STRUCTURE

The ciliary body is the portion of the uveal tract that lies between the iris and the choroid ( Fig. 2-1 ). On cross-section, the ciliary body has the shape of a right triangle. It is attached anteriorly to the scleral spur, creating a potential space (supraciliary space) between itself and the sclera. The iris inserts into the short anterior side of the ciliary body, leaving a narrow width of ciliary face visible on gonioscopy between the peripheral iris and the scleral spur. The lens is attached to the ciliary body by the zonules, which separate the vitreous compartment posteriorly from the aqueous compartment anteriorly ( Fig. 2-2 ). The iris in turn divides the aqueous space into the posterior and anterior chambers. The junction of the iris, sclera, and cornea is called the anterior chamber angle.

Light micrograph of the anterior segment of the eye showing 1, Tenon’s capsule; 2, episclera; 3, sclera; 4, lamina fusca; 5, ciliary body; 6, Schlemm’s canal; and 7, peripheral cornea.

Courtesy of William H Spencer, MD.

Schematic view of the zonules separating the vitreous cavity from the posterior chamber and the iris separating the anterior and posterior chambers.

The ciliary body is composed of muscle, vascular tissue, and epithelium. The ciliary muscle consists of three separate muscles – the longitudinal (meridional), the oblique (radial or intermediate), and the circular (sphincteric). The longitudinal muscle attaches anteriorly to the scleral spur and trabecular meshwork and posteriorly to the suprachoroidal lamina, with some fibers connecting to the choroid and sclera as far posteriorly as the equator of the globe. When the longitudinal muscle contracts, it pulls open the trabecular meshwork and Schlemm’s canal. The circular muscle fibers run parallel to the limbus. When these fibers contract they relax the zonules, allowing the lens to change shape. The radial muscle connects the longitudinal and circular muscles. The function of the radial muscle is not entirely clear, but it is postulated that contraction of the radial fibers may widen the uveal trabecular spaces. It is possible that some or all of the insertions of these ciliary muscle tendons are into an elastic fibrillar network which makes the resultant actions difficult to sort out.

The ciliary body runs from the scleral spur to the ora serrata, a distance of approximately 6 mm (see Fig. 2-1 ). The posterior portion of the ciliary body has a relatively flat inner surface and is named the pars plana. The anterior portion of the ciliary body has approximately 70 to 80 radial ridges (the ciliary processes) on its inner surface and is named the pars plicata ( Fig. 2-3 ). The ciliary processes are approximately 2 mm in length, 0.5 mm in width, and 0.9 mm in height. The surface area of the pars plicata is estimated to be 5.7 cm ² in rabbits and 6 cm ² in humans. Thus the pars plicata has a large surface area (approximately five times the surface area of the corneal endothelium) for both active fluid transport and ultrafiltration.

Scanning electron micrograph of the ciliary processes (C) showing the valleys (V) and the zonular insertions (×155).

From Tripathi RC, Tripathi BJ: Anatomy of the human eye, orbit, and adnexa. In: Davson H, editor: The eye, vegetative physiology and biochemistry, vol. 1 A, 3rd edn., New York, Academic Press, 1984.

Because of the invagination of the embryonic optic vesicle, the inner surfaces of both the pars plana and the pars plicata are lined by two layers of epithelium – an outer pigmented layer that is continuous with the retinal pigment epithelium, and an inner non-pigmented layer that is continuous with the retina ( Fig. 2-4 ). The two layers of the epithelium have their apical surfaces in apposition.

(A) Light micrograph of the ciliary processes (CP), with connective tissue stroma (CT) between the ciliary muscle (CM) and the two epithelial layers. The vessels extend into the processes, and the stroma also contains melanocytes and fibroblasts (×197). (B) Extension of the vessel layer into the ciliary process. The beaded appearance (arrows) of the thin endothelial lining of the capillary (C) is due to ultramicroscopic fenestrations increasing capillary permeability for the formation of aqueous humor (photomicrograph; × 800). The pigmented and non-pigmented epithelial layers are demonstrated.

From Tripathi RC, Tripathi BJ: Anatomy of the human eye, orbit, and adnexa. In: Davson H, editor: The eye, vegetative physiology and biochemistry, vol. 1 A, 3rd edn., New York, Academic Press, 1984.

ULTRASTRUCTURE OF THE CILIARY PROCESSES

Each ciliary process is composed of a central core of stroma and capillaries covered by a double layer of epithelium (see Fig. 2-4B ). The capillary endothelium is thin and has tiny fenestrae that face toward the pigmented ciliary epithelium. The capillary endothelium is surrounded by a basement membrane that contains mural cells (pericytes).

The vascular tissue is surrounded by a thin stroma composed of ground substance, collagen fibrils, and occasional wandering cells. The ground substance contains mucopolysaccharides, protein, and a solute of plasma.

The pigmented epithelium is composed of low cuboidal cells with numerous cytoplasmic melanin granules ( Fig. 2-5 ). This layer is separated from the stroma by an atypical basement membrane, a continuation of Bruch’s membrane containing collagen and elastic fibers. The function of the pigmented epithelium is not entirely clear. The basal portion of this layer has a great number of infoldings and mitochondria, suggesting a role in active metabolic processes. The cytoplasm and cell membrane of the pigmented epithelial cells stain for the presence of carbonic anhydrase.

Schematic view of non-pigmented and pigmented ciliary epithelium.

Modified from Shields MB: Textbook of glaucoma, 2nd edn., Baltimore, Williams & Wilkins, 1987.

The non-pigmented epithelial layer is composed of columnar cells, which are separated from the aqueous humor by a basement membrane. The non-pigmented ciliary epithelium has the morphologic features of a tissue involved in fluid transport, including extensive infoldings in the basal and lateral membranes, numerous mitochondria, well-developed rough endoplasmic reticulum, and tight junctions connecting adjacent apical cell membranes (see Fig. 2-5 ). In addition, sodium-potassium adenosine triphosphatase (Na ⁺ -K ⁺ ATPase) is found near the lateral infoldings of the membranes. Rows of vesicles are seen near the free surface of the epithelium and were called pinocytotic vesicles in the past. It now appears that these vesicles are a fixation artifact.

The potential space between the two epithelial layers is called the ciliary channel. One group of investigators postulates that aqueous humor is secreted into this space, particularly after stimulation of the system with various agents, such as β-adrenergic agonists. This theory requires further study.

Adjacent cells within each epithelial layer and the apical surfaces of the two layers are connected by gap junctions, puncta adherentia, and desmosomes. Gap junctions are low-resistance pathways that provide electrical coupling of cells and facilitate transport of ions and other molecules from one cell to another. Some feel that these gap junctions allow the two kinds of epithelial cells to act as a functional syncitium. Evidence from studies in knock-out mice suggest that connexin43, a major component of the gap junction, is required for aqueous production and mice bred to exclude this component do not produce normal amounts or quality of aqueous humor. Puncta adherentia and desmosomes are structural supports between cell membranes. The non-pigmented ciliary epithelial cells are also joined at their apical membranes by tight junctions (zonulae occludentae), which are thought to be an important component of the blood–aqueous barrier. Tracers injected into the ciliary body pass through the stroma and the clefts between the pigmented epithelial cells until they reach the apical cell membranes of the non-pigmented ciliary epithelium, where they are restricted by the tight junctions. However, these tight junctions are permeable to low molecular weight polar solutes.

There is considerable evidence that aqueous humor is produced in the anterior portion of the ciliary processes. The anterior portion of the non-pigmented ciliary epithelium has morphologic features that indicate active fluid transport, including increased basal and lateral interdigitations, numerous mitochondria, and a well-developed rough endoplasmic reticulum. The epithelium is supplied by a rich capillary network with numerous fenestrations. With a gonioprism, systemically administered fluorescein can be observed entering the posterior chamber at the tips of the ciliary processes. Finally, the non-pigmented ciliary epithelium, especially in the region of the lateral interdigitations, shows evidence of abundant Na ⁺ -K ⁺ ATPase, considerable activity for glycolytic enzymes, and a high rate of incorporation of labeled sulfate into macromolecules, such as glycolipids and glycoproteins.

Many nerve terminals are seen in the connective tissue adjacent to the pigmented epithelium, but they do not appear to penetrate the basal lamina and reach the non-pigmented epithelium. These terminals appear to arise from sympathetic and parasympathetic fibers. In addition, the non-pigmented ciliary epithelial cells have β-adrenergic and cholinergic receptors. The function of these receptors and nerve terminals is not clear.

VASCULAR SUPPLY

The long posterior ciliary arteries arise as trunks from the ophthalmic artery, pierce the globe near the optic nerve, and run forward to the ciliary body, where they anastomose to form the major arterial circle ( Fig. 2-6 ). The anterior ciliary arteries also contribute to the major circle, but to a lesser extent than the long posterior ciliary arteries. Several pre-capillary arterioles branch from the major arterial circle to supply each ciliary process. These arterioles have sphincters that may play a role in regulating blood supply and aqueous humor formation. The pre-capillary arterioles break up into plexuses of tortuous vessels within each ciliary process. The vessels collect and flow into choroidal and pars plana veins, which then flow into the vortex system. Some drainage also occurs via the intrascleral veins to the episcleral veins.

Blood supply to the anterior segment of the eye. LPCA, long posterior ciliary artery; ACA, anterior ciliary artery; MAC, major arterial circle.

The ciliary body has a very high blood flow, estimated to be 81 μl/min in the monkey eye and, by calculation, 154 μl/min in humans. In cats, venous blood from the anterior uvea is only 4–5% less saturated with oxygen than is arterial blood. This indicates that oxygen consumption is not a limiting factor in aqueous humor formation under normal conditions. The rate of plasma flow to the ciliary processes in rabbits is at least 50 μl/min. If the rate of aqueous production is assumed to be 2–4 μl/min, the formation of aqueous humor removes only 4–8% of the volume of plasma available to the ciliary processes. Thus a modest reduction in the rate of plasma flow to the ciliary processes might not be expected to decrease aqueous humor formation substantially. However, animal models do indicate that aqueous humor production falls if ciliary blood flow is reduced by more than 30%. In fact, brimonidine, an α-adrenergic agonist commonly used for glaucoma treatment, may effect a reduction in aqueous formation by causing vasoconstriction of the ciliary body arterial supply.

The ciliary processes of many species, including primates, appear to have limited autoregulation of their blood supply. In general, the vascular responses of the ciliary processes are similar to those of the choroid but dissimilar to those of the iris and retina. Vasodilation of the ciliary blood vessels is seen following administration of carbon dioxide, application of prostaglandins, paracentesis, and parasympathetic stimulation. Vasoconstriction in the anterior uveal tract vessels occurs after stimulation of α-adrenergic nerves.

ULTRAFILTRATION

More than twice the weight of the ciliary processes themselves (or about 150 ml) of blood flows through the ciliary processes each minute. As blood passes through the capillaries of the ciliary processes, about 4% of the plasma filters through the fenestrations in the capillary wall into the interstitial spaces between the capillaries and the ciliary epithelium. The process by which a fluid and its solutes cross a semipermeable membrane under a pressure gradient (e.g., capillary blood pressure) is called ultrafiltration. In the case of the ciliary body, fluid movement is favored by the hydrostatic pressure difference between the capillary pressure and the interstitial fluid pressure (IOP) and is resisted by the difference between the oncotic pressure of the plasma and the aqueous humor.

The rate of protein leakage through the vessel walls into the tissue space of the ciliary processes is relatively low. However, the ciliary epithelial layers are even less permeable to the passage of colloids into the posterior chamber. Thus the colloid concentration in the tissue space of the ciliary processes is approximately 75% of that in plasma. The high concentration of colloids in the tissue space of the ciliary processes favors the movement of water from the plasma into the ciliary stroma but retards the movement of water from the stroma into the posterior chamber. Although a few investigators have postulated that ultrafiltration is responsible for the majority of aqueous humor formation, it is unlikely that the hydrostatic pressure difference between the ciliary capillaries and the posterior chamber can overcome the large oncotic pressure differential. Furthermore, a theory that proposes a predominant role for ultrafiltration does not explain why active ion transport inhibitors such as ouabain are capable of reducing aqueous humor formation by 70–80%. Thus ultrafiltration helps to move fluid out of the capillaries into the stroma but alone is insufficient to account for the volume of fluid moved into the posterior chamber. The latter step requires an active metabolic process. Ultrafiltration and active secretion occur in tandem.

ACTIVE TRANSPORT

Active transport (secretion) is an energy-dependent process that selectively moves a substance against its electrochemical gradient across a cell membrane. It is postulated that the majority of aqueous humor formation depends on an ion or ions being actively secreted into the intercellular clefts of the non-pigmented ciliary epithelium beyond the tight junctions ( Fig. 2-7 ). This process is accomplished by about a million non-pigmented epithelial cells, each of which secretes aqueous humor equal to about one-third of its own intracellular volume per minute. In the small spaces between the epithelial cells, the secreted ion or ions create sufficient osmotic forces to attract water. By the time the newly secreted fluid reaches the posterior chamber, the osmotic driving force has been nearly dissipated.

Pigmented and non-pigmented ciliary epithelium. Ions are secreted into intercellular clefts of the non-pigmented epithelial cells. The ions create sufficient osmotic force to attract water.

Modified from Lutjen-Drecoll E: Morphologic basis for aqueous humor formation. In: Drance SM, Neufeld AH: Glaucoma: applied pharmacology in medical treatment, New York, Grune & Stratton, 1984.

First, the dialysate from the plasma has to be transported into the pigmented epithelial cells. The best current evidence suggests that the paired Na ⁺ /H ⁺ and Cl ⁻ /HCO ⁻ antiports actively transport Na ⁺ and Cl ⁻ from the stroma into the cell. Intercellular gap junctions between the two cell layers appear to be critical. In addition, the natriuretic peptide precursor B (NPPB)-sensitive Cl channels at the basolateral surface in non-pigmented epithelial cells also play a crucial role in regulating the Cl movement across the functional syncytium.

It is not clear which ion or ions are actively transported across the non-pigmented ciliary epithelium, though most theories include sodium, chloride, and/or bicarbonate ( Table 2-2 ). Electrophysiologic studies of the isolated ciliary epithelium indicate that the transepithelial potential difference and the short circuit current, indicators of ion transport across membranes, are dependent on Na ⁺ and HCO ₃ ^−. A number of investigators postulate that the active transport of the sodium ion is the key process in aqueous humor formation. This theory is supported by the observation that membrane-bound ouabain-sensitive Na ⁺ -K ⁺ ATPase (the enzyme that facilitates transport of potassium into, and sodium out of, cells) is found in the non-pigmented ciliary epithelium of many different species, which explains the 70–80% reduction in aqueous humor seen with oubain.

Enough Na ⁺ and K ⁺ ATPase activity is present in the ciliary non-pigmented epithelium to drive aqueous humor formation mainly by the sodium gradient. However, the primacy of Na ⁺ as the driver for aqueous humor formation has been questioned in several species including rabbit, cat, and ox. Candia et al suggested that while active transport of Na ⁺ is important, it cannot account for the entire rate of aqueous formation in vivo. At least in the pig and some other mammals, Cl ⁻ is actively transported across the non-pigmented ciliary epithelium and may be the driving force of aqueous formation. Do & Civan have found that swelling-activated calcium channels in the non-pigmented ciliary epithelium modulate the formation of aqueous in both the cow and the mouse. The notion that chloride transport may be important at least in some species is supported by the observation that, unlike the rabbit, the concentration of chloride ion in bovine, ovine and porcine aqueous humor is higher than in plasma.

For many years investigators believed that the bicarbonate ion could not be actively secreted into the aqueous humor of the primate eye because the posterior chamber bicarbonate concentration is lower than the plasma concentration. However, more recent investigations indicate that bicarbonate is actually present in excess in newly formed posterior chamber aqueous humor. Bicarbonate appears to be in deficit in the aqueous humor because the fluid that is usually sampled has undergone metabolism and diffusional exchange with surrounding tissue. Carbonic anhydrase (CA) type II (isoenzyme C) is present in the cell membrane and cytoplasm of the non-pigmented and pigmented epithelium of the ciliary body. This enzyme catalyses the following reaction:

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