Accommodative movements of the vitreous membrane, choroid, and sclera in young and presbyopic human and nonhuman primate eyes.

PURPOSE We report, for the first time to our knowledge, dynamic movements of the vitreous membrane and peripheral choroid during accommodation, and age-related changes in the anterior sclera. METHODS We studied 11 rhesus monkeys (ages 6-27 years) and 12 human subjects (ages 19-65 years). Accommodation was induced pharmacologically in human subjects and by central electrical stimulation in the monkeys. Ultrasound biomicroscopy, endoscopy, and contrast agents were used to image various intraocular structures. RESULTS In the monkey, the anterior hyaloid membrane bows backward during accommodation in proportion to accommodative amplitude and lens thickening. A cleft exists between the pars plicata region and the anterior hyaloid membrane, and the cleft width increases during accommodation from 0.79 ± 0.01 mm to 1.01 ± 0.02 mm in young eyes (n = 2, P < 0.005), as fluid from the anterior chamber flows around the lens equator toward the cleft. In the older eyes the cleft width was 0.30 ± 0.19 mm, which during accommodation increased to 0.45 ± 0.20 mm (n = 2). During accommodation the ciliary muscle moved forward by approximately 1.0 mm, pulling forward the choroid, retina, vitreous zonule, and the 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.

[1]  S. Wu,et al.  Adler's Physiology of the Eye , 2002 .

[2]  W. Peddie,et al.  Helmholtz's Treatise on Physiological Optics , 1924, Nature.

[3]  E. Tamm,et al.  Nitrergic nerve cells in the primate ciliary muscle are only present in species with a fovea centralis. , 1997, Ophthalmologica. Journal international d'ophtalmologie. International journal of ophthalmology. Zeitschrift fur Augenheilkunde.

[4]  Coleman Dj,et al.  On the hydraulic suspension theory of accommodation. , 1986 .

[5]  E. Tamm,et al.  Ciliary body , 2020, Microscopy research and technique.

[6]  F. Roy,et al.  Mechanism of accommodation in primates. , 2001, Ophthalmology.

[7]  M. Hollins,et al.  Does the central human retina stretch during accommodation? , 1974, Nature.

[8]  R. Schachar,et al.  Mechanism of Accommodation , 2001, International ophthalmology clinics.

[9]  J. Koretz,et al.  Slit-lamp studies of the rhesus monkey eye. I. Survey of the anterior segment. , 1987, Experimental eye research.

[10]  H. Helmholtz Handbuch der physiologischen Optik , 2015 .

[11]  G. Peyman,et al.  TRIAMCINOLONE ACETONIDE AS AN AID TO VISUALIZATION OF THE VITREOUS AND THE POSTERIOR HYALOID DURING PARS PLANA VITRECTOMY , 2000, Retina.

[12]  P. Kaufman,et al.  Accommodative ciliary body and lens function in rhesus monkeys, I: normal lens, zonule and ciliary process configuration in the iridectomized eye. , 2006, Investigative ophthalmology & visual science.

[13]  N. Brown,et al.  The change in shape and internal form of the lens of the eye on accommodation. , 1973, Experimental eye research.

[14]  P. Farnsworth,et al.  Three-dimensional architecture of the suspensory apparatus of the lens of the Rhesus monkey. , 1977, Experimental eye research.

[15]  D J Coleman,et al.  Presbyopia, accommodation, and the mature catenary. , 2001, Ophthalmology.

[16]  H. Burian,et al.  Mechanical changes during accommodation observed by gonioscopy. , 1955, A.M.A. archives of ophthalmology.

[17]  P. Kaufman,et al.  The role of the iris in accommodation of rhesus monkeys. , 1990, Investigative ophthalmology & visual science.

[18]  P. Kaufman,et al.  In vivo videography of the rhesus monkey accommodative apparatus. Age-related loss of ciliary muscle response to central stimulation. , 1990, Archives of ophthalmology.

[19]  J. Goldsmith DYNAMICS OF INTRACAPSULAR CATARACT EXTRACTION: EXPERIMENTAL STUDIES WITH REFERENCE TO THE SUSPENSORY LIGAMENT, HANNOVER'S CANAL AND PETIT'S SPACE , 1943 .

[20]  P. Kaufman,et al.  Surgical intervention and accommodative responses, II: forward ciliary body accommodative movement is facilitated by zonular attachments to the lens capsule. , 2008, Investigative ophthalmology & visual science.

[21]  J. Koretz,et al.  Accommodation and presbyopia in the human eye. 1: Evaluation of in vivo measurement techniques. , 1989, Applied optics.

[22]  Marius Hans Erik Tscherning,et al.  Physiologic Optics: Dioptrics of the Eye, Functions of the Retina, Ocular Movements and Binocular Vision , 2010 .

[23]  W. Crisp The Nature of the Vitreous Body , 1931 .

[24]  P. Kaufman,et al.  Age-related loss of morphologic responses to pilocarpine in rhesus monkey ciliary muscle. , 1988, Archives of ophthalmology.

[25]  S. Strenk,et al.  Magnetic resonance imaging of aging, accommodating, phakic, and pseudophakic ciliary muscle diameters , 2006, Journal of cataract and refractive surgery.

[26]  CONCEPT OF A ZONULAR CHAMBER: PRELIMINARY REPORT , 1942 .

[27]  P. Kaufman,et al.  Extralenticular and lenticular aspects of accommodation and presbyopia in human versus monkey eyes. , 2013, Investigative ophthalmology & visual science.

[28]  J F Koretz,et al.  Slit-lamp studies of the rhesus monkey eye: II. Changes in crystalline lens shape, thickness and position during accommodation and aging. , 1987, Experimental eye research.

[29]  James P. C. Southall,et al.  Mechanism of accommodation. , 1924 .

[30]  E. Lütjen-Drecoll,et al.  Histochemical differences within the ciliary muscle and its function in accommodation. , 1990, Experimental eye research.

[31]  M. Croft,et al.  Ultrasound Biomicroscopy of the Aging Rhesus Monkey Ciliary Region , 2001, Optometry and vision science : official publication of the American Academy of Optometry.

[32]  H. Helmholtz Helmholtz's Treatise on Physiological Optics , 1963 .

[33]  P. Kaufman,et al.  The mechanism of accommodation in primates. , 1999, Ophthalmology.

[34]  C. McCulloch The zonule of Zinn: its origin, course, and insertion, and its relation to neighboring structures. , 1954, Transactions of the American Ophthalmological Society.

[35]  Robert J. Lee,et al.  THE MECHANISM OF ACCOMMODATION. , 1895 .

[36]  P. Kaufman,et al.  Age-dependent loss of accommodative amplitude in rhesus monkeys: an animal model for presbyopia. , 1982, Investigative ophthalmology & visual science.

[37]  P. Kaufman,et al.  Age changes in rhesus monkey ciliary muscle: light and electron microscopy. , 1988, Experimental eye research.

[38]  D. Rentsch,et al.  Staining particulate organic matter with DTAF-a fluorescence dye for carbohydrates and protein:a new approach and application of a 2D image analysis system , 1998 .

[39]  Adrian Glasser,et al.  The zonula, lens, and circumlental space in the normal iridectomized rhesus monkey eye. , 2006, Investigative ophthalmology & visual science.

[40]  P. Kaufman,et al.  Morphology and accommodative function of the vitreous zonule in human and monkey eyes. , 2010, Investigative ophthalmology & visual science.

[41]  D J Coleman,et al.  Unified model for accommodative mechanism. , 1970, American journal of ophthalmology.

[42]  P. Kaufman,et al.  Echothiophate-induced structural alterations in the anterior chamber angle of the cynomolgus monkey. , 1979, Investigative ophthalmology & visual science.

[43]  Adrian Glasser,et al.  Accommodation dynamics in aging rhesus monkeys. , 1998, American journal of physiology. Regulatory, integrative and comparative physiology.

[44]  P. Kaufman,et al.  The development of presbyopia in primates. , 1982, Transactions of the ophthalmological societies of the United Kingdom.

[45]  R. Fisher Is the vitreous necessary for accommodation in man? , 1983, The British journal of ophthalmology.

[46]  P. Kaufman,et al.  Biomechanics of echothiophate-induced anatomic changes in monkey aqueous outflow system , 2005, Graefe's Archive for Clinical and Experimental Ophthalmology.

[47]  P. Kaufman,et al.  Surgical intervention and accommodative responses, I: centripetal ciliary body, capsule, and lens movements in rhesus monkeys of various ages. , 2008, Investigative ophthalmology & visual science.

[48]  P. Kaufman,et al.  Morphologic indication for proprioception in the human ciliary muscle. , 2009, Investigative ophthalmology & visual science.