Hostname: page-component-848d4c4894-jbqgn Total loading time: 0 Render date: 2024-06-23T17:10:33.290Z Has data issue: false hasContentIssue false

The role of the retinal pigment epithelium in eye growth regulation and myopia: A review

Published online by Cambridge University Press:  02 August 2005

JODI RYMER
Affiliation:
School of Optometry, University of California—Berkeley, Berkeley
CHRISTINE F. WILDSOET
Affiliation:
School of Optometry, University of California—Berkeley, Berkeley

Abstract

Myopia is increasing in prevalence world-wide, nearing epidemic proportions in some populations. This has led to expanded research efforts to understand how ocular growth and refractive errors are regulated. Eye growth is sensitive to visual experience, and is altered by both form deprivation and optical defocus. In these cases, the primary targets of growth regulation are the choroidal and scleral layers of the eye that demarcate the boundary of the posterior vitreous chamber. Of significance to this review are observations of local growth modulation that imply that the neural retina itself must be the source of growth-regulating signals. Thus the retinal pigment epithelium (RPE), interposed between the retina and the choroid, is likely to play a critical role in relaying retinal growth signals to the choroid and sclera. This review describes the ion transporters and signal receptors found in the chick RPE and their possible roles in visually driven changes in eye growth. We focus on the effects of four signaling molecules, otherwise implicated in eye growth changes (dopamine, acetylcholine, vasoactive intestinal peptide (VIP), and glucagon), on RPE physiology, including fluid transport. A model for RPE-mediated growth regulation is proposed.

Type
Research Article
Copyright
2005 Cambridge University Press

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

REFERENCES

Bartmann, M., Schaeffel, F., Hagel, G., & Zrenner, E. (1994). Constant light affects retinal dopamine levels and blocks deprivation myopia but not lens-induced refractive errors in chickens. Visual Neuroscience 11, 199208.CrossRefGoogle Scholar
Bedrossian, R.H. (1979). The effect of atropine on myopia. Ophthalmology 86, 713719.CrossRefGoogle Scholar
Buck, C., Schaeffel, F., Simon, P., & Feldkaemper, M. (2004). Effects of positive and negative lens treatment on retinal and choroidal glucagon and glucagon receptor mRNA levels in the chicken. Investigative Ophthalmology and Visual Science 45, 402409.CrossRefGoogle Scholar
Cottriall, C.L., McBrien, N.A., Annies, R., & Leech, E.M. (1999). Prevention of form-deprivation myopia with pirenzepine: A study of drug delivery and distribution. Ophthalmic & Physiological Optics: The Journal of the British College of Ophthalmic Opticians (Optometrists) 19, 327335.CrossRefGoogle Scholar
Cottriall, C.L., Brew, J., Vessey, K.A., & McBrien, N.A. (2001a). Diisopropylfluorophosphate alters retinal neurotransmitter levels and reduces experimentally-induced myopia. Naunyn-Schmiedeberg's Archives of Pharmacology 364, 372382.Google Scholar
Cottriall, C.L., Truong, H.T., & McBrien, N.A. (2001b). Inhibition of myopia development in chicks using himbacine: A role for M(4) receptors? Neuroreport 12, 24532456.Google Scholar
Crewther, D.P. (2000). The role of photoreceptors in the control of refractive state. Progress in Retinal Eye Research 19, 421457.CrossRefGoogle Scholar
Curtin, B. (1985). The Myopias: Basic Science and Clinical Management. Philadelphia, Pennsylvania: Harper & Row.
Diether, S. & Schaeffel, F. (1997). Local changes in eye growth induced by imposed local refractive error despite active accommodation. Vision Research 37, 659668.CrossRefGoogle Scholar
Feldkaemper, M.P. & Schaeffel, F. (2002). Evidence for a potential role of glucagon during eye growth regulation in chicks. Visual Neuroscience 19, 755766.CrossRefGoogle Scholar
Fischer, A.J., McKinnon, L.A., Nathanson, N.M., & Stell, W.K. (1998a). Identification and localization of muscarinic acetylcholine receptors in the ocular tissues of the chick. Journal of Comparative Neurology 392, 273284.Google Scholar
Fischer, A.J., Miethke, P., Morgan, I.G., & Stell, W.K. (1998b). Cholinergic amacrine cells are not required for the progression and atropine-mediated suppression of form-deprivation myopia. Brain Research 794, 4860.Google Scholar
Fischer, A.J., McGuire, J.J., Schaeffel, F., & Stell, W.K. (1999). Light- and focus-dependent expression of the transcription factor ZENK in the chick retina. Nature Neuroscience 2, 706712.CrossRefGoogle Scholar
Fitzgerald, M.E., Wildsoet, C.F., & Reiner, A. (2002). Temporal relationship of choroidal blood flow and thickness changes during recovery from form deprivation myopia in chicks. Experimental Eye Research 74, 561570.CrossRefGoogle Scholar
Fleming, P.A., Harman, A.M., & Beazley, L.D. (1997). Changing topography of the RPE resulting from experimentally induced rapid eye growth. Visual Neuroscience 14, 449461.CrossRefGoogle Scholar
Flitcroft, D., Troilo, D., & Wildsoet, C. (2000). A new perspective on the pharmacological treatment of myopia. In Myopia 2000, ed. Thorn, F., Troilo, D. & Gwiazda, J., pp. 195199. Boston, Massachusetts: Conference on Myopia 2000 Press.
Frambach, D.A. & Misfeldt, D.S. (1983). Furosemide-sensitive Cl transport in embryonic chicken retinal pigment epithelium. American Journal of Physiology 244, F679685.Google Scholar
Friedman, Z., Hackett, S., & Campochiaro, P. (1988). Human retinal pigment epithelial cells possess muscarinic receptors coupled to calcium mobilization. Brain Research 466, 1116.CrossRefGoogle Scholar
Fujikado, T., Hosohata, J., & Omoto, T. (1996). ERG of form deprivation myopia and drug induced ametropia in chicks. Current Eye Research 15, 7986.CrossRefGoogle Scholar
Fujikado, T., Kawasaki, Y., Fujii, J., Taniguchi, N., Okada, M., Suzuki, A., et al. (1997a). The effect of nitric oxide synthase inhibitor on form-deprivation myopia. Current Eye Research 16, 992996.Google Scholar
Fujikado, T., Kawasaki, Y., Suzuki, A., Ohmi, G., & Tano, Y. (1997b). Retinal function with lens-induced myopia compared with form-deprivation myopia in chicks. Graefe's Archive for Clinical and Experimental Ophthalmology 235, 320324.Google Scholar
Gallemore, R.P., Hernandez, E., Tayyanipour, R., Fujii, S., & Steinberg, R.H. (1993). Basolateral membrane Cl and K+ conductances of the dark-adapted chick retinal pigment epithelium. Journal of Neurophysiology 70, 16561668.Google Scholar
Gallemore, R.P., Hughes, B.A., & Miller, S.S. (1997). Retinal pigment epithlial transport mechanisms and their contributions to the electroretinogram. Progress in Retinal Eye Research 16, 509566.CrossRefGoogle Scholar
Gallemore, R.P. & Steinberg, R.H. (1989a). Effects of DIDS on the chick retinal pigment epithelium. I. Membrane potentials, apparent resistances, and mechanisms. Journal of Neuroscience 9, 19681976.Google Scholar
Gallemore, R.P. & Steinberg, R.H. (1989b). Effects of DIDS on the chick retinal pigment epithelium. II. Mechanism of the light peak and other responses originating at the basal membrane. Journal of Neuroscience 9, 19771984.Google Scholar
Gallemore, R.P. & Steinberg, R.H. (1990). Effects of dopamine on the chick retinal pigment epithelium. Membrane potentials and light-evoked responses. Investigative Ophthalmology and Visual Science 31, 6780.Google Scholar
Graham, B. & Judge, S.J. (1999). The effects of spectacle wear in infancy on eye growth and refractive error in the marmoset (Callithrix jacchus). Vision Research 39, 189206.CrossRefGoogle Scholar
Gromada, J., Rorsman, P., Dissing, S., & Wulff, B.S. (1995). Stimulation of cloned human glucagon-like peptide 1 receptor expressed in HEK 293 cells induces cAMP-dependent activation of calcium-induced calcium release. FEBS Letters 373, 182186.CrossRefGoogle Scholar
Guo, S.S., Sivak, J.G., Callender, M.G., & Diehl-Jones, B. (1995). Retinal dopamine and lens-induced refractive errors in chicks. Current Eye Research 14, 385389.CrossRefGoogle Scholar
Hardman, J., Limbird, L., Molinoff, P., Ruddon, R., & Gilman, A., ed. (1996). The Pharmacological Basis of Therapeutics. New York: McGraw-Hill.
Harman, A.M., Hoskins, R., & Beazley, L.D. (1999). Experimental eye enlargement in mature animals changes the retinal pigment epithelium. Visual Neuroscience 16, 619628.Google Scholar
Hirata, A. & Negi, A. (1998). Morphological changes of choriocapillaris in experimentally induced chick myopia. Graefe's Archives for Clinical and Experimental Ophthalmology 236, 132137.CrossRefGoogle Scholar
Hodos, W. & Erichsen, J.T. (1990). Lower-field myopia in birds: An adaptation that keeps the ground in focus. Vision Research 30, 653657.CrossRefGoogle Scholar
Holden, A.L., Hodos, W., Hayes, B.P., & Fitzke, F.W. (1988). Myopia: Induced, normal and clinical. Eye 2 (Suppl.), S242256.CrossRefGoogle Scholar
Hughes, B.A., Gallemore, R.P., & Miller, S.S. (1998). Transport mechanisms in the retinal pigment epithelium. In The Retinal Pigment Epithelium, ed. Marmor, M.F. & Wolfensberger, T.J., pp. 103134. New York: Oxford University Press.
Hung, L.F., Crawford, M.L., & Smith, E.L. (1995). Spectacle lenses alter eye growth and the refractive status of young monkeys. Nature Medicine 1, 761765.CrossRefGoogle Scholar
Hung, L.F., Wallman, J., & Smith, E.L., III (2000). Vision-dependent changes in the choroidal thickness of macaque monkeys. Investigative Ophthalmology and Visual Science 41, 12591269.Google Scholar
Irving, E.L., Sivak, J.G., & Callender, M.G. (1992). Refractive plasticity of the developing chick eye. Ophthalmic & Physiological Optics: The Journal of the British College of Opthalmic Opticians (Optometrists) 12, 448456.CrossRefGoogle Scholar
Iuvone, P.M., Tigges, M., Stone, R.A., Lambert, S., & Laties, A.M. (1991). Effects of apomorphine, a dopamine receptor agonist, on ocular refraction and axial elongation in a primate model of myopia. Investigative Ophthalmology and Visual Science 32, 16741677.Google Scholar
Junghans, B.M., Crewther, S.G., Liang, H., & Crewther, D.P. (1999). A role for choroidal lymphatics during recovery from form deprivation myopia? Optometry and Visual Science: Official Publication of the American Academy of Optometry 76, 796803.Google Scholar
Kee, C.S., Marzani, D., & Wallman, J. (2001). Differences in time course and visual requirements of ocular responses to lenses and diffusers. Investigative Ophthalmology and Visual Science 42, 575583.Google Scholar
Kee, C.-S., Ramamirtham, R., Qiao-Grider, Y., Hung, L.-F., Ward, M., & Smith, E., III (2004). The role of peripheral vision in the refractive-error development of infant monkeys (Macaca mulatta). Investigative Ophthalmology and Visual Science 45, E-1157 available at www.iovs.org.Google Scholar
Keyser, K.T., Hughes, T.E., Whiting, P.J., Lindstrom, J.M., & Karten, H.J. (1988). Cholinoceptive neurons in the retina of the chick: An immunohistochemical study of the nicotinic acetylcholine receptors. Visual Neuroscience 1, 349366.CrossRefGoogle Scholar
Kiyama, H., Katayama-Kumoi, Y., Kimmel, J., Steinbusch, H., Powell, J.F., Smith, A.D., et al. (1985). Three dimensional analysis of retinal neuropeptides and amine in the chick. Brain Research Bulletin 15, 155165.CrossRefGoogle Scholar
Koh, S.W. (1991). VIP stimulation of polarized macromolecule secretion in cultured chick embryonic retinal pigment epithelium. Experimental Cell Research 197, 17.Google Scholar
Koh, S.W. & Chader, G.J. (1984). Elevation of intracellular cyclic AMP and stimulation of adenylate cyclase activity by vasoactive intestinal peptide and glucagon in the retinal pigment epithelium. Journal of Neurochemistry 43, 15221526.CrossRefGoogle Scholar
Kusakari, T., Sato, T., & Tokoro, T. (1997). Regional scleral changes in form-deprivation myopia in chicks. Experimental Eye Research 64, 465476.CrossRefGoogle Scholar
Lauber, J.K. & Oishi, T. (1990). Kainic acid and formoguanamine effects on environmentally-induced eye lesions in chicks. Journal of Ocular Pharmacology 6, 151156.CrossRefGoogle Scholar
Lecchi, M., Marguerat, A., Ionescu, A., Pelizzone, M., Renaud, P., Sommerhalder, J., et al. (2004). Ganglion cells from chick retina display multiple functional nAChR subtypes. Neuroreport 15, 307311.CrossRefGoogle Scholar
Leech, E.M., Cottriall, C.L., & McBrien, N.A. (1995). Pirenzepine prevents form deprivation myopia in a dose dependent manner. Ophthalmic & Physiological Optics: The Journal of the British College of Ophthalmic Opticians (Optometrists) 15, 351356.CrossRefGoogle Scholar
Li, J., Larocca, J.N., Rodriguez-Gabin, A.G., & Charron, M.J. (1997). Expression and signal transduction of the glucagon receptor in betaTC3 cells. Biochimica et Biophysica Acta 1356, 229236.CrossRefGoogle Scholar
Li, J.D., Govardovskii, V.I., & Steinberg, R.H. (1994). Light-dependent hydration of the space surrounding photoreceptors in the cat retina. Visual Neuroscience 11, 743752.CrossRefGoogle Scholar
Li, X.X., Schaeffel, F., Kohler, K., & Zrenner, E. (1992). Dose-dependent effects of 6-hydroxy dopamine on deprivation myopia, electroretinograms, and dopaminergic amacrine cells in chickens. Visual Neuroscience 9, 483492.CrossRefGoogle Scholar
Liang, H., Crewther, D.P., Crewther, S.G., & Barila, A.M. (1995). A role for photoreceptor outer segments in the induction of deprivation myopia. Vision Research 35, 12171225.CrossRefGoogle Scholar
Liang, H., Crewther, S.G., Crewther, D.P., & Pirie, B. (1996). Morphology of the recovery from form deprivation myopia in the chick. Australian and New Zealand Journal of Ophthalmology 24 (2Suppl): 4144.Google Scholar
Liang, H., Crewther, S., Crewther, D., Dickson, M., & Junghans, B. (1998). X-ray microanalysis of the chick choroid and retina in experimental myopia. Investigative Ophthalmology and Visual Science 39, S504.Google Scholar
Liang, H., Crewther, S.G., Crewther, D.P., & Junghans, B.M. (2004). Structural and elemental evidence for edema in the retina, retinal pigment epithelium, and choroid during recovery from experimentally induced myopia. Investigative Ophthalmology and Visual Science 45, 24632474.CrossRefGoogle Scholar
Lin, T., Grimes, P.A., & Stone, R.A. (1993). Expansion of the retinal pigment epithelium in experimental myopia. Vision Research 33, 18811885.CrossRefGoogle Scholar
Lind, G.J., Chew, S.J., Marzani, D., & Wallman, J. (1998). Muscarinic acetylcholine receptor antagonists inhibit chick scleral chondrocytes. Investigative Ophthalmology and Visual Science 39, 22172231.Google Scholar
Luft, W.A., Ming, Y., & Stell, W.K. (2003). Variable effects of previously untested muscarinic receptor antagonists on experimental myopia. Investigative Ophthalmology and Visual Science 44, 13301338.CrossRefGoogle Scholar
Marmor, M.F. (1998a). Control of subretinal fluid and mechanisms of serious detachment. In The Retinal Pigment Epithelium, ed. Marmor, M.F. & Wolfensberger, T.J., pp. 420438. New York: Oxford University Press.
Marmor, M.F. (1998b). Mechanisms of retinal adhesivness. In The Retinal Pigment Epithelium, ed. Marmor, M.F. & Wolfensberger, T.J., pp. 392405. New York: Oxford University Press.
Marmor, M.F. & Wolfensberger, T.J. (1998). The Retinal Pigment Epithelium. New York: Oxford University Press.
Marzani, D. & Wallman, J. (1997). Growth of the two layers of the chick sclera is modulated reciprocally by visual conditions. Investigative Ophthalmology and Visual Science 38, 17261739.Google Scholar
McBrien, N.A., Cottriall, C.L., & Annies, R. (2001). Retinal acetylcholine content in normal and myopic eyes: A role in ocular growth control? Visual Neuroscience 18, 571580.Google Scholar
McBrien, N.A. & Gentle, A. (2001). The role of visual information in the control of scleral matrix biology in myopia. Current Eye Research 23, 313319.CrossRefGoogle Scholar
McBrien, N.A. & Gentle, A. (2003). Role of the sclera in the development and pathological complications of myopia. Progress in Retinal Eye Research 22, 307338.CrossRefGoogle Scholar
McBrien, N.A., Moghaddam, H.O., & Reeder, A.P. (1993). Atropine reduces experimental myopia and eye enlargement via a nonaccommodative mechanism. Investigative Ophthalmology and Visual Science 34, 205215.Google Scholar
McBrien, N.A., Moghaddam, H.O., Cottriall, C.L., Leech, E.M., & Cornell, L.M. (1995). The effects of blockade of retinal cell action potentials on ocular growth, emmetropization and form deprivation myopia in young chicks. Vision Research 35, 11411152.CrossRefGoogle Scholar
McFadden, S. & Wallman, J. (1995). Guinea pig eye growth compensates for spectacle lenses. Investigative Ophthalmology and Visual Science 36 (ARVO Suppl.), S758.Google Scholar
Megaw, P.L., Morgan, I.G., & Boelen, M.K. (1997). Dopaminergic behaviour in chicken retina and the effect of form deprivation. Australian and New Zealand Journal of Ophthalmology 25 (Suppl. 1), S7678.CrossRefGoogle Scholar
Miles, F.A. & Wallman, J. (1990). Local ocular compensation for imposed local refractive error. Vision Research 30, 339349.CrossRefGoogle Scholar
Nao-i, N., Gallemore, R.P., & Steinberg, R.H. (1990). Effects of cAMP and IBMX on the chick retinal pigment epithelium. Membrane potentials and light-evoked responses. Investigative Ophthalmology and Visual Science 31, 5466.Google Scholar
Negi, A. & Marmor, M.F. (1986). Mechanisms of subretinal fluid resorption in the cat eye. Investigative Ophthalmology and Visual Science 27, 15601563.Google Scholar
Nickla, D.L., Wildsoet, C., & Wallman, J. (1997). Compensation for spectacle lenses involves changes in proteoglycan synthesis in both the sclera and choroid. Current Eye Research 16, 320326.CrossRefGoogle Scholar
Norton, T. & Siegwart, J., Jr. (1991). Local myopia produced by partial visual-field deprivation in tree shrew. Society for Neuroscience Abstracts 17, 558.Google Scholar
Norton, T.T., Essinger, J.A., & McBrien, N.A. (1994). Lid-suture myopia in tree shrews with retinal ganglion cell blockade. Visual Neuroscience 11, 143153.CrossRefGoogle Scholar
Ohngemach, S., Hagel, G., & Schaeffel, F. (1997). Concentrations of biogenic amines in fundal layers in chickens with normal visual experience, deprivation, and after reserpine application. Visual Neuroscience 14, 493505.CrossRefGoogle Scholar
Oishi, T. & Lauber, J.K. (1988). Chicks blinded with formoguanamine do not develop lid suture myopia. Current Eye Research 7, 6973.CrossRefGoogle Scholar
Pendrak, K., Nguyen, T., Lin, T., Capehart, C., Zhu, X., & Stone, R.A. (1997). Retinal dopamine in the recovery from experimental myopia. Current Eye Research 16, 152157.CrossRefGoogle Scholar
Pendrak, K., Papastergiou, G.I., Lin, T., Laties, A.M., & Stone, R.A. (2000). Choroidal vascular permeability in visually regulated eye growth. Experimental Eye Research 70, 629637.CrossRefGoogle Scholar
Peterson, W., Meggyesy, C., Yu, K., & Miller, S.S. (1997). Extracellular ATP activates calcium signaling, ion and fluid transport in retinal pigment epithelium. Journal of Neuroscience 17, 23242337.Google Scholar
Peterson, W.M. & Miller, S.S. (1995). Elevation of intracellular cyclic AMP levels in the bovine retinal pigment epithelium (RPE) closes basolateral Cl channels. Investigative Ophthalmology and Visual Science 36, S216.Google Scholar
Peterson, W.M., Quong, J.N., & Miller, S.S. (1998). Mechanisms of fluid transport in retinal pigment epithelium. The Third Great Basin Visual Science Symposium on Retinal Research III, 3442.Google Scholar
Quong, J.N., Quinn, R.H., & Miller, S.S. (1996). Evidence for two types of chloride channels in native fetal human retinal pigment epithelium (Abstract). Investigative Ophthalmology and Visual Science 37, 51109.Google Scholar
Rickers, M. & Schaeffel, F. (1995). Dose-dependent effects of intravitreal pirenzepine on deprivation myopia and lens-induced refractive errors in chickens. Experimental Eye Research 61, 509516.CrossRefGoogle Scholar
Rizzolo, L.J. (1990). The distribution of Na+,K(+)-ATPase in the retinal pigmented epithelium from chicken embryo is polarized in vivo but not in primary cell culture. Experimental Eye Research 51, 435446.CrossRefGoogle Scholar
Rohrer, B., Spira, A.W., & Stell, W.K. (1993). Apomorphine blocks form-deprivation myopia in chickens by a dopamine D2-receptor mechanism acting in retina or pigmented epithelium. Visual Neuroscience 10, 447453.CrossRefGoogle Scholar
Rohrer, B. & Stell, W.K. (1995). Localization of putative dopamine D2-like receptors in the chick retina, using in situ hybridization and immunocytochemistry. Brain Research 695, 110116.CrossRefGoogle Scholar
Rosenfield, M. & Gilmartin, B., ed. (1998). Myopia and nearwork. Oxford; Boston, Massachusetts: Butterworth-Heinemann.
Rymer, J., Miller, S.S., & Edelman, J.L. (2001). Epinephrine increases intracellular [Ca2+] and stimulates KCl-coupled fluid absorption across bovine retinal pigment epithelium. (submitted). Investigative Ophthalmology and Visual Science 42, 19211929.Google Scholar
Sato, T., Yoneyama, T., Kim, H.K., & Suzuki, T.A. (1987). Effect of dopamine and haloperidol on the c-wave and light peak of light-induced retinal responses in chick eye. Documenta Ophthalmologica 65, 8795.CrossRefGoogle Scholar
Schaeffel, F. & Howland, H.C. (1995). Myopia. Vision Research 35, 11351139.CrossRefGoogle Scholar
Schaeffel, F., Glasser, A., & Howland, H.C. (1988). Accommodation, refractive error and eye growth in chickens. Vision Research 28, 639657.CrossRefGoogle Scholar
Schaeffel, F., Hagel, G., Bartmann, M., Kohler, K., & Zrenner, E. (1994). 6-Hydroxy dopamine does not affect lens-induced refractive errors but suppresses deprivation myopia. Vision Research 34, 143149.CrossRefGoogle Scholar
Schaeffel, F., Bartmann, M., Hagel, G., & Zrenner, E. (1995). Studies on the role of the retinal dopamine/melatonin system in experimental refractive errors in chickens. Vision Research 35, 12471264.CrossRefGoogle Scholar
Schaeffel, F., Simon, P., Feldkaemper, M., Ohngemach, S., & Williams, R.W. (2003). Molecular biology of myopia. Clinical and Experimental Optometry: Journal of the Australian Optometrical Association 86, 295307.CrossRefGoogle Scholar
Schmid, K.L. & Wildsoet, C.F. (2004). Inhibitory effects of apomorphine and atropine and their combination on myopia in chicks. Optometry and Vision Science: Official Publication of the American Academy of Optometry 81, 137147.CrossRefGoogle Scholar
Schwahn, H.N., Kaymak, H., & Schaeffel, F. (2000). Effects of atropine on refractive development, dopamine release, and slow retinal potentials in the chick. Visual Neuroscience 17, 165176.Google Scholar
Seko, Y., Tanaka, Y., & Tokoro, T. (1997). Apomorphine inhibits the growth-stimulating effect of retinal pigment epithelium on scleral cells in vitro. Cell Biochemistry and Function 15, 191196.3.0.CO;2-2>CrossRefGoogle Scholar
Seko, Y., Shimokawa, H., Pang, J., & Tokoro, T. (2000). Disturbance of electrolyte balance in vitreous of chicks with form-deprivation myopia. Japanese Journal of Ophthalmology 44, 1519.CrossRefGoogle Scholar
Seltner, R.L. & Stell, W.K. (1995). The effect of vasoactive intestinal peptide on development of form deprivation myopia in the chick: a pharmacological and immunocytochemical study. Vision Research 35, 12651270.CrossRefGoogle Scholar
Siegwart, J., Jr. & Norton, T. (1993). Refractive and ocular changes in tree shrews raised with plus or minus lenses. Investigative Ophthalmology and Visual Science 34, 1208.Google Scholar
Stenkamp, D.L., Iuvone, P.M., & Adler, R. (1994). Photomechanical movements of cultured embryonic photoreceptors: Regulation by exogenous neuromodulators and by a regulable source of endogenous dopamine. Journal of Neuroscience 14, 30833096.Google Scholar
Stone, R., Lin, T., & Laties, A. (1991). Muscarinic Antagonist Effects on Experimental Chick Myopia. Experimental Eye Research 52, 755758.CrossRefGoogle Scholar
Stone, R.A., Laties, A.M., Raviola, E., & Wiesel, T.N. (1988). Increase in retinal vasoactive intestinal polypeptide after eyelid fusion in primates. Proceedings of the National Academy of Sciences of the U.S.A. 85, 257260.CrossRefGoogle Scholar
Stone, R.A., Lin, T., Laties, A.M., & Iuvone, P.M. (1989). Retinal dopamine and form-deprivation myopia. Proceedings of the National Academy of Sciences of the U.S.A. 86, 704706.CrossRefGoogle Scholar
Stone, R.A., Sugimoto, R., Gill, A.S., Liu, J., Capehart, C., & Lindstrom, J.M. (2001). Effects of nicotinic antagonists on ocular growth and experimental myopia. Investigative Ophthalmology and Visual Science 42, 557565.Google Scholar
Troilo, D., Gottlieb, M.D., & Wallman, J. (1987). Visual deprivation causes myopia in chicks with optic nerve section. Current Eye Research 6, 993999.CrossRefGoogle Scholar
Truong, H.T., Cottriall, C.L., Gentle, A., & McBrien, N.A. (2002). Pirenzepine affects scleral metabolic changes in myopia through a non-toxic mechanism. Experimental Eye Research 74, 103111.CrossRefGoogle Scholar
Vessey, K.A., Cottriall, C.L., & McBrien, N.A. (2002). Muscarinic receptor protein expression in the ocular tissues of the chick during normal and myopic eye development. Brain Research Developmental Brain Research 135, 7986.CrossRefGoogle Scholar
Wallman, J., Turkel, J., & Trachtman, J. (1978). Extreme myopia produced by modest change in early visual experience. Science 201, 12491251.CrossRefGoogle Scholar
Wakelam, M.J., Murphy, G.J., Hruby, V.J., & Houslay, M.D. (1986). Activation of two signal-transduction systems in hepatocytes by glucagon. Nature 323, 6871.CrossRefGoogle Scholar
Wallman, J., Wildsoet, C., Xu, A.M., Gottlieb, M.D., Nickla, D.L., Marran, L., et al. (1994). Moving the Retina—Choroidal Modulation of Refractive State. Vision Research 35, 3750.Google Scholar
Wallman, J., Wildsoet, C., Xu, A., Gottlieb, M.D., Nickla, D.L., Marran, L., et al.. (1995). Moving the retina: Choroidal modulation of refractive state. Vision Research 35, 3750.CrossRefGoogle Scholar
Wallman, J. & Winawer, J. (2004). Homeostasis of eye growth and the question of myopia. Neuron 43, 447468.CrossRefGoogle Scholar
Westbrook, A.M., Crewther, S.G., Liang, H., Beresford, J.A., Allen, M., Keller, I., et al. (1995). Formoguanamine-induced inhibition of deprivation myopia in chick is accompanied by choroidal thinning while retinal function is retained. Vision Research 35, 20752088.CrossRefGoogle Scholar
Westbrook, A.M., Crewther, D.P., & Crewther, S.G. (1999). Cone receptor sensitivity is altered in form deprivation myopia in the chicken. Optometry and Vision Science: Official Publication of the American Academy of Optometry 76, 326338.CrossRefGoogle Scholar
Wildsoet, C. (1998). Choroidal influences on refractive development—A novel role for the choroid. Experimental Eye Research 67, S14.Google Scholar
Wildsoet, C. (2003). Neural pathways subserving negative lens-induced emmetropization in chicks—insights from selective lesions of the optic nerve and ciliary nerve. Current Eye Research 27, 371385.CrossRefGoogle Scholar
Wildsoet, C. & Wallman, J. (1995). Choroidal and scleral mechanisms of compensation for spectacle lenses in chicks. Vision Research 35, 11751194.CrossRefGoogle Scholar
Wildsoet, C., McBrien, N., & Clark, I. (1994). Atropine inhibition of lens-induced effects in chicks: Evidence for similar mechanisms underlying form deprivation and lens-induced myopia. Investigative Ophthalmology and Visual Science 35 (ARVO Suppl), 2068.Google Scholar
Wildsoet, C.F. (1997). Active emmetropization—Evidence for its existence and ramifications for clinical practice. Ophthalm Physiol Optics 17, 279290.CrossRefGoogle Scholar
Wildsoet, C.F. & Pettigrew, J.D. (1988). Kainic acid-induced eye enlargement in chickens: Differential effects on anterior and posterior segments. Investigative Ophthalmology and Visual Science 29, 311319.Google Scholar
Winawer, J. & Wallman, J. (2002). Temporal constraints on lens compensation in chicks. Vision Research 42, 26512668.CrossRefGoogle Scholar
Wioland, N., Rudolf, G., & Bonaventure, N. (1990). Electrooculographic and electroretinographic study in the chicken after dopamine and haloperidol. Documenta Ophthalmologica 75, 175180.CrossRefGoogle Scholar
Yew, K. & Wildsoet, C. (2003). The usual effects of high-power negative lens and diffusers show differential susceptibility to disruption to the diurnal light cycle. Investigative Ophthalmology and Visual Science 44, E-Abstract 1979.Google Scholar
Yin, G.C., Gentle, A., & McBrien, N.A. (2004). Muscarinic antagonist control of myopia: A molecular search for the M1 receptor in chick. Molecular Vision 10, 787793.Google Scholar
Yinon, U. & Koslowe, K.C. (1986). Hypermetropia in dark reared chicks and the effect of lid suture. Vision Research 26, 9991005.CrossRefGoogle Scholar