Lens Accommodative Movements of the Vitreous Membrane, Choroid, and Sclera in Young and Presbyopic Human and Nonhuman Primate Eyes Mary Ann Croft,1 T. Michael Nork,1 Jared P. McDonald,1 Alexander Katz,1 Elke Lutjen-Drecoll,¨ 2 and Paul L. Kaufman1,3 1Department of Ophthalmology and Visual Sciences, University of Wisconsin–Madison, Madison, Wisconsin 2Institute of Anatomy II, University of Erlangen–Nuremberg, Erlangen, Germany 3Wisconsin National Primate Research Center, University of Wisconsin–Madison, Madison, Wisconsin Correspondence: Mary Ann Croft, PURPOSE. We report, for the first time to our knowledge, dynamic movements of the vitreous Department of Ophthalmology and membrane and peripheral choroid during accommodation, and age-related changes in the Visual Sciences, University of Wis- anterior sclera. consin Clinical Sciences Center, 600 Highland Avenue, Madison, WI METHODS. We studied 11 rhesus monkeys (ages 6–27 years) and 12 human subjects (ages 19– 53792-3220; 65 years). Accommodation was induced pharmacologically in human subjects and by central [email protected]. electrical stimulation in the monkeys. Ultrasound biomicroscopy, endoscopy, and contrast Submitted: August 25, 2012 agents were used to image various intraocular structures. Accepted: May 25, 2013 RESULTS. In the monkey, the anterior hyaloid membrane bows backward during accommo- Citation: Croft MA, Nork TM, McDon- dation in proportion to accommodative amplitude and lens thickening. A cleft exists between ald JP, Katz A, Lutjen-Drecoll¨ E, Kauf- the pars plicata region and the anterior hyaloid membrane, and the cleft width increases man PL. Accommodative movements during accommodation from 0.79 6 0.01 mm to 1.01 6 0.02 mm in young eyes (n ¼ 2, P < of the vitreous membrane, choroid, 0.005), as fluid from the anterior chamber flows around the lens equator toward the cleft. In and sclera in young and presbyopic the older eyes the cleft width was 0.30 6 0.19 mm, which during accommodation increased human and nonhuman primate eyes. to 0.45 6 0.20 mm (n ¼ 2). During accommodation the ciliary muscle moved forward by Invest Ophthalmol Vis Sci. 2013;54:5049–5058. DOI:10.1167/ approximately 1.0 mm, pulling forward the choroid, retina, vitreous zonule, and the iovs.12-10847 neighboring vitreous interconnected with the vitreous zonule. Among the humans, in the older eyes the scleral contour bowed inward in the region of the limbus, compared to the young eyes. CONCLUSIONS. The monkey anterior hyaloid bends posteriorly during accommodation in proportion to accommodative amplitude and the sclera bows inward with increasing age in both species. Future descriptions of the accommodative mechanism, and approaches to presbyopia therapy, may need to incorporate these findings. Keywords: accommodation, presbyopia, vitreous membrane, lens, choroid he exact manner in which the accommodative forces on Reports exist that argue for and against a role for the Tthe lens change during accommodation is unclear. The vitreous in accommodation and presbyopia.4,7,8 Some studies mechanism of accommodation in the human eye includes the indicate that accommodative amplitude is not diminished in antero-inward movement of the ciliary muscle during contrac- human patients following vitrectomy.7 Another study report- tion. This allows the relaxation of the anterior zonule that ed a loss of approximately 2 diopters of accommodation in suspends the lens, and thereby allows the lens to become human patients (ages 33–41 years) following pars plana 9 thicker and more spherical in shape as the lens substance is vitrectomy. In both instances, the vitrectomy procedure molded by the capsule. avoids the anterior hyaloid membrane (vitreous face) and the periphery of the vitreous. The hydraulic theory posits that, The vitreous, which is in close juxtaposition to the during accommodative contraction, the ciliary muscle exerts accommodative apparatus, also has been posited to be pressure upon the aqueous in the posterior chamber, where it important to the accommodative change of the lens shape, is confined by the iris as the pupil constricts onto the lens either by pushing against the lens (according to Cramer in surface, compressing the lens equator and causing the 1 1851 ) or by forces of vitreous pressure that change the lens anterior lens surface to bulge.10–12 Fincham discounted this 2 shape (suggested by Tscherning in 1904 ), as cited by theory, due to the fact that accommodation is unimpaired by Fincham.3 Coleman and Fish speculated that the lens, zonule, iridectomy or aniridia.3 However, Crawford et al. reported a and anterior vitreous comprise a diaphragm between the 40% loss in accommodative amplitude after iridectomy in the anterior and vitreous chambers, and that a pressure gradient monkey eye.13 To our knowledge, the accommodative between the two chambers is initiated by muscle contraction, movements of the vitreous/anterior hyaloid and peripheral which, in turn, aids accommodative lens shape change.4–6 choroid have never been observed in vivo in the human or Copyright 2013 The Association for Research in Vision and Ophthalmology, Inc. www.iovs.org j ISSN: 1552-5783 5049 Downloaded from jov.arvojournals.org on 10/03/2021 Vitreous Membrane, Choroid, and Sclera IOVS j July 2013 j Vol. 54 j No. 7 j 5050 FIGURE 1. (A) Typical UBM image in an 8-year-old rhesus monkey before injection of triamcinolone (Triesence). The vitreous zonule was clearly visible, but the anterior hyaloid/vitreous membrane was not visualized. (B) UBM image 24 hours after injection of Triesence in the same monkey eye and quadrant as in (A). The location of the vitreous membrane and anterior hyaloid portion of the vitreous membrane are now clearly visible as the Triesence clings to the vitreous membranes. There is a cleft between the ciliary processes (pars plicata region) and the anterior hyaloid membrane; termed the AH cleft. CP, ciliary processes; CM, ciliary muscle. monkey eye, not even in our recent ultrasound biomicro- This research adhered to the tenets of the Declaration of scopic (UBM) and scanning electron microscopic study, Helsinki (human subjects) and to the ARVO Statement for the demonstrating the existence of the vitreous zonule.14 Use of Animals in Ophthalmic and Vision Research, and to To visualize and record the dynamics of the accommoda- institutionally approved animal protocols (rhesus monkeys). tive mechanism, high-resolution imaging (i.e., UBM) is necessaryandcanbeperformedinanesthetizedmon- Ultrasound Biomicroscopy keys.15–19 Magnetic resonance imaging (MRI)20 cannot capture dynamic movements of the various intraocular Triamcinolone acetonide (50 lL of 40 mg/mL, Triesence; structures during accommodation, and cannot image the Bristol-Meyers Squibb Company, Princeton, NJ), which adheres vitreous zonule or the vitreous anterior hyaloid membrane, to the vitreous membranes/fibers,22 was administered via pars due to resolution limitations. The static images at rest, and plana injection to enhance visualization (by either UBM or after pharmacologic stimulation to induce accommodation, endoscopy) of the intravitreal structures (i.e., anterior hyaloid) do supply some valuable information; however, they do not in 4 rhesus monkey eyes. supply the visualization of the structures’ dynamic move- For the monkeys and human subjects, analogous images mentsandtheanalysesinrealtimethatareavailablebydoing were collected, with the anterior/posterior ends of the ciliary the in vivo monkey experiments. body and vitreous zonule oriented in a horizontal direction Our study sought to develop a technique, using contrast within all images. agents, to visualize the vitreous (anterior hyaloid) membrane, and determine its accommodative movement in young and old Endoscopy in the Monkey Eye During human and monkey eyes. We also report, for the first time to Accommodation our knowledge, visualization of the dynamic movements of the peripheral choroid during accommodation/disaccommodation An endoscopic camera system (Model E2 endoscopic camera; in the living monkey eye, along with changes in the anterior EndoOptiks, Little Silver, NJ) with a fiberoptic light and a sclera at the level of the scleral spur. curved imaging probe to allow passage behind the lens, (the camera and the light source were contained within the 20- guage probe), was inserted via the pars plana in 3 rhesus MATERIALS AND METHODS monkey eyes to image the intraocular structures during centrally stimulated accommodation. The images were record- Measurements of accommodation, ultrasound biomicroscopy ed to tape. Two entry points were required: one for the techniques, stimulation of accommodation, and so forth, for endoscopic probe and one for a sutureless 25-gauge infusion the monkey and the human have been described in our cannula (to maintain IOP). One to two weeks before companion study.21 Images from the same experimental endoscopy, a 50 lL bolus of an aminofluorescein dye (0.02% sessions as described therein21 were used for this study. We 5-[4,6-dichlorotriazin-2-yl]-aminofluorescein [DTAF] hydrochlo- recruited 12 human subjects ranging in age from 19 to 65 ride; Sigma-Aldrich, St. Louis, MO), which binds to collagen, years with normal eyes, and 11 rhesus monkeys (Macaca and fluoresces with excitation and emission spectra similar to mulatta) ranging in age from 6 to 27 years with normal eyes sodium fluorescein,23 was injected via the pars plana into the were studied, as described in detail in the companion vitreous cavity to enhance visualization of the vitreous fibers/ study.21 anterior hyaloid membrane. Downloaded from jov.arvojournals.org on 10/03/2021 Vitreous Membrane, Choroid, and Sclera IOVS j July 2013 j Vol. 54 j No. 7 j 5051 FIGURE 2. Left and Middle: UBM images in the temporal quadrant in 8-, 17-, and 25-year-old rhesus monkeys in the unaccommodated and maximally accommodated states following injection of Triesence (triamcinolone acetonide), which clings to the vitreous membrane. Middle: The anterior hyaloid relaxes/curves posteriorly during accommodation (see also Supplementary Video Clips S1, S3). The AH cleft, which lies between the ciliary processes and the anterior hyaloid, is reduced in the older eyes (ages 17 and 25) versus the young eye (age 8).