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Central neural circuits for the light-mediated reflexive control of choroidal blood flow in the pigeon eye: A laser Doppler study

Published online by Cambridge University Press:  02 June 2009

Malinda E. C. Fitzgerald
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee-Memphis, Memphis Department of Biology, Christian Brothers University, Memphis
Paul D. R. Gamlin
Affiliation:
Department of Physiological Optics, University of Alabama at Birmingham, Birmingham
Yuri Zagvazdin
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee-Memphis, Memphis
Anton Reiner
Affiliation:
Department of Anatomy and Neurobiology, University of Tennessee-Memphis, Memphis

Abstract

Electrical stimulation in pigeons of the input from the medial subdivision of the nucleus of Edinger-Westphal (EWM) to the choroidal neurons of the ipsilateral ciliary ganglion, which themselves have input to the choroidal blood vessels of the ipsilateral eye, increases choroidal blood flow (ChBF). Since the EWM receives input from the contralateral suprachiasmatic nucleus (SCN), which in turn receives contralateral retinal input, the present study sought to determine if activation of the SCN by microstimulation or by retinal illumination of the contralateral eye would also yield increases in ChBF in that same eye. Using laser Doppler flowmetry (LDF) to measure ChBF, we found that electrical activation of the contralateral SCN by 100-Hz anodal pulse trains yielded increases in ChBF that were stimulus related and proportional to the stimulating current. These increases in ChBF elicited by the SCN stimulation were accompanied by increases in choroidal volume (vasodilation), but not by increases in systemic blood pressure. Furthermore, the increases could be blocked reversibly by lidocaine injection into the EWM. These results suggest that the increases in ChBF in the eye contralateral to the SCN stimulation were specifically mediated by the SCN-EWM pathway. Retinal illumination with a fiber optic light source was also found to increase ChBF in the illuminated eye, and these effects too could be blocked reversibly with lidocaine injection into the EWM or permanently by the EWM lesion. Control studies confirmed that the light-elicited increases were mediated by increases in choroidal volume (i.e. vasodilation), were not accompanied by systemic blood pressure increases, and were not artifactually generated by transocular illumination of the LDF probe. Thus, the SCN-EWM circuit may be involved in regulating ChBF in response to the level of retinal illumination and/or the visual patterns falling on the retina.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

Albertson, T.E., Walby, W.F. & Joy, R.M. (1992). Modification of GABA-mediated inhibition by various injectable anesthetics. Anesthesiology 77, 488499.CrossRefGoogle ScholarPubMed
Bill, A. (1984). The circulation in the eye. In The Microcirculation. Part 2, Handbook of Physiology, Section 2, ed. Renkin, E.M. & Michel, C.C., pp. 10011035. Baltimore, Maryland: The American Physiological Society.Google Scholar
Bill, A. (1985). Some aspects of the ocular circulation. Investigative Ophthalmology and Visual Science 26, 410424.Google ScholarPubMed
Bill, A. & Nilsson, S. (1985). Control of ocular blood flow. Journal of Cardiovascular Pharmacology 7, S96–S102.Google Scholar
Bill, A. & Sperber, G. (1990). Control of retinal and choroidal blood flow. Eye 4, 319325.Google Scholar
Bill, A., Sperber, G. & Ujiie, K. (1983). Physiology of the choroidal vascular bed. Experimental Eye Research 6, 101107.Google ScholarPubMed
Bill, A., Stjernschantz, J. & Alm, A. (1976). Effects of hexamethonium, biperiden and phentolamine on the vasoconstrictive effects of oculomotor nerve stimulation in rabbits. Experimental Eye Research 23, 615622.CrossRefGoogle ScholarPubMed
Bingelli, R.L. & Paule, W.J. (1969). The pigeon retina: Quantitative aspects of the optic nerve and ganglion cell layer. Journal of Comparative Neurology 137, 118.CrossRefGoogle Scholar
Bloch, S. & Martinoya, C. (1983). Specialization of visual functions for different retinal areas in the pigeon. In Advances in Vertebrate Neuroethology, ed. Ewert, J.-P., Capranica, R.R. & Ingle, D.J., pp. 359368. New York: Plenum Publishing Corp.Google Scholar
Bok, D. (1985). Retinal photoreceptor-pigment epithelium interactions. Investigative Ophthalmology and Visual Science 26, 16591694.Google Scholar
Bonner, R.F. & Nossal, R. (1990). Principles of Laser-Doppler flowmetry. In Laser-Doppler Blood Flowmetry, ed. Shepherd, A.P. & Öberg, P., pp. 1745. Norwell, Massachusetts: Kluwer Academic Publishers.Google Scholar
Borgos, J.A. (1990). TSl's LDV blood flowmeter. In Laser-Doppler Blood Flowmetry, ed. Shepherd, A.P. & Öberg, P., pp. 7392. Norwell, Massachusetts: Kluwer Academic Publishers.CrossRefGoogle Scholar
Buttery, R.G., Haight, J.R. & Bell, K. (1990). Vascular and avascular retinae in mammals. Brain, Behavior, and Evolution 35, 156175.Google Scholar
Cassone, V.M. (1990). Effects of melatonin on vertebrate circadian systems. Trends in Neuroscience 13, 457464.Google Scholar
Cuthbertson, S.L., Fitzgerald, M.E.C., Shih, Y.F., Toledo, C.B., Jackson, B. & Reiner, A. (1995). Innervation of orbital and choroidal blood vessels by the pterygopalatine ganglion in birds. Investigative Ophthalmology and Visual Science (Suppl.) 36, S121.Google Scholar
Cuthbertson, S., Fitzgerald, M.E.C., Shih, Y.F., White, J. & Reiner, A. (1996). Distribution of ciliary ganglion nerve fibers in the avian choroid. Vision Research 36, 775786.CrossRefGoogle Scholar
Durieux, M.E. (1995). Inhibition by ketamine of muscarinic acetylcholine receptor function. Anesthesia and Analgesia 81, 5762.Google ScholarPubMed
Ehinger, B. (1966). Cholinesterases in ocular and orbital tissues of some mammals. Acta Universitatis Lundensis Sectio II 2, 115.Google Scholar
Feke, G.T., Zuckerman, R., Green, G.G. & Weiter, J.J. (1983). Response of human retinal blood flow to light and dark. Investigative Ophthalmology and Visual Science 24, 136141.Google ScholarPubMed
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. (1993). NADPH-diaphorase positive neurons and fibers in the ciliary ganglion and choroid of the pigeon. Society for Neuroscience Abstracts 19, 1202.Google Scholar
Fitzgerald, M.E.C., Vana, B.A. & Reiner, A. (1990 b). 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, 583598.Google Scholar
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, 24832492.Google Scholar
Galifret, Y. (1968). Les diverses arires fonctionelles do la retine du pigeon. Zeitschrift für Zellforschung und Mikroskopische Anatomie 86, 535545.Google Scholar
Gamlin, P.D.R., Reiner, A. & Karten, H.J. (1982). Substance P-containing neurons of the avian suprachiasmatic nucleus project directly to the nucleus of Edinger-Westphal. Proceedings of the National Academy of Sciences of the U.S.A. 79, 38913895.CrossRefGoogle Scholar
Gherezghiher, T., Okubo, H. & Koss, M.C. (1991). Choroidal and ciliary body blood flow analysis: Application of laser Doppler flow-metry in experimental animals. Experimental Eye Research 53, 151156.CrossRefGoogle Scholar
Guglielmone, R. & Cantino, D. (1982). Autonomic innervation of the ocular choroid membrane in the chicken. A fluorescence-histochemical and electron-microscopic study. Cell and Tissue Research 222, 417431.CrossRefGoogle Scholar
Haumschild, D.J. (1986). Microvascular blood flow measurement by laser-Doppler flowmetry. TSI Application Note, St. Paul, MN.Google Scholar
Heal, D.J., Prow, M.R., Butler, S.A. & Buckett, W.R. (1995). Mediation of mydriasis in conscious rats by central postsynaptic α2-adrenoceptors. Pharmacology, Biochemistry, and Behavior 50, 219224.Google Scholar
Henkind, P., Leitman, M. & Weitzman, E. (1973). The diurnal curve in man: New observations. Investigative Ophthalmology and Visual Science 12, 703707.Google ScholarPubMed
Hodos, W., Fitzgerald, M.E.C. & Reiner, A. (1991). Visual acuity losses in pigeons with central lesions that disrupt adaptive regulation of choroidal blood flow. Investigative Ophthalmology and Visual Science (Suppl.) 32, 534.Google Scholar
Kanmura, Y., Kajikuri, J., Itoh, T. & Yoshitake, J. (1993). Effects of ketamine on contraction and synthesis of inositol 1,4,5-trisphosphate in smooth muscle of the rabbit mesenteric artery. Anesthesiology 79, 571579.CrossRefGoogle ScholarPubMed
Karten, H.J. & Hodos, W. (1967). A Stereotaxic Atlas of the Brain of the Pigeon (Columba livia). Baltimore, Maryland: The Johns Hopkins Press.Google Scholar
Kiel, J.W. & Shepherd, A.P. (1992). Autoregulation of choroidal blood flow in the rabbit. Investigative Ophthalmology and Visual Science 33, 23992410.Google ScholarPubMed
Lindsberg, P.J., O'Neill, J.T., Paakkari, I., Hallenbeck, J. & Feuerstein, G. (1989). Validation of laser-Doppler flowmetry in measurement of spinal cord blood flow. American Journal of Physiology 257, 674680.Google Scholar
Macdonald, R.L. & Cohen, D.H. (1973). Heart rateand blood pressure responses to electrical stimulation of the central nervous system in the pigeon (Columba livia). Journal of Comparative Neurology 150, 109136.CrossRefGoogle Scholar
Marshall, J., Mellerio, J. & Palmer, D.A. (1972). Damage to pigeon retinae by moderate illumination from fluorescent lamps. Experimental Eye Research 14, 164169.CrossRefGoogle ScholarPubMed
Meijer, J.H. & Rietveld, W.J. (1989). Neurophysiology of the suprachiasmatic circadian pacemaker in rodents. Physiological Reviews 69, 671707.CrossRefGoogle ScholarPubMed
Meriney, S.D. & Pilar, G.J. (1987). Cholinergic innervation of the smooth muscle cells in the choroid coat of the chick eye and its development. Journal of Neuroscience 7, 38273839.Google Scholar
Meyer, D.B. (1977). The avian eye and its adaptations. In Handbook of Sensory Physiology, ed. Crescitelli, F., pp. 549611. Berlin: Springer Verlag.Google Scholar
Nakanome, Y., Karita, K., Izumi, H. & Tamai, M. (1995). Two types of vasodilation in cat choroid elicited by electrical stimulation of the short ciliary nerve. Experimental Eye Research 60, 3742.CrossRefGoogle ScholarPubMed
Nilsson, S.F.E. (1994). Nitric oxide as a mediator of parasympathetic vasodilation in the uvea. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1288.Google Scholar
Nilsson, S.F.E., Linder, J. & Bill, A. (1985). Characteristics of uveal vasodilation produced by facial nerve stimulation in monkeys, cats and rabbits. Experimental Eye Research 40, 841852.Google Scholar
Ogawa, A., Uemura, M., Kataoka, Y., Oi, K. & Inokuchi, T. (1993). Effects of ketamine on cardiovascular responses mediated by N-methyl-D-aspartate receptor in the rat nucleus tractus solitarius. Anesthesiology 78, 163167.CrossRefGoogle ScholarPubMed
Parver, L., Auker, C. & Carpenter, D. (1983). Choroidal blood flow. III. Reflexive control in human eyes. Archives of Ophthalmology 101, 16041606.CrossRefGoogle ScholarPubMed
Parver, L., Auker, C., Carpenter, D. & Doyle, T. (1982). Choroidal blood flow. II. Reflexive control in the monkey. Archives of Ophthalmology 100, 13271330.CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Wallman, J. & Wildsoet, C.F. (1990). Saccadic oscillations facilitate ocular perfusion from the avian pecten. Nature 343, 362363.Google Scholar
Pilar, G., Nuñez, R., McLennan, l.S. & Meriney, S.D. (1987). Muscarinic and nicotinic synaptic activation of the developing chicken iris. Journal of Neuroscience 7, 38133826.CrossRefGoogle ScholarPubMed
Pilar, G. & Vaughan, P. (1969). Electrophysiological investigations of the pigeon iris neuromuscular junctions. Comparative Biochemistry and Physiology 29, 5172.CrossRefGoogle ScholarPubMed
Reiner, A., Erichsen, J.T., Cabot, J.B., Evinger, C., Fitzgerald, M.E.C. & Karten, H.J. (1991). Neurotransmitter organization of the nucleus of Edinger-Westphal and its projection to the avian ciliary ganglion. Visual Neuroscience 6, 451472.Google Scholar
Reiner, A., Karten, H.J., Gamlin, P.D.R. & Erichsen, J.T. (1983). Functional subdivisions and circuitry of the avian nucleus of Edinger-Westphal. Trends in Neuroscience 6, 140145.CrossRefGoogle Scholar
Riva, C.E. & Feke, G.T. (1981). Laser Doppler velocimetry in the measurement of retinal blood flow. In The Biomedical Laser: Technology and Clinical Applications, ed. Goldman, L., pp. 135161. New York: Springer Verlag.Google Scholar
Riva, C.E., Grunwald, J. & Petrig, B. (1983). Reactivity of the human retinal circulation to darkness: A laser Doppler velocimetry study. Investigative Ophthalmology and Visual Science 24, 737740.Google ScholarPubMed
Riva, C.E., Cranstoun, S.D., Mann, R.M. & Barnes, G.E. (1994). Local choroidal blood flow in the cat by laser Doppler flowmetry. Investigative Ophthalmology and Visual Science 35, 608618.Google Scholar
Ruskell, G.L. (1971). Facial parasympathetic innervation of the choroidal blood-vessels in monkeys. Experimental Eye Research 12, 166172.Google Scholar
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, 219227.Google Scholar
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, 229237.CrossRefGoogle ScholarPubMed
Shih, Y.-F., Fitzgerald, M.E.C. & Reiner, A. (1993 c). Effects of choroidal and ciliary nerve transection on choroidal blood flow, ocular health, and ocular enlargement. Visual Neuroscience 10, 969979.CrossRefGoogle ScholarPubMed
Shih, Y.F., Fitzgerald, M.E.C., Cuthbertson, S.L. & Reiner, A. (1994). Temperature-mediated control of choroidal blood flow by Substance P (SP)-containing trigeminal nerve afferents in chicks. Investigative Ophthalmology and Visual Science (Suppl.) 35, 1641.Google Scholar
Snodderly, D.M. & Weinhaus, R.S. (1990). Retinal vasculature of the fovea of the squirrel monkey, Saimiri sciureus: Three-dimensional architecture, visual screening and relationships to the neuronal layers. Journal of Comparative Neurology 297, 145163.CrossRefGoogle Scholar
Sokal, R.R. & Rohlf, F.J. (1981). Biometry: The Principles and Practice of Statistics in Biological Research, 2nd edition. New York: W.H. Freeman and Co.Google Scholar
Stiris, T.A., Hall, C., Christensen, T. & Bratlid, D. (1991). Effect of different phototherapy lights on retinal and choroidal blood flow. Developmental Pharmacology and Therapeutics 17, 7078.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, 461469.Google Scholar
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, 99103.Google Scholar
Stjernschantz, J. & Bill, A. (1980). Vasomotor effects of facial nerve stimulation: Non-cholinergic vasodilation in the eye. Acta Physiology Scandinavia 109, 4550.CrossRefGoogle Scholar
Strange, R., Wilson, T.M. & Mackenzie, E.T. (1977). Choroidal and cerebral blood flow determined with Kr85 in anesthetized animals. Investigative Ophthalmology and Visual Science 16, 571576.Google Scholar
Sun, W., Erichsen, J.T. & May, P.L. (1994). NADPH-diaphorase reactivity in ciliary ganglion neurons: A comparison of distributions in the pigeon, cat and monkey. Visual Neuroscience 11, 10271031.Google Scholar
Walls, G.L. (1942). The Vertebrate Eye and Its Adaptive Radiation. Bloomfield Hills, Michigan: Cranbrook Institute of Science.Google Scholar
Yamamoto, R., Bredt, D.S., Snyder, S.H. & Stone, R.A. (1993). The localization of nitric oxide synthase in the rat eye and related cranial ganglia. Neuroscience 54, 189200.Google Scholar
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, 700707.Google Scholar
Young, R.W. (1978). The daily rhythm of shedding and degradation of rods and cone outer segment membranes in the chick retina. Investigative Ophthalmology and Visual Science 17, 105116.Google ScholarPubMed
Zagvazdin, Y.S., Fitzgerald, M.E.C., Sancesario, G. & Reiner, A. (1996). Neural nitric oxide (NO) mediates Edinger-Westphal nucleus evoked vasodilation of choroidal blood vessels. Investigative Ophthalmology and Visual Science 37, 666672.Google Scholar