Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-19T22:35:36.919Z Has data issue: false hasContentIssue false

Lid-suture myopia in tree shrews with retinal ganglion cell blockade

Published online by Cambridge University Press:  02 June 2009

Thomas T. Norton
Affiliation:
Department of Physiological Optics, School of Optometry/The Medical Center, University of Alabama at Birmingham, Birmingham, AL
John A. Essinger
Affiliation:
Department of Physiological Optics, School of Optometry/The Medical Center, University of Alabama at Birmingham, Birmingham, AL
Neville A. McBrien
Affiliation:
Department of Optometry and Vision Sciences, University of Wales College of Cardiff, P.O. Box 905, Cardiff CF1 3XF, Wales, United Kingdom

Abstract

To determine whether central communication of retinal signals is necessary for the development of an experimentally induced myopia, tree shrews were exposed to monocular deprivation (MD) while the action potentials of retinal cells in the deprived eye were blocked with intravitreally injected tetrodotoxin (TTX-MD animals). TTX injections (0.6 μ 3 μL) and MD began about 15 days after eye opening, at the start of the susceptible period for the development of lid-suture myopia. Six injections were given, one every second day to produce 12 days of MD and TTX-blockade. Control TTX animals (TTX-open) received TTX in one eye, but not MD, on the same injection schedule and were always found to be behaviorally unresponsive to visual stimuli through the injected eye indicating that TTX blocked central communication of action potentials. Other control animals received intravitreally injected saline in either an open eye (saline-open), or an MD eye (saline-MD). A sham-injected group (sham-inj-MD) received MD and all anesthetic and surgical manipulations except for penetration of the sclera. In all groups, one eye in each animal was an untreated control.

Two effects were found. All MD groups, including the TTX-MD animals, developed a significant vitreous chamber elongation in the deprived eye, indicating that an experimental myopia developed despite ganglion cell blockade. Thus, retinal mechanisms in tree shrew can detect the presence of a degraded visual image and produce an experimental myopia that does not depend on the receipt of visual messages by central neural structures. In addition, eyes in which the sclera was punctured had smaller vitreous chamber depths than comparable uninjected eyes, indicating that puncturing the sclera reduced the normal elongation. These data suggest that forces within the eye normally contribute to its expansion and may be resisted by the choroid and/or the sclera.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Campbell, C.B.G. (1966). Taxonomic status of tree shrews. Science 153, 436.CrossRefGoogle ScholarPubMed
Cartmill, M. (1974). Rethinking primate origins. Science 184, 436443.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Condo, G. (1988). The effect of altered neuronal activity on the development of layers in the lateral geniculate nucleus (LGN). Journal of Neuroscience 8, 395416.CrossRefGoogle Scholar
Coulombre, A.J. (1956). The role of intraocular pressure in the development of the chick eye. Journal of Experimental Zoology 133, 211225.CrossRefGoogle Scholar
Dowling, J.E. (1970). Organization of vertebrate retinas. Investigative Ophthalmology and Visual Science 9, 655680.Google ScholarPubMed
Dubin, M.W., Stark, L.A. & Archer, S.M. (1986). A role for action potential activity in the development of neuronal connections in the kitten retinogeniculate pathway. Journal of Neuroscience 6, 10211036.CrossRefGoogle ScholarPubMed
Glickstein, M. & Millodot, M. (1970). Retinoscopy and eye size. Science 168, 605606.CrossRefGoogle ScholarPubMed
Gottlieb, M.D. & Wallman, J. (1987). Retinal activity modulates eye growth: Evidence from rearing in stroboscopic illumination. Society for Neuroscience Abstracts 13, 1297.Google Scholar
Hein, A. & Held, R. (1967). Dissociation of the visual placing response into elicited and guided components. Science 158, 390392.CrossRefGoogle ScholarPubMed
Hoyt, C.S., Stone, R.D., Frommer, C. & Billson, F.A. (1981). Monocular axial myopia associated with neonatal eyelid closure in human infants. American Journal of Ophthalmology 91, 197200.CrossRefGoogle ScholarPubMed
Irving, E.L., Callender, M.G. & Sivak, J.G. (1991). Inducing myopia, hyperopia and astigmatism in chicks. Optometry and Vision Science 68, 364368.CrossRefGoogle ScholarPubMed
Lauber, J.K., McGinnis, J. & Boyd, J. (1965). Influence of miotics, Diamox and vision occluders on light-induced buphthalmos in domestic fowl. Proceedings of the Society for Developmental Biology and Medicine 120, 572575.CrossRefGoogle ScholarPubMed
Luckett, W.P. (1980). Comparative Biology and Evolutionary Relationships of Tree Shrews. New York: Plenum Press, pp. 1314.CrossRefGoogle Scholar
Marsh-Tootle, W.L. & Norton, T.T. (1989). Refractive and structural measures of lid-suture myopia in tree shrew. Investigative Ophthalmology and Visual Science 30, 22452257.Google ScholarPubMed
McBrien, N.A. & Barnes, D.A. (1984). A review and evaluation of theories of refractive error development. Ophthalmic and Physiological Optics 4, 201213.CrossRefGoogle ScholarPubMed
McBrien, N.A. & Norton, T.T. (1988). Experimental myopia in tree shrew is increased by treatment with lathyritic agents. Investigative Ophthalmology and Visual Science (Suppl.) 29, 33.Google Scholar
McBrien, N.A. & Norton, T.T. (1992). The development of experimental myopia and ocular component dimensions in monocularly lid-sutured tree shrews. Vision Research 32, 843852.CrossRefGoogle ScholarPubMed
McBrien, N.A., Norton, T.T. & McKanna, J.A. (1989). Scleral and corneal morphometry in lathyritic-enhanced experimental myopia in tree shrew. Investigative Ophthalmology and Visual Science (Suppl.) 30, 32.Google Scholar
McBrien, N.A., Moghaddam, H.O., New, R. & Williams, L.R. (1993). Experimental myopia in a diurnal mammal (Sciurus carolinensis) with no accommodative ability. Journal of Physiology 469, 427441.CrossRefGoogle Scholar
McKanna, J.A. & Casagrande, V.A. (1978). Reduced lens development in lid-suture myopia. Experimental Eye Research 26, 715723.CrossRefGoogle ScholarPubMed
Moghaddam, H.O. & McBrien, N.A. (1993). The effects of blockade of retinal ganglion cell action potentials on ocular growth and form-deprivation myopia in the chick. Ophthalmic and Physiological Optics (Abstract) (Oxford) 13, 105.Google Scholar
Nakamura, Y., Nadajima, S. & Grundfest, H. (1965). The action of tetrodotoxin on electrogenic components of squid giant axons. Journal of General Physiology 48, 985996.CrossRefGoogle ScholarPubMed
Norton, T.T. (1990). Experimental myopia in tree shrews. In Myopia and the Control of Eye Growth, (Ciba Foundation Symposium 155), ed. Bock, G. & Widdows, K., pp. 178199. Chichester, England: John Wiley & Sons.Google Scholar
Norton, T.T. & McBrien, N.A. (1992). Normal development of refractive state and ocular component dimensions in the tree shrew (Tupaia belangeri). Vision Research 32, 833842.CrossRefGoogle ScholarPubMed
Norton, T.T., Essinger, J.A. & McBrten, N.A. (1989). Lid-suture myopia in tree shrew despite blockade of ganglion cell action potentials. Investigative Ophthalmology and Visual Science (Suppl.) 30, 31.Google Scholar
Norton, T.T., Rada, J.A. & Hassell, J.R. (1992). Extracellular matrix changes in the sclera of tree shrews with induced myopia. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1054.Google Scholar
O'Leary, D.J. & Millodot, M. (1979). Eyelid closure causes myopia in humans. Experientia 35, 14781479.CrossRefGoogle ScholarPubMed
Pickett-Seltner, R.L., Sivak, J.G. & Pasternak, J.J. (1988). Experimentally induced myopia in chicks: Morphometric and biochemical analysis during the first 14 days after hatching. Vision Research 28, 323328.CrossRefGoogle ScholarPubMed
Rabin, J., Van Sluyters, R.C. & Malach, R. (1981). Emmetropization, a vision-dependent phenomenon. Investigative Ophthalmolgy and Visual Science 20, 561564.Google ScholarPubMed
Raviola, E. & Wiesel, T.N. (1990). Neural control of eye growth and experimental myopia in primates. In Myopia and the Control of Eye Growth, (Ciba Foundation Symposium 155), ed. Bock, G. & Widdows, K., pp. 2244. Chichester, England: John Wiley & Sons.Google ScholarPubMed
Reeder, A.P. & McBrien, N.A. (1993). Biochemical changes in the sclera of tree shrews with high degrees of experimental myopia. Ophthalmic and Physiological Optics (Abstract) (Oxford) 13, 105.Google Scholar
Robb, R.M. (1977). Refractive errors associated with hemangiomas of the eyelids and orbit in infancy. American Journal of Ophthalmology 83, 5258.CrossRefGoogle ScholarPubMed
Schaeffel, F., Glasser, A. & Howland, H.C. (1988). Accommodation, refractive error and eye growth in chickens. Vision Research 28, 639657.CrossRefGoogle ScholarPubMed
Schmid, K.L., Wildsoet, C.F. & Pettigrew, J.D. (1993). The effect of daily periods of normal vision on refractive adaptation in chicks. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1208.Google Scholar
Sherman, S.M., Norton, T.T. & Casagrande, V.A. (1977). Myopia in the lid-sutured tree shrew (Tupaia glis). Brain Research 124, 154157.CrossRefGoogle ScholarPubMed
Shih, Y.-F., Fitzgerald, M.E.C., Norton, T.T., Gamlin, P.D.R., Hodos, W. & Reiner, A. (1993). Reduction in choroidal blood flow occurs in chicks wearing goggles that induce eye growth toward myopia. Current Eye Rresearch 12, 219227.Google ScholarPubMed
Siegwart, J.T. Jr & Norton, T.T. (1990). The sensitive period for experimental myopia in tree shrew. Investigative Ophthalmology and Visual Science (Suppl.) 31, 254.Google Scholar
Siegwart, J.T. Jr & Norton, T.T. (1993). Refractive and ocular changes in tree shrews raised with plus or minus lenses. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1208.Google Scholar
Sommers, D., Kaiser-Kupfer, M.I. & Kupfer, C. (1978). Increased axial length of the eye following neonatal lid suture as measured with A-scan ultrasonography. Investigative Ophthalmology and Visual Science (Suppl.) 17, 295.Google Scholar
Stenstrom, S. (1946). Investigation of the variation and the correlation of the optical elements of human eyes (translated by D. Woolf). American Journal of Optometry and Archives of American Academy of Optometry Monographs Monograph 58, 1948.Google Scholar
Straub, M. (1909). Uber die Aetiologie der Brechungsonomalien des Auges un den Ursprung der Emmetropie. Albrecht v. Graefes Archive der Ophthalmologie 29, 130199.CrossRefGoogle Scholar
Stryker, M.P. & Harris, W.A. (1986). Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. Journal of Neuroscience 6, 21172133.CrossRefGoogle ScholarPubMed
Troilo, D., Gottlieb, M.D. & Wallman, J. (1987). Visual deprivation causes myopia in chicks with optic nerve section. Current Eye Research 6, 993999.CrossRefGoogle ScholarPubMed
Troilo, D. (1990). Experimental studies of emmetropization in the chick. In Myopia and the Control of Eye Growth, (Ciba Foundation Symposium 155), ed. Bock, G. & Widdows, K., pp. 89114. Chichester, England: John Wiley & Sons.Google Scholar
Troilo, D. & Judge, S.J. (1993). Ocular development and visual deprivation myopia in the common marmoset (Callithrix jacchus). Vision Research 33, 13111324.CrossRefGoogle ScholarPubMed
Troilo, D., Glasser, A., Li, T. & Howland, H. (1992). Different strains of chick have different eye growth responses to visual deprivation. Investigative Ophthalmology and Visual Science (Suppl.) 33, 711.Google Scholar
Tron, E. (1929). The optical elements of the refractive power of the eye. Archive für Ophthalmologie 122, 133.Google Scholar
Van Alphen, G.W.H.M. (1961). On emmetropia and ametropia. Ophthalmologica (Suppl.) 142, 192.CrossRefGoogle Scholar
Van Alphen, G.W.H.M. (1986). Choroidal stress and emmetropization. Vision Research 26, 723734.CrossRefGoogle ScholarPubMed
Wallman, J. (1990). Introduction. In Myopia and the Control of Eye Growth, (Ciba Foundation Symposium 155), ed. Bock, G. & Widdows, K., pp. 14. Chichester, England: John Wiley & Sons.Google ScholarPubMed
Wallman, J., Turkel, J. & Trachtman, J. (1978). Extreme myopia produced by modest change in early visual experience. Science 201, 12491251.CrossRefGoogle ScholarPubMed
Wallman, J., Adams, J.I. & Trachtman, J.N. (1981). The eyes of young chickens grow toward emmetropia. Investigative Ophthalmology and Visual Science 20, 557561.Google ScholarPubMed
Wallman, J. & Adams, J.I. (1987). Developmental aspects of experimental myopia in chicks: Susceptibility, recovery and relation to emmetropization. Vision Research 27, 11391163.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Raviola, E. (1977). Myopia and eye enlargement after neonatal lid fusion in monkeys. Nature 266, 6668.CrossRefGoogle ScholarPubMed
Wildsoet, C.F. & Pettigrew, J.D. (1988). Experimental myopia and anomalous eye growth patterns unaffected by optic nerve section in chickens: Evidence for local control of eye growth. Clinical Vision Sciences 3, 99107.Google Scholar
Wong-Riley, M. & Carroll, E.W. (1984). Effects of impulse blockage on cytochrome oxidase activity in monkey visual cortex. Nature 307, 262264.Google Scholar
Wong-Riley, M.T.T. & Norton, T.T. (1988). Histochemical localization of cytochrome oxidase activity in the visual system of the tree shrew: Normal patterns and the effect of retinal impulse blockage. Journal of Comparative Neurology 273, 562578.CrossRefGoogle Scholar