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Centrifugal innervation of the rat retina

Published online by Cambridge University Press:  02 June 2009

Michael Schütte
Michael Schütte
Affiliation:
Department of Ophthalmology, Mt. Sinai School of Medicine, New York
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Abstract

Centrifugal fibers innervating the retina have been shown in all classes of vertebrate, except for mammals where conventional tract-tracing methods have not been able to unmistakably demonstrate their existence. In a previous study, a unilateral, intravitreal injection of 5, 7-dihydroxytryptamine was used to reveal indoleamine-accumulating centrifugal fibers which were visualized by an immunoreaction against serotonin. In the present study, I employed a modification of this method to stain retinopetal neurons in the rat. Terminals were located preferentially in the outer retina; labeled fibers could be traced back along an ipsilateral pathway to somata in the dorso-caudal portions of the chiasm or the medio-lateral preoptic area, and thence towards the suprachiasmatic nuclei. The unique beaded appearance of the fibers distinguishes them from retinal ganglion cell axons. The labeling of central cell bodies strongly suggests that they possess terminals in the retina. Thus, at least some mammalian retinas receive centrifugal innervation. This indoleamine-accumulating retinopetal pathway may be involved in retinal melatonin synthesis, coordination of circadian rhythms, and interocular phenomena.

Keywords

Serotonin (5-hydroxytryptamine)5, 7-dihydroxytryptamineBinocular visionInterocular adaptationCircadian clock
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 6 , November 1995 , pp. 1083 - 1092
Copyright
Copyright © Cambridge University Press 1995

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References

Auerbach, E., Dörrenhaus, A. & Cavonius, C.R. (1992). Changes in sensitivity of the dark-adapted eye during concurrent light adaptation of the other eye. Visual Neuroscience 8, 359–363.CrossRefGoogle ScholarPubMed
Baumgarten, H.G. & Björklund, A. (1976). Neurotoxic indoleamines and monoamine neurons. Annual Review of Pharmacology and Toxicology 16, 101–107.CrossRefGoogle ScholarPubMed
Baumgarten, H.G., Klemm, H.P. & Schlossberger, H.G. (1984). In vivoimetabolism of 14C-5-HT, 14C-5,6-DHT, and 14C-5,7-DHT by MAO/COMT/Aldehyde dehydrogenase in rat brain. In Progress in Tryptophan and Serotonin Research, ed. Schlossberger, H.G., Kochen, W., Linzen, B. & Steihart, H., pp. 241–249.Berlin, New York: W. De Gruyter.Google Scholar
Björklund, A., Baumgarten, H.G. & Nobin, A. (1974). Chemical lesioning of central monoamine axons by means of 5,6-dihydro-xytryptamine and 5, 7-dihydroxytryptamine. Advances in Biochemical Psychopharmacology 10, 13–33.Google ScholarPubMed
Björklund, A. & Nobin, A. (1973). Fluorescence microspectrofluorometric mapping of dopamine and noradrenaline cell groups in the rat diencephalon. Brain Research 51, 193–205.CrossRefGoogle ScholarPubMed
Brunken, W.J., Jin, X.T. & Pis-Lopez, M. (1993). The properties of the serotonergic system in the retina. Progress in Retina Research 12, 75–99.CrossRefGoogle Scholar
Cajal, S.R.y (1889). Sur la morphologie et les connexions des éléments de la rétine des oiseaux. Anatomischer Anzeiger 4, 111–121.Google Scholar
Cajal, S.R.y (1892). La rétine des vertébrés. Cellule 9, 121–225.Google Scholar
Denny, N., Frumkes, T.E., Barris, M.C. & Eysteinsson, T. (1991). Tonic interocular suppression and binocular summation in human vision. Journal of Physiology 437, 449–460.CrossRefGoogle ScholarPubMed
Dogiel, A.S. (1895). Die Retina der Vögel. Archiv der microskopischen Anatomie und Entwicklungsmechanismen 44, 622–648.CrossRefGoogle Scholar
Dowling, J.E. (1965). Discussion of: Wolter J. (1965). The reaction of the centrifugal nerves of the human eye: After photocoagulation, occlusion of the central artery and bilateral enucleation. In The Structure of the Eye, ed. Rohen, J.H., pp. 96–97. Stuttgart: Schattauer.Google Scholar
Dowling, J.E. (1991). Retinal neuromodulation: The role of dopamine. Visual Neuroscience 7, 87–97.CrossRefGoogle ScholarPubMed
Dräger, U.C., Edwards, D.L. & Barnstable, C.J. (1984). Antibodies against filamentous components in discrete cell types of the mouse retina. Journal of Neuroscience 4, 2025–2042.CrossRefGoogle ScholarPubMed
Dubocovich, M.L. (1983). Melatonin is a potent modulator of dopamine release in the retina. Nature 306, 782–784.CrossRefGoogle ScholarPubMed
Ehinger, B. & Florén, I. (1976). Indoleamine-accumulating neurons in the retina of the rabbit, cat, and goldfish. Cell and Tissue Research 175, 37–48.CrossRefGoogle Scholar
Ellias, S.A. & Stevens, J.K. (1980). The dendritic varicosity: A mechanism for electrically isolating the dendrites of the cat retinal amacrine cells? Brain Research 196, 365–372.CrossRefGoogle ScholarPubMed
Florén, I. & Hansson, H. (1980). Investigations into whether 5-hy-droxytryptamine is a neurotransmitter in the retina of rabbit and chicken. Investigative Ophthalmology and Visual Science 19, 117–125.Google Scholar
Fuxe, K., Agnati, L.F., Kalia, M., Goldstein, M., Andersson, K. & Härfstrand, A. (1985). Dopaminergic systems in the brain and pituitary. In Basic and Clinical Aspects of Neuroscience: The Dopaminergic System, ed. Flückinger, E., Müller, E.E. & Thorner, M.O., pp. 11–25. Berlin, Heidelberg, New York, Tokyo: Springer-Sandoz.Google Scholar
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. Journal of Comparative Neurology 301, 433–442.CrossRefGoogle ScholarPubMed
Herrick, C.J. (1941). Development of the optic nerves of Amblystoma. Journal of Comparative Neurology 74, 473–534.CrossRefGoogle Scholar
Itaya, S.K. (1980). Retinal efferents from the pretectal area in the rat. Brain Research 201, 436–441.CrossRefGoogle ScholarPubMed
Itaya, S.K. & Itaya, P.W. (1985). Centrifugal fibers to the rat retina from the medial pretectal area and the periaqueductal grey matter. Brain Research 326, 362–365.CrossRefGoogle Scholar
Itaya, S.K., Williams, T.H. & Engel, E.L. (1978). Anterograde transport of HRP enhanced by poly 1-ornithine. Brain Research 150, 170–176.CrossRefGoogle Scholar
Knoche, H. (1958). Über die Ausbreitung und Herkunft der nervösen Nodulusfasern in Hypothalamus und Retina. Zeitschrift für Zell-forschung 48, 602–616.CrossRefGoogle ScholarPubMed
Krause, W. (1880). Ueber die Fasern des Sehnerven. Albrecht v. Graefes Archiv der Ophthalmologic 26, 102–110.CrossRefGoogle Scholar
Kuhnt, H. (1879). Zur Kenntnis des Sehnerven und der Netzhaut. Albrecht v. Graefes Archiv der Ophthalmologie 25, 179–288.CrossRefGoogle Scholar
Lange, G., Frumkes, T.E., Denny, N. & Schütte, M. (1993). Some suppressive rod-cone interactions involve central visual pathways. Proceedings of the Society for Neuroscience Abstracts 23, 1257.Google Scholar
Lansford, T.G. & Baker, H.D. (1969). Dark adaptation: An interocular light-adaptation effect. Science 164, 1307–1309.CrossRefGoogle ScholarPubMed
Larsen, J.N.B. & Møller, M. (1987). The presence of retinopetal fibres in the optic nerve of the mongolian gerbil (Meriones unguiculatus): A horseradish peroxidase in vitro study. Experimental Eye Research 45, 763–768.CrossRefGoogle ScholarPubMed
Makous, W., Teller, D. & Boothe, R. (1976). Binocular interaction in the dark. Vision Research 16, 473–476.CrossRefGoogle ScholarPubMed
Marc, R.E., Liu, W.-L.S., Scholz, K. & Muller, J.F. (1988). Serotonergic and serotonin-accumulating neurons in the goldfish retina. Journal of Neuroscience 8, 3427–3450.CrossRefGoogle ScholarPubMed
Marchiafava, P.L. (1976). Centrifugal action on amacrine and ganglion cells in the retina of the turtle. Journal of Physiology 255, 137–155.CrossRefGoogle ScholarPubMed
Massey, S.C., Mills, S.L. & Marc, R.E. (1992). All indoleamine-accumulating cells in the rabbit retina contain GABA. Journal of Comparative Neurology 322, 275–291.CrossRefGoogle ScholarPubMed
Matsumoto, Y., Ueda, S. & Kawata, M. (1992). Morphological characterization and distribution of indoleamine-accumulating cells in the rat retina. Acta Histochemica et Cytochemica 25, 45–51.CrossRefGoogle Scholar
Mitchell, C.K. & Redburn, D.A. (1985). Analysis of pre- and postsynaptic factors of the serotonin system in rabbit retina. Journal of Cell Biology 100, 64–73.CrossRefGoogle ScholarPubMed
Moore, R.Y. & Bloom, F.E. (1978). Central catecholamine systems: anatomy and physiology of the dopamine systems. Annual Review of Neuroscience 1, 129–169.CrossRefGoogle ScholarPubMed
Negishi, K., Kato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 108, 279–283.Google Scholar
Negishi, K. & Teranishi, T. (1990). Sequential course of uptake of intra-vitreal 5, 7-dihydroxytryptamine by carp retinal cells. Brain Research 508, 135–141.CrossRefGoogle Scholar
Negishi, K., Teranishi, T. & Kato, S. (1981). 5, 7-Dihydroxytryptamine destroys indoleamine accumulating cell bodies in carp retina. Acta Histochemica et Cytochemica 14, 654–660.CrossRefGoogle Scholar
Nguyen-Legros, J., Vigny, A. & Gay, M. (1983). Postnatal development of TH-like immunoreactivity in the rat retina. Experimental Eye Research 37, 23–32.CrossRefGoogle ScholarPubMed
Nguyen-Legros, J., Moussafi, F. & Simon, A. (1990). Sclerally directed processes of dopaminergic interplexiform cells reach the outer nuclear layer in rat and monkey retina. Visual Neuroscience 4, 547–553.CrossRefGoogle ScholarPubMed
Nishida, K., Ueda, S. & Sano, Y. (1985). Immunohistochemical studies of masked indoleamine cells in the area postrema of the rat. Histochemistry 82, 101–106.CrossRefGoogle ScholarPubMed
Novak, J.Z. (1988). Melatonin inhibits [3H]-dopamine release from the rabbit retina evoked by light, potassium and electrical stimulation. Medical Science Research 16, 1073–1075.Google Scholar
Osborne, N.N. (1984). Indoleamines in the eye with special reference to the serotonergic neurones of the retina. In Progress in Retinal Research, ed. Osborne, N.N. & Chader, G., pp. 61–103. Oxford: Pergamon Press.Google Scholar
Osborne, N.N. (1988). Retinal serotonin and the co-occurrence with other neurotransmitters. In Neuronal Serotonin, ed. Osborne, N.N. & Hamon, M., pp. 129–152. Chichester, New York, Brisbane, Toronto, Singapore: J. Wiley & Sons.Google Scholar
Perlia, R. (1889). Ueber ein neues Opticuscentrum beim Huhne. Albrecht v. Graefes Archiv der Ophthalmologie 35, 20–24.CrossRefGoogle Scholar
Ratto, G.M. & Usai, C. (1989). Modeling of electrical properties of varicose dendrites in retinal radiate amacrine cells. Proceedings of the Society for Neuroscience Abstracts 15, 923.Google Scholar
Redburn, D.A. & Mitchell, C.K. (1989). Darkness stimulates rapid synthesis and release of melatonin in rat retina. Visual Neuroscience 3, 391–403.CrossRefGoogle ScholarPubMed
Reese, B.E. & Geller, S.F. (1995). Precocious invasion of the optic stalk by transient retinopetal axons. Journal of Comparative Neurology 353, 572–584.CrossRefGoogle ScholarPubMed
Repérant, J. & Gallégo, A. (1976). Fibres centrifuges dans la rétine humaine. Archives d≈Anatomie Microscopique et de Morphologie Expérimentale 65, 103–120.Google Scholar
Ritchie, T.C. & Leonard, R.B. (1983). Immunocytochemical demonstration of serotonergic neurons and processes in the retina and optic nerve of the stingray Dasyatis sabina. Brain Research 267, 352–356.CrossRefGoogle ScholarPubMed
Rusoff, A.C. & Hapner, S.J. (1990). Development of retinopetal projections in the cichlid fish Herotilapia multispinosa. Journal of Comparative Neurology 294, 431–442.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1986). A system of indoleamine-accumulating neurons in the rabbit retina. Journal of Neuroscience 6, 3331–3347.CrossRefGoogle ScholarPubMed
Sandell, J.H. & Masland, R.H. (1989). Indoleamine-accumulation by retinal neurons exposed to blood. Histochemistry 92, 57–60.CrossRefGoogle ScholarPubMed
Sanders-Bush, E. (1988). 5-HT receptors: Transmembrane signalling mechanisms: In Neuronal Serotonin, ed. Osborne, N.N. & Hamon, M., pp. 449–464. Chichester, New York, Brisbane, Toronto, Singapore: J. Wiley & Sons.Google Scholar
Savy, C, Yelnik, J., Martin-Martinelli, E., Karpouzas, I. & Nguyen-Legros, J. (1989). Distribution and spatial geometry of dopamine interplexiform cells in the rat retina. 1. Developing retina. Journal of Comparative Neurology 289, 99–110.CrossRefGoogle ScholarPubMed
Schlemermeyer, E. & Chappell, R.L. (1991). Serotonin-like immuno-reactivity reveals centrifugal fibers and a distinct subclass of amacrine cell in the skate retina. Biological Bulletin 181, 327–328.CrossRefGoogle Scholar
Schütte, M. (1994). Serotonergic and serotonin-synthesizing cells in the Xenopus retina. International Journal of Neuroscience 78, 67–73.CrossRefGoogle ScholarPubMed
Schütte, M. & Hoskins, S.G. (1993). Ipsilaterally projecting retinal ganglion cells in Xenopus laevis: An HRP-study. Journal of Comparative Neurology 331, 482–494.CrossRefGoogle ScholarPubMed
Schütte, M. & Weiler, R. (1987). Morphometric analysis of serotoninergic bipolar cells in the retina and its implications for retinal image processing. Journal of Comparative Neurology 260, 619–626.CrossRefGoogle ScholarPubMed
Schütte, M. & Weiler, R. (1988). Mesencephalic innervation of the turtle retina by a single serotonin-containing neuron. Neuroscience Letters 91, 289–294.CrossRefGoogle ScholarPubMed
Schütte, M. & Witkovsky, P. (1990). Serotonin-like immunoreactivity in the retina of the clawed frog Xenopus laevis. Journal of Neurocytology 19, 504–518.CrossRefGoogle ScholarPubMed
Schütte, M. & Witkovsky, P. (1991). Dopaminergic interplexiform cells and centrifugal fibres in the Xenopus retina. Journal of Neurocytology 20, 195–207.CrossRefGoogle ScholarPubMed
Sretavan, D.W. (1990). Specific routing of retinal ganglion cell axons at the mammalian optic chiasm during embryonic development. Journal of Neuroscience 10, 1995–2007.CrossRefGoogle ScholarPubMed
Sretavan, D.W., Puré, E., Siegel, M.W. & Reichardt, L.F. (1995). Disruption of retinal axon ingrowth by ablation of embryonic mouse optic chiasm neurons. Science 269, 98–101.CrossRefGoogle ScholarPubMed
Stell, W.K., Walker, S.E., Chohan, K.S. & Ball, A.K. (1984). The goldfish nervus terminalis: A luteinizing hormone-releasing hormone and molluscan cardioexcitatory peptide immunoreactive olfactoretinal pathway. Proceedings of the National Academy of Sciences of the USA 81, 940–944.CrossRefGoogle ScholarPubMed
Takeuchi, Y. (1988). Distribution of serotonin neurons in the mammalian brain. In Neuronal Serotonin, ed. Osborne, N.N. & Hamon, M., pp. 25–56. Chichester, New York, Brisbane, Toronto, Singapore: J. Wiley & Sons.Google Scholar
Tauchi, M., Madigan, N.K. & Masland, R.H. (1990). Shapes and distributions of the catecholamine-accumulating neurons in the rabbit retina. Journal of Comparative Neurology 293, 178–189.CrossRefGoogle ScholarPubMed
Terman, J.S., Remé, C.E. & Terman, M. (1993). Rod outer segment disk shedding in rats with lesions of the suprachiasmatic nucleus. Brain Research 605, 256–264.CrossRefGoogle ScholarPubMed
Thomas, K.B., Tigges, M. & Iuvone, P.M. (1993). Melatonin synthesis and circadian tryptophan hydroxylase activity in chicken retina following destruction of serotonin immunoreactive amacrine and bipolar cells by kainic acid. Brain Research 601, 303–308.CrossRefGoogle ScholarPubMed
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.CrossRefGoogle Scholar
Uchiyama, H., Reh, T.A. & Stell, W.K. (1988). Immunocytochemical and morphological evidence for a retinopetal projection in anuran amphibians. Journal of Comparative Neurology 274, 48–59.CrossRefGoogle ScholarPubMed
Umino, O. & Dowling, J.E. (1991). Dopamine release from interplexiform cells in the retina: Effects of GnRH, FMRFamide, bicuculline, and enkephalin on horizontal cell activity. Journal of Neuroscience 11, 3034–3046.CrossRefGoogle ScholarPubMed
Vaney, D.I. (1896). Morphological identification of serotonin-accumulating amacrine cells in the living retina. Science 233, 444–446.CrossRefGoogle Scholar
Versaux-Botteri, C., Nguyen-Legros, J., Vigny, A. & Raoux, N. (1984). Morphology, density, and distribution of tyrosine hydroxylase-like immunoreactive cells in the retina of mice. Brain Research 301, 192–197.CrossRefGoogle ScholarPubMed
Villar, M.J., Vitale, M.L. & Parisi, M.N. (1987). Dorsal raphé serotonergic projection to the retina. A combined peroxidase tracing-neurochemical/high-performance liquid chromatography study in the rat. Neuroscience 22, 681–686.CrossRefGoogle Scholar
Voigt, T. & Wässle, H. (1987). Dopaminergic innervation of An amacrine cells in the mammalian retina. Journal of Neuroscience 7, 4115–4128.CrossRefGoogle Scholar
Wallenberg, A. (1898). Das mediale Opticusbundel der Taube. Neurologisches Zenlralblatt 17, 532–537.Google Scholar
Wässle, H., Voigt, T. & Patel, B. (1987). Morphological and immunocytochemical identification of indoleamine accumulating neurons in the cat retina. Journal of Neuroscience 7, 1574–1585.CrossRefGoogle ScholarPubMed
Weiler, R. & Schütte, M. (1985 a). Morphological and pharmacological analysis of putative serotonergic bipolar and amacrine cells in the retina of a turtle. Cell and Tissue Research 241, 373–382.CrossRefGoogle ScholarPubMed
Weiler, R. & Schütte, M. (1985 b). Kainic acid-induced release of serotonin from off-bipolar cells in the turtle retina. Brain Research 360, 379–383.CrossRefGoogle ScholarPubMed
Weiler, R. (1985). Mesencephalic pathway to the retina exhibits enkephalin-like immunoreactivity. Neuroscience Letters 55, 11–16.CrossRefGoogle Scholar
Witkovsky, P. & Schütte, M. (1991). The organization of dopaminergic neurons in vertebrate retinas. Visual Neuroscience 7, 113–124.CrossRefGoogle ScholarPubMed
Wolter, J.R. (1965). The reaction of the centrifugal nerves of the human eye: After photocoagulation, occlusion of the central artery and bilateral enucleation. In The Structure of the Eye, ed. Rohen, J.H., pp. 85–95. Stuttgart: Schattauer.Google Scholar
Wulle, I. & Schnitzer, J. (1989). Distribution and morphology of tyrosine hydroxylase-immunoreactive neurons in the developing mouse retina. Developmental Brain Research 48, 59–72.CrossRefGoogle ScholarPubMed
Zucker, C.L. & Dowling, J.E. (1987). Centrifugal fibers synapse on dopaminergic interplexiform cells in the teleost retina. Nature 330, 166–168.CrossRefGoogle ScholarPubMed