We have documented the age-related functional changes of various components of the accommodative apparatus of the rhesus monkey. These results demonstrate that study of the entire age range is required to determine which component of the accommodative apparatus changes first with age.
Collectively, the data of the current study show that the loss in forward ciliary body movement with age occurs sooner than the loss in centripetal lens equator movement. The loss in forward muscle movement is partially compensated for by the level of increased centripetal muscle movement required to achieve zonular relaxation and lens rounding. Overall, the amplitude of the centripetal ciliary body movement is somewhat reduced with age. It is unlikely that the lenses of the middle-aged monkeys changed substantially in internal refractive properties or hardness compared to those of the young animals since the centripetal lens movement per diopter of accommodation was the same in both the young and middle-aged animals.
The higher amplitudes of centripetal lens movement were not achieved in the middle-aged eyes, possibly due to the 55% loss in forward ciliary body movement. Even during supramaximal stimulation, despite the compensating centripetal CP movement, no further lens movement was induced in the middle-aged eyes. There are hundreds of zonular fibers extending from the valleys of the ciliary processes to the anterior and posterior lens surfaces, in addition to those that extend between the ciliary processes and the lens equator (Glasser and Campbell, 1998
; Rohen, 1979
). Some of these zonular attachments may be more dependent on forward ciliary body movement than centripetal CP movement to achieve relaxation and allow lens rounding.
Without the supramaximal stimulation data included, multiple regression analysis showed that most of the variability in accommodative amplitude was explained by centripetal CP movement in all three age groups, while the centripetal lens movement was also important to explain some part of accommodative amplitude (based on the stepwise regression analysis; ). This was not surprising, since it is known that both parameters are needed for accommodation. Centripetal CP movement may reflect both the centripetal lens equatorial movement and the thickening of the lens, which may be why centripetal CP movement was so important in the stepwise regression models to predict accommodation.
Goniovideographically measured centripetal CP movements predominantly represent centripetal ciliary body movements, but these measurements do not really distinguish centripetal from forward ciliary body movement. Thus, centripetal CP movements that we report here may actually be a hybrid or composite, in contrast to movements measured by UBM that can isolate measurement of forward ciliary body movement. Nonetheless, the techniques of measuring forward ciliary body movement by UBM and centripetal CP movement by goniovideography clearly provide separate and distinct information about ciliary body function and its change with age (Croft et al., 2006a
Presbyopia is by definition the loss in accommodative amplitude, due to the loss in the ability of the lens to change shape. Given the CP versus lens relationships in , one might argue that the CP movement has not dampened with age but the lens movement has. However, the same amount of lens movement per diopter of accommodation exists in both the young and middle-aged eyes ().
Given the difference between young and middle-aged eyes in CP and forward ciliary body movement, one might consider the possibility of a Type I error (the possibility of a false assumption of a significant difference between the groups, with no biological basis). The probability of such an error is low (typically p=0.05 or a 5% chance) and, based on an overall examination of the data, we considered the existence of a Type I error an unlikely possibility.
The active movement of the ciliary body is possible only by ciliary muscle contraction. Due to the posterior restriction of muscle movement in the aging eye, the longitudinal portion of the muscle may undergo more of an isometric contraction than the circular portion—thus the marked loss in forward movement. However, the circular portion of the muscle during contraction applies its force centripetally, a direction that is perpendicular to the restriction and that is not in direct opposition to the restriction. In support of this idea, Tamm et al. (1992) reported that the area encompassing the circular portion of the ciliary muscle increases with age in excised human eyes, while the area of the longitudinal portion of the ciliary muscle decreases with age. This aging change may be adaptive to compensate for the muscle's posterior restriction or to further support the accommodative effort as the lens thickens with age. The aging change mentioned above would likely not be to compensate for the decreased deformability of the lens (at least in the middle-aged monkey eyes), since, by extrapolation from human data, changes in lens deformability do not occur until after age 19 in monkeys (~age 40 in humans; see second to last paragraph of the discussion, below).
By examination of dynamic UBM images of a 16-year-old rhesus monkey eye during supramaximal stimulation to induce accommodation, one can understand how there could be an age-related loss in forward ciliary body movement while substantial centripetal CP movement remained, based on ocular geometry (Video Clip #1
). Age-related stiffening of the posterior attachments (i.e., choroid, posterior muscle tendons (Tamm et al., 1992), and/or posterior vitreous zonule, which extend in a straight line from the ora serrata to the zonular plexus in the valleys of the ciliary processes (Lütjen-Drecoll et al., Unpublished results)) could dampen forward ciliary body movement, with substantial centripetal CP movement remaining.
With the lens substance removed (leaving an empty capsular bag), the centripetal muscle movement was enhanced but forward muscle movement was unchanged compared to the normal iridectomized eye. With the lens substance and capsule removed (thus severing the anterior zonular attachments between the ciliary muscle and the lens capsule), the loss of forward muscle movement was far more pronounced (50%) than the loss in centripetal muscle movement (10-15%) (Croft et al., 2008
) (Wasilewski et al., 2008
). This suggests that there may be agonistic tractional forces, supplied by the attachment of the anterior zonula/lens complex to the ciliary muscle during accommodation, that enhance muscle movement and are far more important to forward movement than to centripetal movement of the muscle. These forces provide anterior traction to the muscle and counterbalance those forces that pull the muscle back into the resting state (i.e., posterior elastic tendons, choroid). Alternatively, the anterior attachments of the muscle to the anterior zonula/lens complex may simply be an anchor by which the muscle pulls itself forward and thereby contribute passively to forward muscle movement. Whether the attachment of the anterior zonula/lens complex to the ciliary muscle provides traction or plays a “passive anchor” role in ciliary muscle contraction, it facilitates forward muscle movement until zonular relaxation is achieved during the accommodative response.
Formation of chemical bonds between lens fibers might also cause dampened lens equator movement, but it was beyond the scope of this study to determine bonding between the lens fiber cells in the young and middle-aged rhesus eyes. In excised human eyes, age-related changes in lens compliance (Weeber et al., 2005
) and lens resistance to deformation (Glasser and Campbell, 1999
) were minimal prior to age 40 (age in monkey years ~19). The lens resistance to deformation increased dramatically after the age of 40 in excised human lenses (Glasser and Campbell, 1999
). Age-related lens thickening by itself could be considered a significant change and could play a role in the pathophysiology of presbyopia. However, Alió et al. (2005)
reported that, while human lens thickness begins increasing before the age of 40, the density of the human lens nucleus only begins increasing after age 40, and does so linearly with age. Alió also reported an increase in intraocular light scattering and aberrations after age 40, which decreases the optical image quality (Alió et al., 2005
). This suggests that significant cumulative lens changes are not apparent until after the age of 40 in humans, by which time, as mentioned previously, more than 2/3 of the accommodative ability has been lost (Duane, 1922
This study demonstrates that ciliary body function begins to change with age before lens function changes. Our data show that the lens accommodative response (i.e., centripetal lens movement required to induce a given level of accommodation) was not significantly changed in the middle-aged monkeys (12-16.5 years) compared to the young monkeys; thus, it is unlikely that the resting lenses of the middle-aged monkeys changed in refractive power compared to the young animals. The age-related loss in ciliary body function (i.e., loss of forward ciliary body movement) that we measured could be due to decreasing elasticity of the choroid, the posterior ciliary muscle tendons, or the posterior vitreous zonule. Chemical or physical lysis or other treatment of these inelastic attachments may sustain the ability of the ciliary body to move forward during accommodative effort and thus prevent or delay secondary age-related lenticular changes and perhaps facilitate the mobility/deformability of accommodating IOLs.