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Effect of choroidal and ciliary nerve transection on choroidal blood flow, retinal health, and ocular enlargement

Published online by Cambridge University Press:  02 June 2009

Yung-Feng Shih ,
Malinda E. C. Fitzgerald  and
Anton Reiner
Yung-Feng Shih
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee —Memphis, Memphis
Malinda E. C. Fitzgerald
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee —Memphis, Memphis
Anton Reiner
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee —Memphis, Memphis
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Abstract

Our previous studies suggested that reduced choroidal blood flow (CBF) occurs with manipulations that yield myopic eye growth and that these reductions are primarily a consequence of the ocular enlargement. We could not entirely rule out the possibility, however, that reductions in CBF are at least to some extent antecedent and causal to the ocular enlargement. We therefore in the present study examined the effects on eye size of artificially reducing CBF by unilaterally transecting the choroidal nerves of the ciliary ganglion in four-day-old chicks. For comparison, we also transected the ciliary nerves in a second group of chicks or transected both ciliary and choroidal nerves in a third group of chicks. The effects of the nerve transections were evaluated in comparison to the effects of the orbital surgery itself (without nerve transection) in a fourth group termed the sham-operated control group. Two weeks after transection, CBF was measured using laser Doppler velocimetry, the ocular axial, nasotemporal and dorsoventral lengths were measured, and the eyes weighed.

The results showed that CBF in birds with either choroidal nerve cuts or choroidal plus ciliary nerve cuts was greatly reduced in the treated eye (20–40% of nontreated eye). The treated eyes of these birds also showed gross depigmentation and histologically evident loss of the outer retina, most typically in the temporal retina. Birds with ciliary nerve cuts showed increased CBF in both eyes (131% right eye and 154% left eye compared to shams). Since ciliary nerve cuts yield fixed dilated pupils, increased CBF with ciliary nerve cuts appears consistent with the previously reported involvement of the choroidal nerves within a neural circuit subserving light-mediated upregulation of CBF. Clear effects on eye size were observed in the treated eyes in each group. The sham surgery alone yielded slight enlargement of the right eye compared to left eye, particularly in the axial dimension. In the choroidal nerve and the both nerve cut groups, nasotemporal and dorsoventral elongation were slightly diminished in the treated eyes compared to the sham-treated eyes. In contrast, enlargement of the right eye was slightly enhanced in the ciliary nerve cut group compared to the sham-treated eyes. The overall results suggest that large decreases in CBF do not enhance myopic eye growth, although large increases in CBF may.

Keywords

Choroidal nerveCiliary nerveChoroidal blood flowMyopiaRetinal degeneration
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 5 , September 1993 , pp. 969 - 979
Copyright
Copyright © Cambridge University Press 1993

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References

Auker, C.R., Parver, L.M., Doyle, T. & Carpenter, D.O. (1982). Choroidal blood flow: 1. Ocular tissue temperature as a measure of flow. Archives of Ophthalmology 100, 1323–1326.CrossRefGoogle Scholar
Avetisov, E.S. & Savitaskaya, N.F. (1977). Some features of ocular microcirculation in myopia. Annual of Ophthalmology 9, 1261–1264.Google ScholarPubMed
Bonner, R.F. & Nossal, R. (1990). Principals of Laser-Doppler flowmetry. In Laser-Doppler Blood Flowmetry, ed. Shepherd, A.P. & Öberg, P.A., pp. 17–45, Norwell, Massachusetts: Kluwer Academic Publishers.CrossRefGoogle Scholar
Borgos, J.A. (1990). TSI's LDV blood flowmeter. In Laser-Doppler Blood Flowmetry, ed. Shepherd, A.P. & Öberg, P.A., pp. 73–92. Norwell, Massachusetts: Kluwer Academic Publishers.CrossRefGoogle Scholar
Caldwell, R.B. & Fitzgerald, M.E.C. (1991). The choriocapillaris in spontaneously diabetic rats. Microvascular Research 42, 229–244.CrossRefGoogle ScholarPubMed
Curtin, B.J. (1985). The Myopias: Basic and Clinical Management. Philadelphia, Pennsylvania: Harper&Row.Google Scholar
Cuthbertson, S., Fitzgerald, M.E.C., Shih, Y.-F., White, J. & Reiner, A. (1993). Distribution of ciliary ganglion nerve fibers in the avian choroid. Investigative Ophthalmology and Visual Science (Suppl.)34, 1393.Google Scholar
Ehrlich, D., Sattayasai, J., Zappia, J. & Barrington, M. (1990). Effects of selective neurotoxins on eye growth in the young chick. In Myopia and the Control of Eye Growth, ed. Bock, G.R. & Wid-Dows, K., pp. 63–88. Chichester, England: John Wiley and Sons.Google Scholar
Ernest, J. & Goldstick, T. (1979). Choroidal blood flow measurement in the monkey by clearance of indocyanine green dye. Experimental Eye Research 29, 7–14.CrossRefGoogle ScholarPubMed
Fitzgerald, M.E.C. & Caldwell, R.B. (1990). The retinal microvas-culature of spontaneously diabetic BB rats: Structure and luminal surface properties. Microvascular Research 39, 15–27.CrossRefGoogle Scholar
Fitzgerald, M.E.C. & Reiner, A. (1989). Lesions of the nucleus of Edinger-Westphal deleteriously affect photoreceptors in avian retina. Investigative Ophthalmology and Vision Science 30, 464.Google Scholar
Fitzgerald, M.E.C. & Reiner, A. (1990). Light-mediated reflexive control of choroidal blood flow in the pigeon eye. Society for Neuroscience Abstracts 16, 1077.Google Scholar
Fitzgerald, M.E.C, Vana, B.A. & Reiner, A. (1990 a). Evidence for retinal pathology following interruption of neural regulation of choroidal blood flow: Müller cells express GFAP following lesions of the nucleus of Edinger-Westphal in pigeons. Current Eye Research 9, 583–598.CrossRefGoogle ScholarPubMed
Fitzgerald, M.E.C, Vana, B.A. & Reiner, A. (1990 b). Control of choroidal blood flow by the nucleus of Edinger-Westphal: A laser-Doppler study. Investigative Ophthalmology and Visual Science 31, 2483–2492.Google ScholarPubMed
Fitzgerald, M.E.C, Shih, Y.F. & Reiner, A. (1992). Effects of choroidal and ciliary nerve cuts on choroidal blood flow and ocular growth. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1053.Google Scholar
Gamlin, P.D.R., Reiner, A., Erichsen, J.T., Karten, H.J. & Cohen, D.H. (1984). The neural substrate for the pupillary light reflex in the pigeon (Columba livia). Journal of Comparative Neurology 226, 523–543.CrossRefGoogle ScholarPubMed
Gay, A.J., Golder, H. & Smith, M. (1964). Chorioretinal vascular occlusions with latex spheres. Investigative Ophthalmology 3, 647–656.Google ScholarPubMed
Gherezghiher, T., Okubo, H. & Koss, M.C. (1991). Choroidal and ciliary body blood flow analysis: Application of laser Doppler flowmetry in experimental animals. Experimental Eye Research 13, 151–156.CrossRefGoogle Scholar
Giovannini, A., Colombati, S. & Tosti, G. (1988). Pathogenic myopia and pharmaceutical agents: Rheooculographic experience. Acta Ophthalmologica (Suppl.) 185 (66), 100–101.CrossRefGoogle Scholar
Colder, H. & Gay, A.J. (1967). Chorioretinal vascular occlusions with latex microspheres (a long-term study). Part II. Investigative Ophthalmology 6, 51–58.Google Scholar
Goldschmidt, E. (1990). Myopia in humans: Can progression be arrested? In Myopia and the Control of Eye Growth, ed. Bock, G.R. & Widdows, K., pp. 222–234. Chichester, England: John Wiley and Sons.Google Scholar
Hodos, W. & Kuenzel, W.J. (1984). Retinal-image degradation produces ocular enlargement in chicks. Investigative Ophthalmology and Visual Science 25, 652–659.Google ScholarPubMed
Kirk, R.E. (1982). Multiple comparison tests. In Experimental Design: Procedures for the Behavioral Sciences, pp. 106–110. Monterey, California: Brooks/Cole Publishing.Google Scholar
Lin, T. & Stone, R. (1991). Autonomic and visual interactions in the regulation of eye growth and refraction. Investigative Ophthalmology and Visual Science (Suppl.) 32, 1202.Google Scholar
McKanna, J.A. & Casagrande, V.A. (1978). Reduced lens development in lid-suture myopia. Experimental Eye Research 26, 715–723.CrossRefGoogle ScholarPubMed
McKanna, J.A. & Casagrande, V.A. (1981). Atropine affects lid-suture myopia development: Experimental studies of chronic atropinization in tree shrews. Documental Ophthalmology Proceeding Series 28, 187–192.CrossRefGoogle Scholar
Norton, T.T. (1990). Experimental myopia in tree shrews. In Myopia and the Control of Eye Growth, ed. Bock, G.R. & Widdows, K., pp. 178–199. Chichester, England: John Wiley and Sons.Google Scholar
Oishi, T. & Lauber, J.K. (1988). Chicks blinded with formoguanamine do not develop lid suture myopia. Current Eye Research 7, 69–73.CrossRefGoogle Scholar
Raviola, E. & Wiesel, T.N. (1990). Neural control of eye growth and experimental myopia in primates. In Myopia and the Control of Eye Growth, ed. Bock, G.R. & Widdows, K., pp. 22–44. Chichester, England: John Wiley and Sons.Google ScholarPubMed
Reiner, A., Erichsen, J.T., Cabot, J.B., Evinger, C, Fitzgerald, M.E.C. & Karten, H.J. (1991 a). Neurotransmitter organization of the nucleus of Edinger-Westphal and its projection to the avian ciliary ganglion. Visual Neuroscience 6, 451–472.CrossRefGoogle Scholar
Reiner, A., Fitzgerald, M.E.C. & Hodos, W. (1991 b). Reductions in choroidal blood flow occur in chicks wearing occluders that induce eye growth toward myopia. Investigative Ophthalmology and Visual Science (Suppl.) 32, 2614.Google Scholar
Reiner, A., Fitzgerald, M.E.C. & Gamlin, P.D.R. (1990). Central neural circuits controlling choroidal blood flow: A Laser-Doppler Study. Investigative Ophthalmology and Visual Science (Suppl.) 31, 38.Google Scholar
Reiner, A., Karten, H.J., Gamlin, P.D.R. & Erichsen, J.T. (1983). Parasympathetic ocular control: Functional subdivisions and circuitry of the avian nucleus of Edinger-Westphal. Trends in Neuroscience 6, 140–145.CrossRefGoogle Scholar
Schaeffel, F., Glasser, A. & Howland, H.C. (1988). Accommodation, refractive error, and eye growth in chickens. Vision Research 28, 639–657.CrossRefGoogle ScholarPubMed
Schaeffel, F., Howland, H.C. & Farkas, L. (1986). Natural accommodation in the growing chicken. Vision Research 26, 1977–1993.CrossRefGoogle ScholarPubMed
Shih, Y.-F., Fitzgerald, M.E.C, Norton, T.T., Gamlin, P.D.R., Hodos, W. & Reiner, A. (1993 a). Reductions in choroidal blood flow occur in chicks wearing goggles that induce eye growth toward myopia. Current Eye Research 12, 219–227.CrossRefGoogle ScholarPubMed
Shih, Y.F., Fitzgerald, M.E.C. & Reiner, A. (1993 b). Choroidal blood flow is reduced in chicks with ocular enlargement induced by corneal incisions. Current Eye Research 12, 229–237.CrossRefGoogle ScholarPubMed
Shih, Y.-F., Fitzgerald, M.E.C. & Reiner, A. (1993 c). Identification of retinal layers controlling ocular growth in chicks. Investigative Ophthalmology and Visual Science (Suppl.) 34, 1209.Google Scholar
Shih, Y.F., Horng, I.H., Yang, C.H., Lin, L.L.K., Peng, Y. & Hung, P.T. (1991 a). Ocular pulse amplitude in myopia. Journal of Ocular Pharmacology 7, 83–87.CrossRefGoogle ScholarPubMed
Stjernschantz, J., Alm, A. & Bill, A. (1976). Effects of intracranial oculomotor nerve stimulation on ocular blood flow in rabbits: Modification by indomethacin. Experimental Eye Research 23, 461–469.CrossRefGoogle ScholarPubMed
Stjernschantz, J. & Bill, A. (1979). Effect of intracranial stimulation of the oculomotor nerve on ocular blood flow in the monkey, cat, and rabbit. Investigative Ophthalmology and Visual Science 18, 99–103.Google Scholar
To'mey, K.F., Faris, B.M., Jalkh, A.E. & Nasr, A.M. (1981). Ocular pulse in high myopia. Annual of Ophthalmology 13, 569–571.Google ScholarPubMed
Troilo, D. (1990). Experimental studies of emmetropization in the chick. In Myopia and the Control of Eye Growth, ed. Bock, G.R. & Widdows, K., pp. 89–114. Chichester, England: John Wiley and Sons.Google Scholar
van Alphen, G.W.H.M. (1990). Emmetropization in the primate eye. In Myopia and the Control of Eye Growth, ed. Bock, G.R. & Widdows, K., pp. 115–125. Chichester, England: John Wiley and Sons.Google Scholar
Wallman, J., Gottlieb, M.D., Rajaram, V. & Fugate-Wentzek, L.A. (1987). Local retinal regions control local eye growth and myopia. Science 237, 73–77.CrossRefGoogle ScholarPubMed
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, 311–319.Google ScholarPubMed
Yancey, C.M. & Linsenmeier, R.A. (1988). The electroretinogram and choroidal PO2 in the cat during elevated intraocular pressure. Investigative Ophthalmology and Visual Science 29, 700–707.Google ScholarPubMed