparse sympathetic innervation of ciliary muscle, which has a very limited capacity to relax the muscle.

Fig. 40.12 The neural pathways of the pupillary light reflex (left) and the accommodation reflex (right).

(From Oxford Textbook of Functional Anatomy, Vol 3 Head and Neck, MacKinnon P, Morris J (eds) 1990. By permission of Oxford University Press.)

Accommodation is usually accompanied by constriction of the pupil brought about by contraction of the sphincter pupillae (see p. 682) and convergent eye movements caused by contraction of the medial, superior, and inferior recti (all innervated by the oculomotor nerve). This is the ‘near triad’ which may become disrupted in various diseases.

Supraciliary layer

The thin supraciliary layer separates the sclera from the ciliary muscle and is largely composed of collagen fibres derived from the two layers it divides. It also forms an alternative ‘unconventional’ route (other than the canal of Schlemm) for the drainage of aqueous humour (see p. 686).