Clinical background
Accommodation refers to a process whereby a change in position as well as increased curvature of the crystalline lens increases the conjugation power of the eye, i.e., its ability to converge an image to focus on the retina. This process allows for the focus of a near object of regard on the retina. The first well-recognized and now widely accepted theory of accommodation was proposed by Hermann von Helmholtz in 1856. Helmholtz’s theory posits that accommodation occurs through a relative rounding of the lens due to relaxation of the zonules, the fibrous elements that suspend the lens in place. The ciliary muscle attaching to the fibrous zonules contracts during accommodation, leading to relaxation of the zonules and therefore rounding of the crystalline lens. The change in shape of the lens leads to increased conjugation power of the eye, and therefore enhanced focus at near ( Figure 35.1 ).
As humans age, a well-established age-correlated decrease in accommodation occurs starting at just over the age of 40. This process is known as presbyopia. The causes of presbyopia are varied and include changes in the lens shape, size and compliance, as well as changes in the ciliary body and zonular structure.
Based on the various etiologies of presbyopia, multiple surgical approaches have been introduced for restoring accommodation in the presbyopic or pseudophakic population with variable effectiveness. These procedures can be broadly categorized into two groups: procedures intended to enhance the change in crystalline lens shape during accommodation that is attenuated in presbyopia, and procedures whereby the rigid and enlarged crystalline lens is removed and replaced by a multifocal or accommodative intraocular lens (IOL).
Pathology
Lens changes in presbyopia
The lens increases in thickness with age, with a 60-year-old lens having on average one-third greater volume than a 30-year-old lens ( Box 35.1 ). This is demonstrated by extensive cadaveric analysis, ultrasound, and scheimpflug biomicroscopy. In theory, a larger lens is more difficult to deform than a smaller lens. Mimicking zonular forces, Glasser and Campbell demonstrated that older lenses exhibit less change in focal length when stretched radially, both with and without the lens capsule. Fisher has studied in great detail changes in the elasticity and water content of the lens substance, and has demonstrated constant water content with increased stiffening of the lens substance with age. By Fisher’s mathematical modeling, these lens changes contribute 55% of presbyopia.
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Thickness of the crystalline lens increases
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The ciliary body muscular insertion becomes stiffer with age but the muscle itself retains contractility. Overall ciliary body muscle function decreases
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The lens capsule decreases in elasticity
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Zonular attachments migrate anteriorly
Ciliary body changes in presbyopia
An age-dependent decline in ciliary body movement, amplitude, and velocity was demonstrated by Croft et al through dynamic real-time videography in monkeys. This finding suggests that decreased functioning of the ciliary body itself may contribute to presbyopia. Poyer et al, however, found no evidence of variable muscle function with age by observing in vitro ciliary muscle contractility induced by cholinergic agents. Examination of rhesus monkey eyes by biomicroscopy and electron microscopy revealed that posterior tendons of ciliary muscle in older monkeys exhibited increased fibrillar material compared to those of younger monkeys. Increased mechanical stiffness of the posterior insertion of the muscle with age with preserved muscle contractility may therefore contribute to presbyopia.
Lens capsular changes in presbyopia
Fisher postulated that, if the lens capsule is truly elastic, it can transmit radial forces from zonules to the lens and alter the lens shape during accommodation without requiring an anteroposterior force, such as vitreous pressure. Fisher demonstrated that the lens capsule does have elasticity sufficient to deform the shape of the lens anteroposteriorly, as shown by centrifuging lenses to create a radial force mimicking zonules. Fisher’s work demonstrated that this elasticity appears to decrease precipitously with age, a process thought to contribute at least 40% of presbyopia. The lens capsule’s ability to mould the lens necessitates compliance of the lens matrix as well as sufficient force generated from the capsule. Both of these factors appear to decline with age.
Zonular changes in presbyopia
With age, the zonular attachments to the lens migrate anteriorly, likely due to the expansion of the lens size. With a greater tangential orientation of the zonules to the lens, zonules are less able to generate force, contributing to presbyopia.
Alternative theories of presbyopia
In 1994, Schachar proposed a theory of accommodation that rebukes the widely accepted Helmholtz theory ( Box 35.2 ). According to Schachar’s theory, zonular tension primarily increases during accommodation. As the anterior and posterior surfaces of the lens round during accommodation, the anterior and posterior zonules, those that are visualized by biomicroscopy in vivo, relax. Meanwhile, the more important equatorial zonules increase in tension during accommodation with contraction of the ciliary body. This leads to relative flattening of the peripheral lens, but steepening of the central lens. Following this theory, increased lenticular size with age decreases equatorial zonular tension, leading to presbyopia. Scleral expansion surgery may counteract presbyopia by reinstating equatorial zonular tension.
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Zonular tension increases during accommodation. Increased lenticular size with age decreases zonular tension, leading to presbyopia
By Schachar’s theory, increased equatorial zonular tension during accommodation should pull the lens equator toward the sclera. Glasser and Kaufman’s work contradicts Schachar’s theory by demonstrating in vivo that the lens equator moves away from the sclera during accommodation in monkeys induced by Edinger–Westphal stimulation as well as local pharmacologic agents. Their work also revealed a downward sag of the lens with gravity during accommodation, which further challenges Schachar’s theory.
Coleman proposed a theory in 1970 supporting a role for vitreous pressure in the processes of accommodation and presbyopia ( Box 35.3 ). His catenary theory states that the lens, zonules, and vitreous act as a diaphragm controlling differential pressures in the anterior and vitreous chambers. Ciliary body contraction during accommodation initiates movement of the diaphragm, creating a differential pressure gradient in the eye between the anterior chamber and the vitreous cavity. Coleman asserts that this pressure gradient is crucial in establishing a reproducible “catenary” shape of the anterior lens surface during accommodation. Coleman’s theory is supported by a mechanical model and demonstration of differential pressures in the two chambers during accommodation. By Coleman’s model, the development of more flexible IOLs may provide some degree of accommodation.
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Differential pressures in the anterior and posterior chambers are created during ciliary body contraction, creating a reproducible shape of the anterior lens surface important for accommodation
Mathematical modeling suggests that posterior pressure by the vitreous may be important in the process of accommodation, supporting Coleman’s theory. However, recent modeling with a two-dimensional axisymmetric model did not reveal an increase in refractive power with posterior lenticular pressure.
Etiology
Loss of accommodation most commonly occurs by three primary mechanisms: presbyopia as a normal process of aging, pseudophakia (lens extraction followed by implantation of an artificial lens without the ability to accommodate), and aphakia (lens extraction without replacement). Less commonly, premature loss of accommodation can occur secondary to paralysis, spasm, or atony of the ciliary muscle. For example, cycloplegia with a pharmacologic agent such as atropine will paralyze the ciliary muscle and inhibit accommodation. A cranial nerve 3 palsy also paralyzes accommodation via loss of neurologic innervation of the ciliary muscle ( Box 35.4 ).
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Normal aging process
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Pseudophakia
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Aphakia
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Changes in ciliary body functioning (spasm, paralysis, or atony)
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Cranial nerve 3 palsy
Pathophysiology
The lens
According to the Helmholtz theory of accommodation, the equatorial zonules maintain tension on the lens at rest, allowing for a relative flattening of the central curvature of the lens and an enlarged diameter. An effort to focus at near induces ciliary body contraction which paradoxically relaxes the zonules due to a centripetal movement of the muscle ( Figure 35.1 ). In turn, the zonules release tension on the equator of the lens, allowing the lens to round up at the anterior and posterior surfaces, increasing in thickness and therefore the converging power of the eye ( Box 35.5 ).
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The equatorial zonules relax during accommodation, leading to rounding of the central lens curvature, increasing the converging power of the eye
In the modern era, through ultrasound biomicroscopy and goniovideography, Glasser and Kaufman have been able to substantiate the Helmholtz theory and further characterize the accommodative process in monkeys. These investigators have documented that not only does the lens equator move away from the sclera radially during accommodation, but it also moves anteriorly due to a forward migration of the ciliary body during contraction. The contracting ciliary body, anchored to the scleral spur, trabecular meshwork, and peripheral cornea, acts as a sling to bring the lens forward during accommodation. Conversely, the elastic choroid and posterior zonules pull the lens posteriorly during relaxation of accommodation.
In addition to intraocular changes altering the lens, a number of other intraocular and extraocular changes are known to occur during accommodation to assist with viewing objects at changing distances. These factors are not considered true components of accommodation by its strict definition.
Pupil size
The pupil becomes smaller with accommodation effort by way of parasympathetic innervation of the iris sphincter from the Edinger–Westphal nucleus via the third cranial nerve. Such a process is known to enhance depth of focus that assists with near viewing. Recent work has demonstrated that the dynamic pupil near response does not change appreciably with age, and therefore likely does not contribute to or counteract presbyopia. Static pupil size tends to decrease with age.
Convergence
Changes in stimulation of the rectus muscles bilaterally allow for convergence of the eyes to focus on objects binocularly at varying distances. Stimuli for accommodation, both binocular and monocular, initiate convergence ( Box 35.6 ). Therefore, accommodation within the eye and ocular convergence occur in parallel.
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Pupil size decreases
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Convergence
Neural pathways in accommodation
Accommodation is initiated by voluntary effort to focus on near objects. Multiple stimuli for accommodation have been identified, but not all are well understood. It is likely that the most powerful stimulus for accommodation is retinal disparity between the two eyes as they focus on an object at varying distances. Monocular accommodation is driven by other cues for distance. For example, a change in angular size of an object has also been shown to induce accommodation even in the absence of actual distance change if all else is kept constant. Image blur also induces accommodation. Placing minus lenses in front of the eye, with angular size maintained constant, appears to induce accommodation by way of blur. This effect is diminished when blur cues are blunted, such as with decreased illumination or increased depth of focus with a pinhole. The mechanism by which the brain appears to recognize the appropriate direction of accommodation with blurring is unknown. Simply blurring an object without changing the refractive status of the eye or the object distance does not induce accommodation ( Box 35.7 ).
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Retinal disparity between the two eyes
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Change in angular size of an object
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Image blur
Neuronal pathways in the brain controlling accommodation are not fully understood but appear to involve primarily the Edinger–Westphal complex in the midbrain. The Edinger–Westphal complex receives inputs from the ventral and rostral midbrain, the likely location for receipt of accommodative cues such as retinal image disparity. From the Edinger–Westphal complex, the parasympathetics and third-nerve fascicles leave and synapse at the ciliary ganglion. Postsynaptic fibers continue to join the posterior ciliary nerves reaching the iris sphincter for control of pupil size as well as the ciliary body for control of accommodation ( Figure 35.2 ).
