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The retinal targets of centrifugal neurons and the retinal neurons projecting to the accessory optic system

Published online by Cambridge University Press:  02 June 2009

Debora L. Nickla ,
Michael D. Gottlieb ,
Gonzalo Marin ,
Ximena Rojas ,
Luiz R. G. Britto  and
Josh Wallman
Debora L. Nickla
Affiliation:
Department of Biology, The City College of the City University of New York, New York
Michael D. Gottlieb
Affiliation:
Department of Biology, The City College of the City University of New York, New York
Gonzalo Marin
Affiliation:
Department of Biology, The City College of the City University of New York, New York
Ximena Rojas
Affiliation:
Department of Biology, The City College of the City University of New York, New York
Luiz R. G. Britto
Affiliation:
Department of Physiology and Biophysics, Institute of Biomedical Sciences, Saõ Paulo State University, 05508–900 Saõ Paulo, Brazil
Josh Wallman
Affiliation:
Department of Biology, The City College of the City University of New York, New York
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Abstract

In birds, neurons of the isthmo-optic nucleus (ION), as well as “ectopic” neurons, send axons to the retina, where they synapse on cells in the inner nuclear layer (INL). Previous work has shown that centrifugal axons can be divided into two anatomically distinct types depending on their mode of termination: either “convergent” or “divergent” (Ramon y Cajal, 1889; Maturana & Frenk, 1965). We show that cytochrome-oxidase histochemistry specifically labels “convergent” centrifugal axons and target neurons which appear to be amacrine cells, as well as three “types” of ganglion cells: two types found in the INL (displaced ganglion cells) and one in the ganglion cell layer. Labeled target amacrine cells have distinct darkly labeled “nests” of boutons enveloping the somas, are associated with labeled centrifugal fibers, and are confined to central retina. Lesions of the isthmo-optic tract abolish the cytochrome-oxidase labeling in the centrifugal axons and in the target amacrine cells but not in the ganglion cells. Cytochrome-oxidase-labeled ganglion cells in the INL are large; one type is oval and similar to the classical displaced ganglion cells of Dogiel, which have been reported to receive centrifugal input; the other type is rounder. Rhodamine beads injected into the accessory optic system results in retrograde label in both types of cells, showing that two distinct types of displaced ganglion cells project to the accessory optic system in chickens. The ganglion cells in the ganglion cell layer that label for cytochrome oxidase also project to the accessory optic system. These have proximal dendrites that ramify in the outer inner plexiform layer. Neither the target amacrine cells nor either of the displaced ganglion cells are immunoreactive for the inhibitory transmitter gamma aminobutyric acid. At least some of the target amacrine cells may, however, be cholinoceptive: we found that the antibody to the alpha-7 subunit of the nicotinic ACh receptor labels a population of cells in the INL that are similar in location, size, and the presence of labeled bouton-like structures to those we find labeled with cytochrome oxidase. This antibody also labels neurons in the ION proper but not ectopic cells. In conclusion, it appears that cytochrome oxidase may be a marker for “convergent” centrifugal axons and at least one of their target cells in the INL.

Keywords

Amacrine cellCentrifugal fibersChickCytochrome oxidaseDisplaced ganglion cellGABAIsthmo-optic nucleusNicotinic acetylcholine receptor
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 2 , March 1994 , pp. 401 - 409
Copyright
Copyright © Cambridge University Press 1994

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References

Britto, L.R.G., Keyser, K.T., Hamassaki, D.E. & Karten, H.J. (1988). Catecholaminergic subpopulation of retinal displaced ganglion cells projects to the accessory optic nucleus in the pigeon (Columba La). Journal of Comparative Neurology 269, 109–117.CrossRefGoogle Scholar
Britto, L.R.G., Keyser, K.T., Lindstrom, J.M. & Karten, H.J. (1992). Immunohistochemical localization of nicotinic acetylcholine receptor subunits in the mesencephalon and diencephalon of the chick. Journal of Comparative Neurology 317, 325–340.CrossRefGoogle ScholarPubMed
Cervetto, L., Marchiafava, P.L. & Pasina, E. (1976). Influence of efferent retinal fibres on responsiveness of ganglion cells to light. Nature 260, 56–57.CrossRefGoogle ScholarPubMed
Clarke, P.G.H. & Cowan, W.M. (1975). Ectopic neurons and aberrant connections during neural development. Proceedings of the National Academy of Sciences of the U.S.A. 72, 4455–4458.CrossRefGoogle ScholarPubMed
Cowan, W.M. (1970). Centrifugal fibers to the avian retina. British Medical Bulletin 26, 112–118.CrossRefGoogle Scholar
Crandall, J.E., Heaton, M.B. & Brownell, W.E. (1977). Tectal projection of displaced ganglion cells in avian retina. Investigative Ophthalmology and Visual Science 16, 774–776.Google ScholarPubMed
Crossland, W.J. & HuGhes, C.P. (1978). Observations on the afferent and efferent connections of the avian isthmo-optic nucleus. Brain Research 145, 239–256.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Cowan, W.M. (1966). An electron microscope study of normal and degenerating centrifugal fiber terminals in the pigeon retina. Zeitschrift für Zellforschung 71, 14–28.CrossRefGoogle ScholarPubMed
Fite, K.V., Brecha, N., Karten, H.J. & Hunt, S.P. (1981). Displaced ganglion cells and the accessory optic system of pigeon. Journal of Comparative Neurology 195, 279–288.CrossRefGoogle ScholarPubMed
Fritzsch, B., Clarke, P.G.H. & Crapon de Caprona, M.-D. (1989). Development of two types of centrifugal fibers in the chick retina: A study with Dil in fixed tissue. Society for Neuroscience Abstracts 15, 1389.Google Scholar
Gottlieb, M.D., Nickla, D.L. & Wallman, J. (1990). The centrifugal pathway in the chick retina appears to be specifically labeled by cytochrome oxidase histochemistry. Investigative Ophthalmology and Visual Science (Suppl.) 31, 211.Google Scholar
Hayes, B.P. & Holden, A.L. (1983 a). The distribution of displaced ganglion cells in the retina of the pigeon. Experimental Brain Research 49, 181–188.Google ScholarPubMed
Hayes, B.P. & Holden, A.L. (1983 b). The distribution of centrifugal terminals in the pigeon retina. Experimental Brain Research 49, 189–197.Google ScholarPubMed
Heaton, M.B., Alvarez, I.M. & Brownell, J.E. (1979). The displaced ganglion cells in the avian retina: Developmental and comparative considerations. Anatomy and Embryology 155, 161–178.CrossRefGoogle ScholarPubMed
Karten, H.J., Fite, K.V. & Brecha, N. (1977). Specific projection of displaced retinal ganglion cells upon the accessory optic system in pigeon (Columba livia). Proceedings of the National Academy of Sciences of the U.S.A. 74, 1753–1756.CrossRefGoogle Scholar
Keyser, K.T., Britto, L.R.G., Schoepfer, R., Whiting, P., Cooper, J., Conroy, W., Agnieszka, B.-P., Karten, H.J. & Lindstrom, J. (1993). Three subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick retina. Journal of Neuroscience 13, 442–454.CrossRefGoogle ScholarPubMed
Luo, X.G., Hevner, R.F. & Wong-Riley, M.T.T. (1989). Double labeling of cytochrome oxidase and gamma-aminobutyric acid in central nervous system neurons of adult cats. Journal of Neuroscience Methods 30, 189–195.CrossRefGoogle ScholarPubMed
Marchiafava, P.L. (1976). Centrifugal actions on amacrine and ganglion cells in the retina of the turtle. Journal of Physiology 255, 137–155.CrossRefGoogle ScholarPubMed
Marin, G., Letelier, J.C. & Wallman, J. (1990). Saccade-related responses of centrifugal neurons projecting to the chicken retina. Experimental Brain Research 82, 263–270.CrossRefGoogle Scholar
Maturana, H.R. & Frenk, S. (1965). Synaptic connections of the centrifugal fibers in the pigeon retina. Science 150, 359–362.CrossRefGoogle ScholarPubMed
McGill, J.I., Powell, T.P.S. & Cowan, W.M. (1966 a). The retinal representation upon the optic tectum and the isthmo-optic nucleus in the pigeon. Journal of Anatomy 100, 5–33.Google ScholarPubMed
McGill, J.I., Powell, T.P.S. & Co'wan, W.M. (1966 b). The organization of the projection of the centrifugal fibers to the retina in the pigeon. Journal of Anatomy 100, 35–49.Google Scholar
Miles, F. (1972 a). Centrifugal control of the avian retina. I. Receptive-field properties of retinal ganglion cells. Brain Research 48, 65–92.CrossRefGoogle ScholarPubMed
Miles, F. (1972 b). Centrifugal control of the avian retina. III. Effects of electrical stimulation of the isthmo-optic tract on the receptive-field properties of retinal ganglion cells. Brain Research 48, 115–128.CrossRefGoogle Scholar
Mjaatvedt, A.E. & Wong-Rhey, M.T.T. (1988). Relationship between synaptogenesis and cytochrome oxidase activity in Purkinje cells of the developing rat cerebellum. Journal of Comparative Neurology 277, 155–182.CrossRefGoogle ScholarPubMed
Nickla, D.L., Gottlieb, M.D., Marin, G., Rojas, X. & Wallman, J. (1990). Cytochrome oxidase histochemistry labels displaced ganglion cells that project to the accessory optic system (AOS) in the chick. Society of Neuroscience Abstracts 16, 347.Google Scholar
Prada, F.A., Chmelewski, C.E., Dorado, M.E., Prada, C. & Genis-Galvez, J.M. (1989). Displaced ganglion cells in the chick retina. Neuroscience Research 6, 329–339.CrossRefGoogle ScholarPubMed
Pearlman, A.L. & Hughes, C.P. (1976 a). Functional role of efferents to the avian retina. I. Analysis of retinal ganglion cell receptive fields. Journal of Comparative Neurology 166, 111–122.CrossRefGoogle Scholar
Pearlman, A.L. & Hughes, C.P. (1976 b). Functional role of efferents to the avian retina. II. Effects of reversible cooling of the isthmo-optic nucleus. Journal of Comparative Neurology 166, 123–132.CrossRefGoogle Scholar
Ramony, Cajal S. (1889). Sur la morphologie et les connexions des elements de la retine des oiseaux. In The Structure of the Rettna, ed. Thorpe, S.A. & Glickstein, M., pp. 83–92. Springfield: Charles C. Thomas Publisher. 1972.Google Scholar
Reiner, A. (1981). A projection of displaced ganglion cells to the accessory optic nuclei in the turtle. Brain Research 204, 403–409.CrossRefGoogle Scholar
Reiner, A., Brecha, N. & Karten, H.J. (1979). A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken. Neuroscience 4, 1679–1688.CrossRefGoogle Scholar
Sparks, D.L. & Hartwich-Young, R. (1989). The deep layers of the superior colliculus. In Reviews of Oculomotor Research, Volume 3: The Neurobiology of Saccadic Eye Movements, ed., Wurtz, R.H. & Goldberg, M.E., pp. 213–218. New York: Elsevier.Google Scholar
Uchiyama, H. (1989). Centrifugal pathways to the retina: Influence of the optic tectum. Visual Neuroscience 3, 183–206.CrossRefGoogle Scholar
Wolf-Oberhollenzer, F. (1987). A study of the centrifugal projections to the pigeon retina using two fluorescent markers. Neuroscience Letters 73, 16–20.CrossRefGoogle Scholar
Wong-Riley, M.T.T. (1979). Changes in the visual system of monocu-larly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed
Wong-Riley, M.T.T. (1989). Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends in Neuroscience 12, 94–101.CrossRefGoogle ScholarPubMed