Abstract
Numerous degenerative changes in the visual system occur with age, including a loss of accommodative function possibly related to hardening of the lens or loss of ciliary muscle mobility. The rhesus monkey is a reliable animal model for studying age-related changes in ocular function, including loss of accommodation. Calorie restriction (CR) is the only consistent intervention to slow aging and extend lifespan in rodents, and more recently the beneficial effects of CR have been reported in nonhuman primates. The goal of the present study was to evaluate age-related changes in ocular accommodation and the potential effect of long-term (>8 years) CR on accommodation in male and female rhesus monkeys. Refraction, accommodation (Hartinger coincidence refractometer), and lens thickness (A-scan ultrasound) were measured in 97 male and female rhesus monkeys age 8–36 years under Telazol/acepromazine anesthesia. Refraction and accommodation measurements were taken before and after 40% carbachol corneal iontophoresis to induce maximum accommodation. Half the animals were in the control (CON) group and were fed ad libitum. The CR group received 30% fewer calories than age- and weight-matched controls. Males were on CR for 12 years and females for eight years. With increasing age, accommodative ability declined in both CON and CR monkeys by 1.03 ± 0.12 (P = 0.001) and 1.18 ± 0.12 (P = 0.001) diopters/year, respectively. The age-related decline did not differ significantly between the groups (P = 0.374). Baseline lens thickness increased with age in both groups by 0.03 ± 0.005 mm/year (P = 0.001) and 0.02 ± 0.005 mm/year (P = 0.001) for the CON and CR groups, respectively. The tendency for the for the lens to thicken with age occurred at a slower rate in the CR group vs. the CON group but the difference was not statistically significant (P = 0.086). Baseline refraction was −2.8 ± 0.55 and −3.0 ± 0.62 diopters for CON and CR, respectively. Baseline refraction tended to become slightly more negative with age (P = 0.070), but this trend did not differ significantly between the groups (P = 0.587). In summary, there was no difference in the slope of the age-related changes in accommodation, lens thickness, or refraction in the carbachol-treated eyes due to diet. These data are consistent with previous findings of decreased accommodative ability in aging rhesus monkeys, comparable to the age-dependent decrease in accommodative ability in humans. This study is the first to indicate that the accommodative system may not benefit from calorie restriction.
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Bito LZ, DeRousseau CJ and Kaufman PL et al. (1982) Age-dependent loss of accommodative amplitude in rhesus monkeys: an animal model for presbyopia. Invest Ophthalmol Vis Sci 23: 23–31
Crawford K, Terasawa E and Kaufman PL (1989) Reproducible stimulation of ciliary muscle contraction in the cynomolgus monkey via a permanent indwelling midbrain electrode. Brain Res 503: 265–272
Crawford K, Gabelt BT and Kaufman PL et al. (1990) Effect of various anesthetic and autonomic drugs on refraction in monkeys. Curr Eye Res 9: 525–532
Croft MA, Kaufman PL and Crawford KS et al. (1998) Accommodation dynamics in aging rhesus monkeys. Am J Phys 44: R1885–R1897
Duane A (1922) Studies in monocular and binocular accommodation with their clinical applications. Am J Ophthalmol 5: 867–877
Fincham E (1937) The mechanism of accommodation. Br J Ophthalmol 8: 7–80
Fisher RF (1969) Elastic constants of the human lens capsule. J Phys (London) 201: 1–19
Fisher RF (1973) Presbyopia and the changes with age in the human crystalline lens. J Phys (London) 228: 765–779
Glasser A and Campbell MCW (1998) Presbyopia and the optical changes in the human crystalline lens with age. Vis Res 38(2): 209–229
Ingram DK, Cutler RG and Weindruch R et al. (1990) Dietary restriction and aging: the initiation of a primate study. J Gerontol 45(5): B148–B163
Kaufman PL (1992) Accommodation and presbyopia: neuromuscular and biophysical aspects. In: Hart WM Jr (ed) Adler’s Physiology of the Eye: Clinical Application, pp 391–411. Mosby, St. Louis, MO
Kaufman PL and Bito LZ (1982) The occurrence of senile cataracts, ocular hypertension, and glaucoma in rhesus monkeys: an animal model for presbyopia. Exp Eye Res 34: 287–291
Kaufman PL and Davis GE (1980) “Minified” Goldmann applanating prism for tonometry in monkeys and humans. Arch Ophthalmol 98: 542–546
Kaufman PL, Bito LZ and DeRousseau CJ (1982) The development of presbyopia in primates. Trans Ophthalmol Soc UK 102: 323–326
Kawai S-I, Vora S and Das S et al. (2001) Modeling of risk factors for the degeneration of retinal ganglion cells following ischemia/reperfusion in rats: effects of age, caloric restriction, diabetes, pigmentation and glaucoma. FASEB j 15: 1285–1287
Kemnitz JW, Weindruch R and Roecker EB et al. (1993) Dietary restriction of adult male rhesus monkeys: design, methodology, and preliminary findings from the first year of study. J Gerontol 48: B17–B26
Koretz JF, Bertasso AM and Neider MW et al. (1987) Slit-lamp studies of the rhesus monkey eye. II. Changes in crystalline lens shape, thickness and position during accommodation and aging. Exp Eye Res 45: 317–326
Lane MA, Ingram DK and Ball SS et al. (1997) Dehydroepiandrosterone sulfate: a biomarker of primate aging slowed by calorie restriction. J Clin Endocrinol Metab 82: 2093–2096
Lane MA, Black A and Ingram DK et al. (1998) Calorie restriction in nonhuman primates: implications for age-related disease risk. J Anti-Aging Med 1: 315–325
Mattison JA, Black A and Huck J et al. (2005) Age-related decline in caloric intake and motivation for food in rhesus monkeys. Neurobiol Aging 26: 1117–1127
Neufeld AH and Gachie EN (2003) The inherent, age-dependent loss of retinal ganglion cells is related to the lifespan of the species. Neurobiol Aging 24: 167–172
Obin M, Halbleib M and Lipman R et al. (2000a) Calorie restriction increases light-dependent photoreceptor cell loss in the neural retina of Fischer 344 rats. Neurobiol Aging 21: 639–645
Obin M, Pike A and Halbleib M et al. (2000b) Calorie restriction modulates age-dependent changes in the retinas of Brown Norway rats. Mech Ageing Dev 114: 133–147
O’Steen WK and Landfield PW (1991) Dietary restriction does not alter retinal aging in the Fischer 344 rat. Neurobiol Aging 12: 455–462
Owens DA and Liebowitz HW (1980) The intermediate resting point of accommodation: recent evidence and applications. Proc Int Soc Eye Res 1: 71
Pau H and Krantz J (1991) The increasing sclerosis of the human lens with age and its relevance to accommodation and presbyopia. Graefe’s Arch Clin Exp Ophthalmol 229: 294–296
Roth GS, Lesnikov V and Lesnikov M et al. (2001) Dietary caloric restriction prevents the age-related decline in plasma melatonin levels of rhesus monkeys. J Clin Endocrinol Metab 86: 3292–3295
Tamm E, Lutjen-Drecoll E and Jungkunz W et al. (1991) Posterior attachment of ciliary muscle in young, accommodating old, presbyopic monkeys. Investig Ophthalmol Vis Sci 32(5): 1678–1692
Tamm E, Croft MA and Jungkunz W et al. (1992) Age-related loss of ciliary muscle mobility in the rhesus monkey: role of the choroid. Arch Ophthalmol 110: 871–876
Undie AS and Friedman E (1993) Diet restriction prevents aging-induced deficits in brain phosphoinositide metabolism. J Gerontol 48: B62–B67
Warren MA, Freestone T and Thomas AJ (1989) Undernutrition during early adult life significantly affects neuronal connectivity in rat visual cortex. Exp Neurol 103: 290–292
Westheimer G and Blair SM (1973) Accommodation of the eye during sleep and anesthesia. Vis Res 13: 1035–1036
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Mattison, J.A., Croft, M.A., Dahl, D.B. et al. Accommodative function in rhesus monkeys: effects of aging and calorie restriction. AGE 27, 59–67 (2005). https://doi.org/10.1007/s11357-005-4005-8
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DOI: https://doi.org/10.1007/s11357-005-4005-8