INTRODUCTION

The term "accommodation" means the ability of the eye to alter its dioptric power so as to focus on objects at different distances. There are several explanatory theories of the accommodation phenomenon, and Helmholtz's theory (1855) clearly receives greater consensus among the scientific community.

To obtain a correct visual acuity, the convergence of the parallel light rays that cross the ocular globe in a focal point, located at the level of the retina and coincident with the macula lutea, is necessary from the point of view of the optical system. This convergence requires the existence and correct functioning of structures responsible for the refraction of light rays, which include the cornea, crystalline lens, vitreous humor and aqueous humor^1,2 (Figure 1) (Total refractive power).

HISTORICAL CONTEXTUALIZATION

The first demonstration of an accommodative mechanism dates back to 1619 when Scheiner experimented with drilling two holes in a piece of card and therethrough observing an object placed at different distances, concluding that only at a certain distance the objects seen in that way did not appear in duplicate^3,4. The first explanation for this event arose only in the following century, in 1759, when William Porterfield suggested that the mechanism by which objects could be focused was caused by changes at the crystalline level, not found in cases of aphakia (absence of the lens)^3,5. Shortly thereafter, in 1763, Albrecht von Haller supplemented Porterfield's explanation by considering that pupil contraction would also play an important role in the physiological mechanism of accommodation⁴. Thomas Young went even further and in 1801 proposed that changes in the lens involved the degree of curvature of the lens, rejecting the idea that the accommodation was due to changes in the axial length of the eye and the curvature of the cornea, as previously speculated that it could be^5,6.

It was Helmholtz (1821-1894) who made the most important contribution in this area, noting in 1855 that the crystalline thickness increased during accommodation and that this change was due to the contraction of a muscle, the ciliary muscle described by Crampton and Müller, which allowed the reduction of tension on the lens itself^4,6. This fact made possible the increase of the thickness and decrease of the equatorial diameter of the lens simultaneously, which contributed to the increase of its refractive power.

In the twentieth century, Fincham demonstrated that the peculiar shape of the lens was due to the structure of its capsule, constituted by an anterior segment thicker than the posterior segment and being thicker in its peripheral region than in the poles. According to Fincham, these differences in the lens capsule would be the origin of the hyperbolic form of the lens during the accommodation process^4,6. It was in the light of this knowledge that the theoretical foundations for the physiology of accommodation were successively perfected, and the theory is now accepted based on the original assumptions of Helmholtz. The accommodation mechanism in its entirety is described below.

PHYSIOLOGY OF ACCOMMODATION

Reflex of accommodation

The process of focusing a close object implies the existence of three different mechanisms: eye convergence, accommodation of refractive structures and contraction of the pupils, globally designated as accommodative triad and controlled by the action of the autonomous nervous system^1,7.

It all begins when an object is presented at a short distance from the individual and the light rays from it reach the retina, being captured by the photoreceptors (cones and rods) that constitute the 1^st neuron of the optical pathway. The transduction that takes place at the level of the photoreceptors gives rise to nerve impulses that go to the bipolar cells (2^nd neuron) and these to the ganglion cells of the retina (3^rd neuron), whose axons form the optic nerve. From the ganglion cells of the retina, two types of fibers originate:

1. Cortical fibers, corresponding to about 90% of the total, that transmit the impulse to the external or lateral geniculate body of the thalamus, where the synapse is made with the 4^th neuron, which finally reaches the primary visual cortex (V1) and later the secondary visual areas (V2, V3, V4 and others) after synapse with interneurons⁷.
2. Non-cortical fibers, corresponding to the remaining 10%, that go to the pre-tectal area (which also receives afferences from the secondary visual cortex), located posterior to the superior collicles, where after a new synapse formation the neurons reach the nucleus of Perlia, located between the two Eddinger-Wesphal nuclei, from which two types of functionally different neurons originate:

a. Neurons that make synapses with the somatic motor nucleus of the third cranial nerve (common ocular motor nerve - MOC), from which in turn axons depart to the internal rectus muscles, allowing the convergence movement^1,7.

B. Neurons that make synapses with the accessory and visceral nuclei of the MOC, as is the case of the Eddinger-Westphal nucleus, from which also parasympathetic preganglionic axons depart to the ciliary ganglion. Here two types of different neurons arise^1,7:

i. Neurons for the ciliary muscle, allowing crystalline accommodation.

ii. Neurons for the constrictor muscle of the pupil, inducing miosis (Figure 2).

Ocular mechanism of accommodation

Following the accommodation reflex, the parasympathetic postganglionic neurons departing for the ciliary muscle are excited, with acetylcholine release leading to contraction of the ciliary muscle. The contraction of this muscle causes a displacement of the medial apex of the ciliary body towards the axis of the ocular globe, leading to a relaxation of the suspensory fibers of the lens. This fact contributes to a change in the forces exerted on the lens capsule, allowing it to assume its accommodated shape, characterized by a decrease in the diameter and increase in the thickness thereof, as well as by an increase in the curvature of the anterior and, to a lesser extent, posterior capsules^1,2,4,6,8,9. It is then through these structural changes that the crystalline manages to increase its dioptric power, which is indispensable to enable near vision. In parallel, there is a decrease in the depth of the anterior and posterior chambers due to increased crystalline thickness, which occurs in 75% of its extent due to the anterior movement of the anterior portion of the capsule and in 25% to the posterior movement of the posterior portion of the capsule¹⁰ (Figure 3).

When the accommodative stimulus ceases, the ciliary muscle relaxes, which causes a centrifugal movement of the apex of the ciliary body. This movement increases the tension on the suspensory ligaments, which in turn increases the tension on the lens capsule and causes it to return to its unaccommodated form⁸.

The process described above leads not only to an increase in the dioptric power of the lens, but also to an exacerbation of the spherical aberrations of the lens^8,11. This term designates the set of situations in which the paraxial rays are focused at a more anterior point compared to the rays that affect the more peripheral regions of the lens. This effect is altered by the contraction of the pupil constrictor muscle (due to the action of the parasympathetic postganglionic neurons), which by reducing the pupillary orifice diameter allows only the paraxial rays to penetrate the eye. By focusing these on a lens region with a higher refractive index, the miosis that occurs simultaneously increases the amplitude of the accommodation⁸.

Alternative Theories of Accommodation

The mechanism described for the physiology of accommodation is fundamentally based on the original assumptions of Helmholtz elaborated in the nineteenth century. However, it should be noted that in the twentieth century two theories emerged that challenged the foundations of the German physicist, the theories of Tscherning (1909) and Schachar (1993), both arguing for an increase in tension in the suspensory ligaments of the crystalline lens rather than a decrease of it^4,6,9.

According to Tscherning, contraction of the ciliary muscle would lead to an increase in tension on the suspensory ligaments of the lens, this being its accommodated shape characterized by a flattening of the peripheral regions and increased curvature at its center. Moreover, this theory differed from that of Helmholtz because it considered that there would be an increase and not a decrease in the equatorial diameter of the lens^4,6,9. This theory was later abandoned by the scientific evidence that a decrease in said diameter actually occurred during the smaller, posterior degree of its capsule, and then through accommodation. As an example, Glasser, Ostrin and Wendt¹² concluded that there was a decrease of 7.04% in the measurement of lens diameter during accommodation, based on studies performed on the Rhesus monkey, and that this decrease was greater as the amplitude of the stimulus used to induce accommodation increased.

On the other hand, according to Schachar et al the contraction of the ciliary muscle would generate increased tension on the posterior portion of the equatorial lens capsule (Figure 3) while at the same time relaxing the anterior and posterior suspensory fibers of the lens. In this way, during the process of accommodation there would be a traction of the equatorial region of the lens towards the sclera, which, together with the relaxation of the anterior and posterior suspension fibers, would simultaneously flatten the peripheral region of the lens and increase the curvature in its central region^4,6,9. However, this theory was equally rejected by Glasser and Kaufman, who through in vivo studies showed that during accommodation the lens equator moves away from the sclera rather than approaching it¹³ (Figure 4).

In this way, Helmholtz's original theory is maintained, complemented by the findings of Fincham and other authors as an accepted theoretical foundation for the mechanism of accommodation.

PHYSIOLOGICAL CHANGES IN ACCOMMODATION

Presbicia

Accommodation capacity changes throughout life. The gradual and physiological loss of the capacity of accommodation with age is called presbyopia, beginning at an early stage of life, decreasing by about 2.5 D per decade, and culminating in the complete loss of accommodation capacity at 50-55 years⁸. It is believed that the genesis of presbyopia is multifactorial, involving changes in the lens and its capsule, as well as changes in the ciliary muscle and the tension of the suspensory ligaments of the lens^4,8,9,14.

Age-attributable accommodation disorders

The loss of long-term accommodation capacity is based on the occurrence of age-related changes in various ocular structures. Some of the modifications verified in each part of the system that allow the accommodation are described. The thickness of the anterior portion of the lens capsule at birth is approximately 11 micrometers, increasing to about 33 micrometers in the individual at about 75 years, and decreasing slightly after that age, according to Krag, Olsen and Andreasson¹⁵ (Figure 5A). In addition, the same authors demonstrated that the anterior portion of the capsule became progressively less elastic, having the ability to increase its length up to 108% in the young individual when stretched, and that this value decreased to about 40% at 98 years (Figure 5B). Another important conclusion reached by this study was that the force needed to break the anterior segment of the capsule remained constant up to 35 years, decreasing linearly from that age.

Crystalline dimensions

The crystalline lens continuously grows throughout life, increasing its axial thickness as a result of the addition of new fibers, while maintaining its equatorial diameter. In addition, it is found that the curvature of the anterior and posterior segments of the lens capsule also undergoes an increase, which, when analyzed in conjunction with the increase in axial thickness and maintenance of the equatorial diameter, remembers the shape acquired by the lens after the process of accommodation^9,14,16,17. The only difference lies in the fact that the increase in the axial thickness of the lens results from an increase in the thickness of the anterior and posterior cortex of the lens in the presbyopic individual, whereas in the non-presbyopic individual this increase is achieved by an increase in the thickness of the nucleus of the crystalline lens⁸. It should be noted, however, that although the crystalline lens appears to assume its accommodated shape, presbyopia is characterized by a loss of near vision, introducing the concept of “lens paradox”^14,16,17. The reason for this is related to the fact that there is a progressive loss of the crystalline refractive index due to the formation of insoluble protein aggregates and an increase in their content in water¹⁶. Finally, it should be noted that the set of structural changes in the lens contribute to the fact that the spherical negative aberrations present in the young individual become positive in presbyopia, thus failing to compensate for the ever-present spherical aberrations of the cornea^9,17,18 (Figure 6). In this type of aberration, the more peripheral rays are focused at a point closer to the lens relative to the paraxial rays. Thus, the occurrence of miosis during accommodation in the presbyope leads to only the paraxial rays penetrating the eye, being refracted in the region of lower dioptric power of the lens. It is concluded that this situation contrasts with the accommodation occurring in the young, in which the miosis observed in an eye with negative spherical aberrations causes the rays to focus on the region of greater refractive power of the lens. In summary, the same event (miosis) is advantageous in the young and harmful in the presbyopic¹⁸.

Crystalline stiffness

The stiffness of the lens increases exponentially throughout life^19,20. In the crystalline of the young individual, the nucleus presents less rigidity than the cortex, and the accommodation process is carried out thanks to an increase in the rigidity of the nuclear region. As age progresses, there is an increase in the stiffness of both the nucleus and the cortex of the lens, which is more marked in the former in such a way that the stiffness of the nucleus exceeds that of the cortex at around 35 years¹⁹ (Figure 7).

It is believed that this fact is decisive in the process of loss of accommodative capacity by interfering with the perfect balance between the nucleus, capsule of the lens and tension of the suspensory ligaments that allows the set of mechanisms necessary for accommodation. Regarding the rigidity of the lens, Glasser, Kroft and Kaufman²⁰ performed an experiment in which they isolated the lens of three individuals of different age groups (5, 23 and 84 years) and measured their equatorial and anteroposterior diameters before and after removal of the capsule. They found that in the young individual the presence of the capsule allows the crystalline to assume its accommodated form, changing to the non-accommodated shape when the capsule is removed. The same was not observed in the elderly, in which they concluded that the two diameters were independent of the presence of the capsule, thus suggesting that the lens of the presbyopic individual ceases to be able to respond to the capsule during the accommodation process (Figure 8).

Suspensory Ligaments of the Crystalline lens

In a presbyopic individual there is an increase in the thickness of the lens and the curvature of its capsule, which means that the capsular insertion of the anterior fibers undergoes an anterior displacement with aging. In parallel, it is verified that the distance between the capsular insertion of the ligaments and the ciliary body remains constant, which allows us to conclude that there is a decrease of the angle of insertion of the most anterior fibers. This causes the force generated by the contraction of the ciliary muscle to act almost tangentially on the capsule, thus making it more difficult to induce the morphological changes of the crystalline lens needed for the accommodation process^9,14,17. Another possible explanation for the development of presbyopia rests on the existence of a decrease in the space around the crystalline (circumlental space), since the equatorial diameter of the crystalline remains constant, while simultaneously there is a centripetal displacement of the apex of the ciliary body with aging. The reduction of this space causes a reduction in the tension of the suspending ligaments on the lens capsule, which implies a smaller capacity of alteration of its refractive power since the angle of insertion of the fibers does not allow, in this case, to reduce the tension on the lens capsule^9,17.

Explanatory theories of presbyopia

Based on the modifications that have occurred in each component of the accommodation system, several theories have emerged to explain the development of presbyopia, which can be divided into lenticular theories involving changes in stiffness, lens dimensions and capsule, extra-lenticular theories, which are based on modifications in the ciliary muscle and choroid, as well as geometric theories, which advocate changes in the capsular insertion of the suspensory ligaments^4,9,14,17.

As for lenticular theories, two different explanatory mechanisms stand out: the Hess-Gullstrand theory and the Duane-Fincham theory^9,23. According to the first, the measure of contraction of the ciliary muscle required to produce a change in one unit in the dioptric power of the eye remains constant throughout life, which means that the accommodative convergence / accommodation (AC / A) ratio does not change with age⁹. In contrast, the Duane-Fincham theory argues that the measure of contraction of the ciliary muscle increases with age in order to produce the same refractive power, which implies an increase in AC / A ratio with aging²³. From the certainty that there is a decrease in the amplitude of accommodation with age, it seems reasonable to consider that there is an increase in the contraction force of the ciliary muscle to produce a similar change in the dioptric power of the eye, which favors the Duane-Fincham theory. However, it seems equally plausible that the ciliary muscle may have some contractile reserve in situations where accommodation capacity is minimal, which supports Hess-Gullstrand's theory⁹. Multiple studies will therefore be necessary to ascertain which of the two theories best explains the lens changes involved in the genesis of presbyopia.