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Anatomy

Mina Pantcheva, MD; Malik Y. Kahook, MD; and E. Michael Van Buskirk, MD

The human eye is bound by 3 concentric, virtually spherical layers or coats: the outer fibrous layer, the cornea and sclera; the middle vascular layer, the uveal tract; and the inner neurosensory layer, the retina. The interior of the globe is divided into 3 compartments: the anterior chamber between iris and cornea, the posterior chamber between lens and posterior iris, and the vitreous cavity, posterior to the lens, comprising most of the ocular volume. The aqueous humor is contained by the posterior chamber and the anterior chamber and has a volume of about 200 μL.¹ Aqueous humor flows from the ciliary processes at about 2 to 2.5 μL/min.¹

The uveal tract attaches to the sclera at 3 sites: the optic nerve, the vortex veins, and the chamber angle. The latter consists of an inward roll of collagenous tissue, the scleral spur, that serves as the partial insertion of the ciliary muscle fibers that are important for maintenance of aqueous humor outflow and accommodation. These attachments can become clinically relevant especially after blunt trauma when shear forces between the ocular layers tear the ciliary muscle and uvea away from the scleral spur, leading to cyclodialysis, iridodialysis, or angle recession and secondary glaucoma.

AQUEOUS HUMOR OUTFLOW PATHWAYS

Aqueous humor leaves the eye primarily through the so-called conventional outflow pathways: the trabecular meshwork (TM), Schlemm’s canal, the aqueous humor collector channels, and the aqueous veins, to the episcleral veins, orbital veins, and the intracranial cavernous venous sinus. A substantial portion leaves by means of the uveoscleral outflow pathways, through the anterior chamber angle, the anterior extreme of the ciliary muscle, the posterior uvea, the suprachoroidal space, the sclera (perhaps along perforations for veins and nerves), and into the orbital tissues.^2,3 In contrast to conventional outflow, which is dependent upon the intraocular pressure (IOP), uveoscleral outflow is relatively pressure independent. It is enhanced by certain prostaglandins and can become significant in the inflamed eye, possibly contributing to the low IOP sometimes seen in uveitis. In addition, pharmacologic prostaglandin analog compounds, administered topically, appear to stimulate uveoscleral outflow and reduce IOP in glaucomatous eyes, even in those typically resistant to outflow-stimulating drugs, such as cholinergic agents. In addition, some absorption takes place through the iris, but this may not be physiologically or clinically significant.

CONVENTIONAL AQUEOUS HUMOR OUTFLOW PATHWAYS

A thorough understanding of the anatomy of the anterior chamber angle is essential for any clinician treating glaucoma as well as for scientists investigating this tiny but complex region. The precise proportions and relations of the various structures of the chamber angle are dependent on anatomic characteristics, such as size of the globe, the refractive error, the size and position of the lens, and physiologic factors associated with aqueous secretion, accommodative tone, venous pressure, and postural position. The peripheral iris, or iris root, blends with the anterior and medial fibers of the ciliary muscle to form the apex of the anterior chamber angle, posterior to the true TM and scleral spur (Figure 2-1). The ciliary muscle fibers then pass anteriorly to insert into the scleral spur and TM to complete the angle. Thus, the anterior chamber angle typically subtends about 30 degrees with the iris making one arm and the scleral spur, TM, and cornea comprising the other. The iris plane may vary from flat to slightly concave or convex, but is typically convex, with a smooth transition from the mid-iris to the angle apex.

THE TRABECULAR MESHWORK

The TM lies in the corneoscleral arm of the chamber angle, just anterior to the angle apex. It extends between the scleral spur posteriorly and the peripheral cornea or Schwalbe’s line anteriorly. Functionally, the scleral spur, ciliary muscle, TM, and Schlemm’s canal work as a single unit to comprise the conventional aqueous outflow pathways. The TM in cross-section is triangular in shape, its apex at the corneal periphery, in effect suspended from the peripheral extreme of Descemet’s membrane, Schwalbe’s line. The base of the triangular mesh is then formed by the scleral spur and the inner fibers of the ciliary muscle.

The inner wall of the meshwork faces the anterior chamber, and the outer comprises the inner wall of Schlemm’s canal. The TM may be divided into 3 histologically identifiable components: the most inner aspect, the uveal meshwork; the central component, the corneoscleral meshwork; and the outer aspect, the juxtacanalicular (JXT) tissue-inner wall of Schlemm’s canal (Figure 2-2). Outgoing aqueous humor passes through each element sequentially, from the uveal meshwork, through the corneoscleral meshwork, and then the JXT tissue to enter Schlemm’s canal.

The uveal meshwork is perhaps most variable from eye to eye and, hence, most difficult to define. During fetal development, an intact tissue layer extends from the cornea over the angle to the iris surface. During the final trimester, this layer undergoes a dissolution process as the remainder of the TM matures to accommodate aqueous outflow.⁴ The uveal meshwork contains large spaces between tissue lamellae and, thus, typically contributes little if any significant resistance to aqueous humor outflow. When the iridocorneal fetal tissue layer fails to undergo normal developmental dissolution in the final gestational trimester, this anomalous uveal meshwork tissue can block aqueous humor outflow, leading to so-called primary congenital glaucoma. Such membranes can be incised surgically to restore physiologic aqueous outflow. In other unusual circumstances, such persistent tissue layers apparently are sufficiently permeable to permit adequate IOP in early childhood but become clinically significant in adolescence with a visible uveal tissue layer covering the normal TM. The remaining uveal tissue remnants become the uveal meshwork and typically consist of strands of uveal tissue from the peripheral iris to the mid- or anterior corneoscleral meshwork. These are sometimes called iris processes, may contain melanin, and can be variably pigmented. In some cases, uveal meshwork strands extend all the way to Schwalbe’s line. Prominent uveal meshwork with iris processes are not particularly associated with glaucoma but are sometimes seen with various forms of congenital glaucoma. In others, the uveal meshwork has a diaphanous membranous quality. Usually, the uveal meshwork does not form a significant component to aqueous humor outflow resistance, but when substantial, probably can contribute, for example, in some congenital or juvenile-onset glaucomas.

The bulk of the TM consists of the corneoscleral portion, of about 10 to 15 perforated collagenous sheets, or layers, suspended between Schwalbe’s line or the peripheral cornea anteriorly and ciliary muscle or scleral spur posteriorly. The outer layers arise directly from the scleral spur, but the inner layers arise directly from insertions of the inner fibers of the ciliary muscle. Each lamella consists of a central collagen core, overlain by basement membrane and endothelial-type trabecular cells and a complex extracellular macromolecular interstitium. Trabecular cells form a variably intact monolayer to line the interstices of the meshwork. They are multipotential cells with great phagocytic and migratory capabilities in response to physiologic, pathologic, and injurious stimuli.5 The trabecular cells gradually diminish in density throughout life.⁶ This trabecular depopulation is accelerated in primary open-angle glaucoma.⁶ Stimulation of the trabeculum with some forms of mild injury, such as laser trabeculoplasty, appear to enhance trabecular cell division and migration, temporarily repopulating the tissue with newly formed cells.^7,8 The relative mechanical tension of the ciliary muscle fibers on the corneoscleral lamella plays a major role in modulating resistance to aqueous humor outflow, but the exact mechanism of this modulation is not well understood. The insertion of the longitudinal ciliary muscle fibers into the scleral spur and corneoscleral sheets is vital for maintenance and modulation of aqueous humor outflow. Shearing forces associated with the global distortion during blunt ocular trauma can disrupt the ciliary muscle insertion, leading to collapse of the TM against the scleral wall, increased trabecular outflow resistance, and severe glaucoma, known as angle recession. Because of the disinsertion of the ciliary muscle, conventional cyclotonic therapy with cholinergic-stimulating agents like pilocarpine becomes ineffective with angle recession.

The JXT tissue (or cribriform meshwork) comprises the most outer portion of the trabeculum and lies between the most outer corneoscleral lamella and Schlemm’s canal. This tissue is a more loosely organized, reticulated connective tissue composed of variable amounts of collagen, proteoglycans, glycoproteins, and hyaluronic acid.⁹ It is hypocellular compared to the corneoscleral meshwork. The outer aspect of the JXT tissue consists of the endothelial cells lining the inner wall of Schlemm’s canal. These are joined by tight junctions, but appear to be highly distendable, forming giant vacuoles in response to a pressure gradient across the TM.^10–13 The exact route by which aqueous humor passes from the interstices of the corneoscleral meshwork to the lumen of Schlemm’s canal is a topic of great research efforts. Arguments^11,12 have been advanced that pores develop between or through endothelial cells. Some^10,13 believe the formation and collapse of the giant vacuoles to be important to maintenance of aqueous humor outflow. In the JXT tissue, the outflowing aqueous humor directly encounters an extracellular tissue barrier through which it must percolate without access to open spaces. Thus, anatomically, this tissue, with the inner wall endothelial lining of Schlemm’s canal, appears to account for the principal component of aqueous humor outflow resistance, and experimental studies in monkeys and eye bank eyes confirm its primary importance.¹⁴ Moreover, accumulation of extracellular material in the JXT tissue, appearing as plaques in electron microscopic sections, is associated with open-angle glaucoma.¹⁵ Thus, the precise site of resistance to outflow in the normal and glaucomatous eye is not completely understood, but the peripheral JXT connective tissue and Schlemm’s canal inner wall appear to be the most likely location. Many of the pathophysiologic mechanisms cited (eg, cellular depopulation, plaque accumulation) also are associated with aging, but are accelerated and exaggerated in the glaucomatous eye.

Schlemm’s canal is an endothelial-lined aqueous conducting channel lying circumferentially parallel to, and contiguous with, the outer aspect of the TM; its inner wall endothelium comprises the outer lining of the JXT tissue (see Figure 2-2). The canal is oval shaped cross-sectionally, its posterior aspect determined by the scleral sulcus, lying within the scleral spur internally and posteriorly and with the scleral wall externally. Most of the inner aspect lies adjacent to the TM and anteriorly is bordered by the junction of the anterior meshwork and the cornea. Although the canal usually forms an intact circumferential channel, it is crossed by numerous septae from inner to outer wall and branches to multiple lumens in some locations. The outer wall is perforated by about 30 to 35 collector channels whose endothelium is contiguous with that of intrascleral veins. Although one can commonly observe retrograde flow of blood from these veins into the lumen of Schlemm’s canal, in the adult eye, most aqueous humor appears to travel radially across the lumen of the canal with little circumferential flow in the canal lumen.¹⁶

CILIARY BODY ANATOMY

The ciliary body lies posterior to the iris and comprises the ciliary muscle and ciliary processes (see Figure 2-1). Both structures possess unique morphologic features that are essential to their specialized functions for accommodation, outflow facility regulation, and aqueous humor formation.

The ciliary muscle subtends a triangular, cross-sectional profile with its apex pointing posteriorly, ending at the ora serrata. The outermost longitudinal fibers insert as tendinous bands into the corneoscleral TM and scleral spur, whereas the middle radial and inner circular fibers are only loosely adherent to the adjacent sclera via sparse collagen fibers. Ciliary muscle contraction decreases the resistance to outflow of aqueous humor, apparently through mechanical tension on the TM.

Lying internal to the ciliary muscle, the ciliary processes form the pars plicata, which, along with the more posterior pars plana, constitute the lateral wall of the posterior chamber (see Figure 2-1). Approximately 70 to 80 radially arrayed major ciliary processes project into the posterior chamber (Figure 2-3). Their anterior borders arise from the iris root, sweeping behind the iris to form the ciliary sulcus (see Figure 2-1). These major processes measure approximately 2 mm long, 0.5 mm wide, and 1 mm high and possess an irregular surface. Smaller, minor ciliary processes lie between the major processes and do not project as far into the posterior chamber.

In cross-section, the major ciliary processes manifest 3 components (Figure 2-4): an inner capillary core, a surrounding loose stroma, and a double-layered epithelium continuous with that of the pars plana. These components each possess unique morphologic features that underpin their contribution to aqueous humor formation, a 2-stage process that begins with passive ultrafiltration of plasma from the capillaries into the stroma followed by movement through the ciliary epithelium into the posterior chamber. Because the aqueous humor derives from the ciliary processes, reduction of IOP can be accomplished by disturbing the ciliary body pharmacologically or surgically. Many drugs block aqueous humor inflow by interfering with the normal secretory process in the epithelium or by reducing arteriolar perfusion of regional ciliary processes. Most of the pharmacologic agents, such as carbonic anhydrase inhibitors, beta-adrenergic antagonists, and alpha-2 adrenergic agonists, appear to act in this manner directly on the ciliary epithelium. Some of the vasoactive adrenergic agents also can induce localized arteriolar constriction in the anterior ciliary processes.¹⁷

Aqueous humor inflow can also be inhibited by destruction of some or all of the ciliary processes with cryotherapy or laser photocoagulation. The treating clinician must be aware of the anatomic location of the processes at the anterior portion of the ciliary body, about 1.5 to 2 mm posterior to the corneoscleral limbus, to achieve the most effective result with the least tissue destruction when using a transscleral approach.

CILIARY BODY MICROVASCULATURE

The ciliary body receives blood from 2 sources: the anterior ciliary arteries and the long posterior ciliary arteries. Branches from all of these arteries anastomose freely with each other to produce a complex, redundant system characterized by numerous collateral channels that ensure consistent anterior segment perfusion even after partial interruption of its arterial supply, such as following strabismus and retinal detachment surgery.¹⁸ Derived from the ophthalmic artery, 2 anterior ciliary arteries approach the limbus from the border of each rectus muscle with the exception of the lateral rectus, which contributes only one. Within the episclera, these arteries commonly branch and then interconnect, often forming a nearly complete anastomotic vascular ring that can occasionally be observed clinically.

At the limbus, several branches from each anterior ciliary artery turn inward, perforating the limbal sclera to enter the capillary bed of the ciliary muscle. These branches arborize within the ciliary muscle and interconnect with each other and with branches from the nasal and temporal long posterior ciliary arteries.¹⁸ These interconnections form a second anastomotic vascular ring, the intramuscular circle, representing the major source of collateral blood flow to the ciliary body between the anterior and long posterior ciliary arterial systems.

Other branches from the intramuscular circle pass anteriorly to the root of the iris, where they bend and branch at right angles to form the major arterial circle that lies tangential to the limbus. The major arterial circle is often discontinuous and may constitute the only minor contributor to anterior segment collateral blood flow (Figure 2-5).

The ciliary processes receive their arterial supply from 2 types of arterioles—anterior and posterior—that emanate from the major arterial circle.¹⁹ Anterior arterioles arise in tufts and often show focal constrictions as they span the ciliary sulcus. As they enter the processes, they rapidly dilate into irregular, large, vein-like capillaries that are initially directed anteriorly toward the ciliary process tip. These capillaries then turn and pass posteriorly within the internal margin of the process to empty into the choroidal veins. The posterior arterioles, generally less numerous and less constricted than the anterior, enter the basal regions of the ciliary processes, apparently to serve the basal and posterior regions of the ciliary processes. These capillaries also travel in a posterior direction, concentric to those from the anterior arterioles. Thus, capillaries derived from anterior arterioles serve the margins of the ciliary process, and those arising more posteriorly are situated within the base of the process. Interprocess connections also arise from the posterior arterioles and serve the minor ciliary processes on either side and the basal regions of neighboring major processes.

THE CILIARY EPITHELIUM

The ciliary epithelium actively secretes some components of aqueous humor and provides the barrier that prevents macromolecules from reaching the posterior chamber. The ciliary epithelium consists of 2 layers of cells, the outer pigmented and the inner nonpigmented, facing the posterior chamber. Despite its bilayered structure, the ciliary epithelium is not compound but consists of 2 simple epithelia joined apex to apex with the basal lamina of the pigmented layer resting on the stroma of the ciliary body and that of the nonpigmented layer lining the posterior chamber. This unusual arrangement results from invagination of the optic vesicle to form the optic cup during embryonic development.

The inner nonpigmented ciliary epithelium is continuous anteriorly with the pigment epithelium of the iris and posteriorly with the neurosensory retina at the ora serrata. The pigmented epithelium continues anteriorly as the anterior myoepithelium of the iris and posteriorly as the retinal pigment epithelium. The nonpigmented ciliary epithelial cells lack melanin and, compared with the cells of the pigmented epithelium, have more and larger mitochondria and rough endoplasmic reticulum, indicating a greater metabolic capacity. These features are amplified in the cells of the nonpigmented layer that lie in the anterior pars plicata whence derives the greater contribution overall to the production of aqueous humor.²⁰

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