Ординатура / Офтальмология / Английские материалы / Hyperopia and Presbyopia_Tsubota, Boxer Wachler, Azar_2003

In an attempt to prove his accommodative mechanism, Tscherning studied the behavior of bovine lenses (Fig. 5). He observed that when inward pressure was applied at the lens equator, the anterior and posterior surface curvatures flattened; but when outward zonular tension was applied at the lens equator, the anterior surface curvature increased. Schachar also performed similar experiments on bovine lenses to provide experimental support for his accommodative mechanism and recorded an increase in optical power of the lens with outward-directed zonular tension at the lens equator (33). The bovine eye and lens bear little resemblance to that of the primate. The bovine eye is unlikely to accommodate, since it has a diminutive ciliary muscle (34) and a lens that is considerably thicker, more spherical, and harder than the primate lens. The paradoxical optical results that Tscherning and Schachar et al. (28,35) observed from tests on bovine lenses may be due to the fact that the bovine lens is structurally and functionally quite different from the primate lens. It is inappropriate to draw conclusions on the accommodative performance of the primate lens or on the primate accommodative mechanism from observations of the

Figure 5 Tscherning (Ref. 28.), like Schachar et al. (33), performed experiments on bovine lenses.

(A) When Tscherning applied a squeezing force to the equator of the bovine lens, a peripheral flattening and central steepening resulted (solid line) relative to unstressed lens (dashed line). (B) Tscherning believed that the nucleus was harder and had steeper curvatures than the surfaces of the lens and so provided a resistive force around which the cortex is molded. (C) When Tscherning applied a stretching tension to the lens equator (solid line), the softer lens cortex was molded around the hardened nucleus such that there is an increase in curvature at the center of the lens relative to the unstretched lens (dashed line). Note that there is no change in thickness of the lens with either squeezing or stretching. While this may be an accurate depiction of the behavior of the bovine lens, this lens is harder and more spherical than that of the primate lens and is from an animal that probably has no accommodation. Results from studies on bovine lenses cannot be extrapolated to prove anything about the accommodative performance of the human lens or the accommodative mechanism of the human eye. It is well established, for example, that there is an increase in axial thickness of the human lens during accommodation. (From Ref. 28.).

performance of bovine lenses. Tscherning found no change in axial thickness of the bovine lens with stretching, and Schachar (33) does not mention lens thickness. It is well established that the lens thickness increase by 10% with accommodation in the human eye (35,36). Our recent results show a 23% increase in lens thickness with 12D of accommodation in young rhesus monkey eyes (unpublished observations). When accommodation tests are performed on primate lenses known to be capable of accommodation, very different results from those of Tscherning and Schachar are found. Outward-directed zonular tension applied to young primate lenses causes a decrease in power due to flattening of the lens surface curvatures, in accordance with the Helmholtz accommodative mechanism (11). The extent of change in lens power at any age matches the expected accommodative amplitude (11). It is possible to demonstrate paradoxical optical effects of mechanical stretching on bovine lenses (33), artificial fluid-filled lenses (37–39), or air-filled Mylar balloon lenses (40). However, these lenses bear little resemblance to the primate lens, so there is little that can be concluded about accommodation in primates from tests on such lenses.

Both Tscherning’s and Schachar’s theories require some part of the anterior-internal aspect of the ciliary muscle to recede to increase zonular tension at the lens equator during accommodation. Subsequent to Helmholtz’s description of accommodation, even Tscherning (28) himself was aware of reports that described how, in aniridic patients, the ciliary processes could be observed to move (“swell”) toward the lens equator and that the lens diameter was observed to decrease with accommodation. Lens diameter is observed to decrease with accommodation in human eyes (41). Ultrasound biomicroscopy and goniovideography shows similar accommodative movements in monkey eyes (Fig. 6) (42). These observations contradict the mechanistic descriptions of Tscherning and Schachar. Schachar has postulated how the ciliary muscle contracts to increase zonular tension based on an analysis of a histological section (43). However no direct evidence exists to support the proposed movements of the ciliary muscle, and ultrasound biomicroscopy of the accommodative movements of the ciliary body (42) does not support the mechanism of action required by Schachar.

L. MEASUREMENT OF ACCOMMODATION

Tscherning begins his chapter on the accommodative mechanism with a section on the measurement of the amplitude of accommodation, in which he writes “to determine [the near point] exactly is generally of little practical importance.” The significance of this misconception is no more certain than today. Despite claims that accommodation is restored in presbyopes, there are no published objective measurements to demonstrate this. Subjective near reading tests used to determine if scleral expansion restores accommodation (44) are inaccurate and unreliable and do not unequivocally measure accommodation. The only documented attempt to measure accommodation postoperatively in scleral expansion patients using objective methods found none (45). Accurate, objective measurement of accommodation is imperative to establish the efficacy of surgical procedures claimed to restore accommodation. Tscherning did not have access to infrared optometers and other objective instruments that are available today to measure accommodation. Unlike the push-up test that is used clinically, these instruments are capable of unequivocally measuring accommodation dynamically and objectively. While the push-up test provides an indication of near reading ability, in some cases this may have no relationship to accommodative ability. For example if the push-up test were used to measure accommoda-

Figure 6 Recent experiments on iridectomized rhesus monkeys using Edinger-Westphal stimulated accommodation are in agreement with the Helmholtz accommodative mechanism (42). (A) A gonioscopy lens placed on the temporal cornea allows visualization of the ciliary processes and lens equator. (B) The movements of these structures can be observed during accommodation. (C) The subtracted image pair shows that the eye remains relatively stable during accommodation, but there is a pronounced movement of the ciliary processes and lens equator away from the sclera with accommodation. (D) The ciliary muscle and lens equator can be observed with ultrasound biomicroscopy (UBM). (E) The apex of the ciliary muscle and the lens equator move away from the sclera during accommodation. (F) The subtracted image pair shows that while the eye is relatively stable, the ciliary muscle and lens equator move away from the sclera during accommodation. (G) The entire equatorial diameter of the lens can be seen when a Goldman lens is placed on the cornea.

(H) With accommodation, there is a concentric decrease in equatorial diameter of the crystalline lens and an inward movement of the ciliary processes. (I) The subtracted image pair shows that the eye remains relatively stable relative to the pronounced accommodative movements that are observed. Each of the movements observed are in accordance with the Helmholtz accommodative mechanism and opposite to those proposed by Schachar. The accommodative movements observed, such as a concentric decrease in lens diameter (G–I), cannot be explained by eye movements. (From Ref. 42.)

tion in a presbyope wearing multifocal contact lenses, one might erroneously conclude that active accommodation is present. The multifocal contact lenses may provide functional distance and near reading ability but obviously without restoring accommodation. Clearly the push-up test does not unequivocally measure accommodation and cannot differentiate multifocality from functional accommodation. An objective optometer that dynamically measures the refraction of the eye is the appropriate method to unequivocally demonstrate the presence of accommodation.

While Tscherning may not have appreciated the importance of accurate measurement of accommodation, he was aware of good methods to stimulate accommodation. Tscherning described the use of topical instillation of a muscarinic agonist to stimulate accommodation. Muscarinic agonists such as pilocarpine and carbachol act directly on the acetylcholine receptors of the ciliary muscle and cause it to contract. If the optical refractive power of the eye is measured with an objective optometer before and after the instillation of topical pilocarpine, for example, the optometer will record a change in refraction as accommodation occurs. Depending on the drug’s concentration, its penetration into the eye, and the amount absorbed by the ciliary muscle, the accommodative response may vary. While pharmacological stimulation may not stimulate maximal accommodation and would therefore not provide an accurate measure of the full accommodative amplitude, it will provide an objective demonstration of whether accommodation is present.

M. HELMHOLTZ’S CONTRIBUTION

From his observations of the eye during accommodation, Helmholtz noted that the anterior surface of the crystalline moves forward and that the anterior lens surface curvature increases (a decrease in the radius of curvature). This latter observation was demonstrated by observing the minification of the third Purkinje image reflected from the anterior lens surface. Helmholtz also observed an apparent minification of the posterior lens surface’s Purkinje images and concluded from calculations that the curvature of the posterior lens surface increases slightly with accommodation but without appreciable movement of the posterior lens surface. Helmholtz suggested that these observations meant that the lens axial thickness increased by about 0.5 mm with accommodation and, that since the lens volume is constant, the equatorial diameter of the lens must be reduced with accommodation.

As to the mechanism by which the observed accommodative changes occur, Helmholtz was less certain due to the difficulties in observing the accommodative movements of the ciliary body directly.

Prior to Helmholtz, Cramer and Donders believed that the iris and the ciliary muscle induced accommodation of the lens. They supposed that the iris pushed backward on the peripheral anterior surface of the lens and that the ciliary muscle increased the vitreous pressure behind the lens. Helmholtz recognized that this was inconsistent with the increase in lens thickness that he had observed. Helmholtz believed that the mechanism proposed by Cramer and Donders would tend to decrease lens thickness and flatten the posterior lens surface.

Helmholtz believed that when the eye is focused at distance, the lens is stretched by the zonule attached to the lens equator. Based on an understanding of the anatomical attachment of these zonular fibers to the ciliary body, Helmholtz hypothesized that with a contraction of the ciliary muscle, the zonular insertion in the ciliary body is moved toward the lens to release the tension at the lens equator, allowing a decrease in lens diameter, an increase in lens thickness, and an increase in both lens surface curvatures.

Observations of accommodation in a patient with a paralyzed iris and in another with a completely detached iris convinced Helmholtz that the iris did not cause the accommodative change in the lens.

Helmholtz also observed that the form of the lens is changed and that it becomes thicker on cutting the zonule. He did not believe that the lens was composed of a lens muscle (musculus crystallinus), as others had suggested, but, in describing the accommodative mechanism, he also failed to provide an explanation why this change in the form of the lens occurs.

From his observations, Helmholtz ultimately concluded that the ciliary muscle was responsible for inducing accommodation. Helmholtz was aware of Mu¨ller’s (5) description of circular fibers of the ciliary muscle and appreciated that it acted as a sphincter muscle in conjunction with the meridional and radial fibers. In particular, a contraction of the circular and meridional fibers moves the tip of the ciliary processes toward the lens equator to release zonular tension. Helmholtz was unsure if the ciliary processes push directly on the lens equator, as occurs in birds eyes with accommodation, since he could not directly observe the edge of the lens. Although this is unlikely to occur in human eyes, it is observed to occur at maximum accommodation in iridectomized monkey eyes (42).

Thus, Helmholtz recognized that, at rest, zonular tension pulls outward on the lens equator and that a contraction of the ciliary muscle moved the ciliary processes toward the lens equator and released tension on the zonule, allowing an increase in lens anterior and posterior surface curvatures, an increase in lens thickness, a decrease in lens diameter, a forward movement of the lens anterior surface, and little or no movement in the posterior lens surface.

Although Helmholtz provided a comprehensive and accurate description of how accommodation occurs, he gave no indication of how or why the lens becomes accommodated, simply assuming that it did this through its supposed elasticity. He made no mention of a role for the lens capsule, the posterior zonular fibers, or the elasticity of the posterior attachment of the ciliary muscle to the choroid, all anatomical structures now known to play important roles in accommodation. Helmholtz also believed that the posterior lens surface does not move with accommodation, but this is now well documented to occur (46,47).

N. GULLSTRAND’S CONTRIBUTION

Gullstrand also contributed to our current understanding of accommodation in the appendix to Helmholtz’s posthumous third edition of the Treatise on Physiological Optics. Gullstrand’s descriptions built on the groundwork that Helmholtz had laid.

On summarizing the knowledge concerning the lens posterior surface, Gullstrand wrote: “The only definitive conclusions that can be drawn from these investigations is that as yet there is no proof of a change in position of the posterior surface of the lens in accommodation, and that the curvature of the posterior surface of the lens increases in accommodation, though to a very slight extent.”

Gullstrand’s investigations suggested that with accommodation, the anterior lens surface radius of curvature decreased from 10.0 to 5.33 mm and that the anterior lens surface moved forward by 0.4 mm. More recent measurements suggest forward movement of the anterior lens surface of between 0.2 to 0.3 mm with accommodation (46).

Gullstrand inferred a role for the lens capsule in describing the intracapsular accommodative mechanism. He described that the lens undergoes accommodative changes as a consequence of the extracapsular accommodative changes.

Helmholtz had correctly postulated that zonular tension at the lens equator is released during accommodation. Gullstrand showed that evidence for this had been presented by Hess (48), who demonstrated that, with a strong accommodative effort, the lens sags downward in the direction of gravity, that there is an increase in amplitude of accommodation when the head is bent forward and a decrease when the head is bent backward, and that the lens sags sagittally downward in the frontal plane after administration of eserine to induce accommodative spasm.

O. FINCHAM’S CONTRIBUTION

Fincham (13) made significant contributions to what we understand about accommodation today. He showed that the zonule is an elastic tissue and repeated observations made by Tscherning, Helmholtz, and others on the accommodative changes in curvature, lens thickness, anterior chamber depth, and vitreous chamber depth. Fincham identified that the lens thickness increases to a greater degree than the anterior chamber decreases with accommodation and therefore that the lens posterior surface moves backward with accommodation. From his measurements of accommodation in an eye with traumatic aniridia, Fincham observed centripetal movement of the ciliary processes and a smaller decrease in lens diameter. He also observed that with accommodation, both the lens nucleus and lens surface undergo similar change in curvature, demonstrating that the whole of the lens substance rather than just the lens cortex is involved in accommodation. Together with Graves (49), Fincham observed that in the empty capsular bag of a patient with traumatic aphakia, the anterior and posterior capsular surfaces were flattened and parallel to each other in the unaccommodated state but became flaccid, widely separated, and wrinkled during an accommodative effort. Fincham concluded that the capsule is held under tension in the unaccommodated state and that the tension is released with accommodation. Fincham also measured greater changes in the anterior chamber depth with accommodation when a subject is looking down than when looking forward, supporting an accommodative release of zonular tension. He observed, in a young enucleated eye, that the lens takes on a more accommodated form, with increased anterior surface curvature, when the zonule is cut and the lens freed from the zonular suspension and that when the capsule is removed, the lens substance tends to take on the unaccommodated form. All these observations led Fincham to the inevitable conclusion that accommodation is caused by capsular molding of the plastic lens substance into an accommodated form. Fincham studied the capsules of various animal species in histological section and found them to be of relatively uniform thickness in nonaccommodating mammals, but in humans it was thinnest at the posterior pole and of maximum thickness on the anterior surface about 2 mm from the equator and on the posterior surface about 1 mm from the equator. Fincham described how these variations in capsular thickness allow the lens polar surfaces to undergo steeper changes in curvature with accommodation than the peripheral lens surfaces, thus allowing the accommodated lens to take on a conoidal form. Finally, Fincham restates the Helmholtz accommodative mechanism, but now with the recognition that resting zonular tension pulls the lens into a flattened and unaccommodated form and that the capsular forces mold the lens into an accommodated form when zonular tension is released. Fincham recognized that presbyopia and the loss of accommodative amplitude can be explained simply by the lens substance losing its elasticity and the capsule failing to be able to mold the hardened lens. In accordance with Smith’s (22) observation that the equatorial diameter of isolated lenses does not reflect the diameter of the lens in the living eye, Fincham stated that when

Figure 7 (A) Fincham (13) showed that the primate lens capsule is not of uniform thickness. A diagram of the capsule, in which thickness is exaggerated relative to size, shows the posterior surface to be thinner than the anterior surface and regions of increased thickness on the anterior and posterior peripheral surfaces. The elasticity of the capsule provides the force to mold the lens substance into an accommodated form. In the absence of the capsule, the lens substance is in a flattened and maximally unaccommodated form. When outward-directed zonular tension is released with accommodation, the capsule molds the lens to increase the lens anterior and posterior surface curvatures.

(B) In support of this capsular theory of accommodation, Fincham cites the evidence from Graves (49) of the behavior of the empty capsular bag in a patient with traumatic aphakia. In the unaccommodated state, the anterior and posterior capsular surfaces were flat against each other. With a voluntary accommodative effort, the two surfaces became more flaccid and separated slightly. After the iris was dilated and accommodation was stimulated with eserine, the two surfaces of the capsule separated widely and the posterior surface (P) moved backward in the eye, becoming flaccid and wrinkled, while the anterior surface (A) showed a forward curve. (From Ref. 13.)

removed from the eye and isolated from external zonular forces, younger lenses tend to become accommodated while older presbyopic lenses do not undergo a change in shape.

P.EVIDENCE AGAINST SCHACHAR’S THEORY OF ACCOMMODATION

While Schachar’s theory of accommodation has been widely discussed, when scrutinized with results from the nearly 150 years of research on accommodation since Helmholtz, numerous inconsistencies appear. Schachar’s theory requires that accommodation occur through an increase in the lens surface curvatures consequent to an increase in zonular tension at the lens equator, but without any significant change in the lens thickness. If anything, increased tension on the zonule at the lens equator would be expected to decrease its thickness. However, the lens is well documented to undergo an increase in axial thickness with accommodation. This is readily documented by A-scan ultrasonography (50) but has most convincingly been documented by studies in which an ultrasound transducer was vacuum suctioned to the sclera of the eye to ensure that the transducer did not move with respect to the axis of the eye when accommodation occurred (36). In addition, increases in lens thickness have also been measured during accommodation to an aligned optical target with partial coherence interferometry, a noncontact, high-precision measurement technique (46). These studies show a 0.5-mm increase in the lens axial thickness with accommodation. An increase in thickness of this magnitude could not occur under Schachar’s theory, with an increase in zonular tension. These studies of accommodative changes in the lens also show that the lens posterior surface moves backward in the eye to decrease vitreous chamber depth and that the lens anterior surface moves forward to decrease anterior chamber depth. It is impossible, under Schachar’s theory, to explain how lens thickness can increase and anterior chamber depth and vitreous chamber depth decrease during accommodation with an increase in zonular tension at the lens equator.

Schachar’s theory requires that that the zonule at the lens equator be composed of three separate and distinct subgroups—anterior, posterior, and equatorial bundles (43,51). Scanning electron micrographic studies (6) and direct examination of the zonule in enucleated human eyes (11) do not support this view. Further, Schachar’s theory requires that the equatorial zonular fibers be attached to the anterior face of the ciliary muscle just beneath the root of the iris—the region of the ciliary muscle that Schachar believes to move outward to selectively increase the tension on the equatorial zonular bundle (43). Direct examination of the ciliary body shows that the zonular fibers attach all along the pars plicata and not to the anterior face of the ciliary muscle, as required by Schachar’s theory. Ultrasound biomicroscopy shows this anterior face of the ciliary muscle to move forward with accommodation (42) rather than backward, as required by Schachar’s theory.

Schachar’s theory requires that the lens equator move toward the sclera by 50 m with accommodation (52). Independent experiments have imaged movements of the lens equator in several different ways during centrally or pharmacologically stimulated accommodation in iridectomized monkey eyes (42). Swan-Jacob gonioscopy and ultrasound biomicroscopy showed a 0.25-mm movement of the lens equator away from the sclera during accommodation. Imaging with a Goldman lens showed a concentric decrease in the crystalline lens diameter with accommodation. Pharmacologically stimulated accommodation, not subject to the systematic convergent eye movements that occur with centrally stimulated accommodation, also showed movement of the lens equator away from the

sclera and a concentric decrease in lens diameter. The lens was also observed to sag downward under the influence of gravity during accommodation irrespective of the orientation of the head, thus demonstrating that zonular tension is reduced rather than increased as required by Schachar’s theory. Sutures were placed beneath the medial and lateral rectus muscles to reduce eye movements that occur with centrally stimulated accommodation.

Q. EVIDENCE AGAINST SCHACHAR’S THEORY OF PRESBYOPIA

Schachar’s theory of presbyopia also fails on scrutiny at many levels. Fundamental to Schachar’s theory of presbyopia is his claim that the lens grows throughout life, increasing in equatorial diameter by 20 m per year. It is this increased lens diameter that Schachar suggests results in crowding of the posterior chamber with a consequent loss of resting zonular tension. Schachar’s claims for an increase in lens diameter come from a single study in which lens diameter was measured in isolated human lenses (22). Rafferty (23) cites this study when stating that the lens undergoes an increase in diameter of 0.02 mm/ year. Rafferty (23) is the single source cited by Schachar to support the notion that the lens grows in equatorial diameter (24,25,40,51–53). Smith (22) recognized that his measurements of the diameter of the isolated lens do not reflect the diameter of the lens in the living eye. Smith (22) states that when the lens is removed from the eye, it undergoes a change in shape becoming more accommodated, relatively more so for the younger than the older lenses. These data do not reflect equatorial growth of the lens. Only recently has technology become available to measure lens diameter in vivo in living human eyes. Lens diameter measured with MRI in living eyes shows no increase with increasing age (26). The MRI study does show an age-dependent decrease in circumlental space or distance between ciliary processes and lens equator. However; this is clearly not due to increased lens diameter but may be due to an age-related change in configuration of the ciliary body (54).

Based on his theory of accommodation and presbyopia, Schachar has suggested that accommodation can be restored by scleral expansion (24). Setting the numerous problems with Schachar’s theory of accommodation aside, under the classic notion that presbyopia occurs due to an increased hardness or “sclerosis” of the lens, it is hard to understand how accommodation could be restored by scleral expansion. Mechanical stretching experiments of human eye bank eyes suggests that the presbyopic lens is incapable of being made to undergo accommodative changes (11). These experiments show that young lenses can be made to undergo accommodative changes in focal length matching accommodative amplitudes in youth, but that when lenses over the age of 60 years are subjected to the same mechanical tests, they fail to undergo any change in focal length. This result is supported by the MRI studies showing that in presbyopes, accommodative movements of the ciliary body occur, but without changes in the lens (26). The human lens undergoes a fourfold increase in hardness over the human life span (16). Scleral expansion cannot restore the accommodative capacity to the crystalline lens. While scleral expansion possibly may increase resting zonular tension or even enhance the efficacy of ciliary muscle contraction, this is unlikely to provide sufficient force to enable presbyopic lenses to accommodate. In any event, whatever serendipitous beneficial consequences scleral expansion surgery may have would be undermined by the inevitability of cataract and the required removal of the crystalline lens in cataract surgery.

R.DOES SCLERAL EXPANSION SURGERY RESTORE ACCOMMODATION?

Regardless of the accommodative mechanism or the causes of presbyopia, it is theoretically possible that scleral expansion surgery may restore accommodation through some unknown mechanism. However, the only published objective measurements of accommodation in patients with postoperative scleral expansion show that no accommodation is restored (45). Subjective tests suggest that near reading distance may be temporarily improved following scleral expansion (44). It is not clear why this would occur. The pushup or near reading test that is typically used to assess accommodation postoperatively is inappropriate to determine if accommodation occurs. The push-up test does not unequivocally measure accommodation and is subject to errors due to depth of focus of the eye and ocular aberrations. By definition, accommodation is a dioptric change in optical power of the eye. If accommodation occurs, this can be measured with objective instrumentation designed to measure the optical power of the eye. Unilateral scleral expansion surgery reportedly improves near vision bilaterally. A physiological explanation for this is unlikely, but it may reflect the inadequacy of subjective accommodation testing. It is possible, for example, that scleral expansion surgery may inadvertently introduce corneal or lenticular aberrations or some degree of multifocality to the eye. While this may prove beneficial to provide some degree of functional near vision, it is clearly not accommodation. Schachar has suggested that this is not the cause of the improved near vision, since keratometry is unaltered by scleral expansion (24). However, this does not address the possibility of aberrations in the lens. In addition to instrumentation available to measure accommodation objectively, excellent wavefront technology exists to objectively measure the aberrations of the eye. These measurements should be made preand postoperatively, in conjunction with objective and appropriate measurements of accommodation to demonstrate if there are any benefits to scleral expansion.

REFERENCES

1.von Helmholz H. Ueber die Accommodation des Auges. Arch Ophthalmol 1853; 1:1–74.

2.von Helmholz HH. Handbuch der Physiologishen Optik. In: Southall JPC, trans. Helmholtz’s Treatise on Physiological Optics. New York: Dover, 1962:143–172.

3.Tamm ER, Lu¨tjen-Drecoll E. Ciliary body. Micro Res Tech 1996; 33:390–439.

4.Bru¨cke E. Ueber den Musculus Cramptonianus und den Spannmuskel der Choroidea. Arch Anat, Physiol Wissenschaft Med 1846; 1:370.

5.Mu¨ller H. U¨ ber einen ringfo¨rmigen Muskel am Ciliarmuskel des Menschen und u¨ber den Mechanismus der Akkommodation. Graefes Arch Ophthalmol 1858; 3:1.

6.Rohen JW. Scanning electron microscopic studies of the zonular apparatus in human and monkey eyes, Invest Ophthalmol Vis Sci 1979; 18:133–144.

7.Glasser A, Croft MA, Brumback L, Kaufman PL. Ultrasound biomicroscopy of the aging rhesus monkey ciliary region. Optom Vis Sci 2001; 78(6):417–424.

8.Farnsworth PN, Burke P. Three-dimensional architecture of the suspensory apparatus of the aging lens of the rhesus monkey. Exp Eye Res 1977; 25:563–576.

9.Schachar RA. Zonular function: a new hypothesis with clinical implications. Arch Ophthalmol 1994; 26:36–38.

10.McCulloch C. The zonule of Zinn: its origin, course, and insertion, and its relation to neighboring structures. Trans Am Ophthalmol Soc 1954; 52:525–585.

11.Glasser A, Campbell MCW. Presbyopia and the optical changes in the human crystalline lens with age. Vision Res 1998; 38:209–229.