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Dendritic distribution of two populations of ganglion cells and the retinopetal fibers in the retina of the silver lamprey (Ichthyomyzon unicuspis)

Published online by Cambridge University Press:  02 June 2009

Bernd Fritzsch  and
Shaun P. Collin
Bernd Fritzsch
Affiliation:
Department of Neurosciences A-001, Scripps Institution of Oceanography, University of Californiaat San Diego, La Jolla
Shaun P. Collin
Affiliation:
Department of Neurosciences A-001, Scripps Institution of Oceanography, University of Californiaat San Diego, La Jolla
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Abstract

The distribution of ganglion cells in the retina of the silver lamprey, Ichthyomyzon unicuspis, was revealed by retrograde labeling from the optic nerve with horseradish peroxidase (HRP) and fluorescent-labeled dextrans in live animals and with the fluorescent dye DiI in aldehyde-fixed tissue. The majority of ganglion cells (74%) termed the “outer ganglion cells,” are multipolar and are located at the vitread boundary of the inner nuclear layer. The remaining ganglion cells (26%), termed the “inner ganglion cells” are bipolar and are distributed in a sublamina within the inner plexiform layer. The dense, dendritic meshwork of the outer ganglion cells is largely restricted to the sclerad half of the inner plexiform layer with some cells possessing dendrites which pass through the inner nuclear layer to terminate within the outer plexiform layer. The dendrites of the inner ganglion cells form a thin, dendritic network apposing the inner limiting membrane. Axons from both populations of ganglion cells originate from dendrites or the soma and form fascicles lying adjacent to the outer ganglion cell somata.

Retinopetal fibers, originating from bilaterally distributed neurons of the tegmental midbrain, were thin and varicose and ran parallel to the ganglion cell axons to terminate either with a varicose enlargement or a few short sidebranches in the sclerad third of the inner plexiform layer. The unusual organization of the lamprey retina and outgroup comparison with hagfish suggests that agnathans share a presumably primitive type of retinal ganglion cell organization compared to that of gnathostomes.

Keywords

LampreyRetinaGanglion cellRetinopetal fibersRetinal topography
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 6 , June 1990 , pp. 533 - 545
Copyright
Copyright © Cambridge University Press 1990

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References

Buhl, E.H. & Peichl, L. (1986). Morphology of rabbit retinal ganglion cells projecting to the medial terminal nucleus of the accessory optic system. Journal of Comparative Neurology 253, 163–174.Google Scholar
Buhl, E.H. & Dann, J.F. (1988). Morphological diversity of displaced retinal ganglion cells in the rat: a lucifer yellow study. Journal of Comparative Neurology 269, 210–218.CrossRefGoogle Scholar
Cajal, R.S. (1893). La rétine des vertébrés. Translation by Maguire, D. & Rodieck, R.W. In The Vertebrate Retina, ed. Rodieck, R.W. (1973), pp. 774–904. San Francisco: Freeman.Google Scholar
Collin, S.P. (1988). The retina of the shovel-nosed ray, Rhinobatos batillum (Rhinobatidae): morphology and quantitative analysis of the ganglion, amacrine, and bipolar cell populations. Experimental Biology 47, 195–207.Google ScholarPubMed
Collin, S.P. (1989). Topography and morphology of retinal ganglion cells in the coral trout, Plectropoma leopardus (Serranidae): a retrograde cobaltous-lysine study. Journal of Comparative Neurology 281, 143–158.Google Scholar
Collin, S.P., Fritzsch, B. & Northcutt, R.G. (1990). Topographic distribution and dendritic morphology of subclasses of retinal ganglion cells in the silver lamprey, ichthyomyzon unicuspis. (in preparation).Google Scholar
Collin, S.P. & Pettigrew, J.D. (1988 a). Retinal ganglion cell topography in teleosts: a comparison between Nissl-stained material and retrograde labeling from the optic nerve. Journal of Comparative Neurology 276, 412–422.CrossRefGoogle ScholarPubMed
Collin, S.P. & Pettigrew, J.D. (1988 b). Retinal topography in reef teleosts, I: Some species with well-developed areae but poorly developed streaks. Brain Behavior and Evolution 31, 269–282.Google Scholar
Crapon, De Caprona M.-D. & Fritzsch, B. (1983). The development of the retinopetal nucleus olfactoretinalis of two cichlid fish as revealed by horseradish peroxidase. Developmental Brain Research 11, 282–301.Google Scholar
Dacey, D.M. (1985). Wide-spreading terminal axons in the inner plexiform layer of the cat's retina: evidence for intrinsic axon collaterals of ganglion cells. Journal of Comparative Neurology 242, 247–262.CrossRefGoogle ScholarPubMed
Dann, J.F. & Buhl, E.H. (1987). Retinal ganglion cells projecting to the accessory optic system in the rat. Journal of Comparative Neurology 262, 141–158.Google Scholar
Dann, J.F., Buhl, E.H. & Peichl, L. (1988). Postnatal dendritic maturation of alpha and beta ganglion cells in cat retina. Journal of Neuroscience 8, 1485–1499.CrossRefGoogle ScholarPubMed
Dogiel, A.S. (1895). Die Retina der Vögel. Archiv für Mikroskopie und Anatomie 44, 622–648.CrossRefGoogle Scholar
Dowling, J.E. (1987). The Retina. An Approachable Part of the Brain. London: The Belknap Press of Harvard University Press.Google Scholar
Dreher, B. & Robinson, S.R. (1988). Development of the retinofugal pathway in birds and mammals: evidence for a common “timetable.” Brain Behavior and Evolution 31, 369–390.CrossRefGoogle ScholarPubMed
Dunlop, S.A., Humphrey, M.F. & Beazley, L.D. (1989). Survival of displaced ganglion cells after optic nerve regeneration in the frog (Hyla moorei). Neuroscience Abstracts 15, 872.Google Scholar
Fite, K.V. (1985). Pretectal and accessory-optic visual nuclei of fish, amphibia, and reptiles: theme and variations. Brain Behavior and Evolution 26, 71–90.Google Scholar
Franz, V. (1932). Auge und Akkomodation von Petromyzon (Lampetra) fluviatilis L. Zoologische Jahrbücher 52, 118–178.Google Scholar
Fritzsch, B., Sonntag, R., Dubuc, R., Ohta, Y. & Grillner, S. (1990 a). Organization of the six motor nuclei innervating the ocular muscles in lamprey. Journal of Comparative Neurology 294, 491–506.Google Scholar
Fritzsch, B., Crapon, De Caprona M.-D. & Clarke, P.G.H. (1990 b). The development of two fiber types projecting to the retina of chicken as revealed with Dil. Journal of Comparative Neurology (submitted).Google Scholar
Fritzsch, B. & Wilm, C. (1990). Dextran amines in neuronal tracing. Trends in Neuroscience 13, 14.CrossRefGoogle ScholarPubMed
Glover, J.C., Petursdottir, G. & Jansen, J.K.S. (1986). Fluorescent dextran-amines used as axonal tracers in the nervous system of the chicken embryo. Journal of Neuroscience Methods 18, 243–254.Google Scholar
Godement, P., Vanselow, J., Thanos, S. & Bonhoeffer, F. (1987). A study in developing visual systems with a new method of staining neurones and their processes in fixed tissue. Development 101, 687–713.Google Scholar
Holmberg, K. (1977). The cyclostome retina. In Handbook of Sensory Physiology: The Visual System in Vertebrates. Vol VII/5, ed., Mackay, D.M. & Teuber, H.L., pp. 47–66. New York: Springer-Verlag.Google Scholar
Holmberg, K. (1978). Light- and electron-microscopic investigation of the optic nerve fiber layer in the river lamprey (Lampetra fluviatilis). Vision Research 18, 1313–1320.CrossRefGoogle ScholarPubMed
Hughes, A. (1975). A qualitative analysis of the cat retinal ganglion cell topography. Journal of Comparative Neurology 163, 107–128.Google Scholar
Hughes, A. (1985). New perspectives in retinal organization. In Progress in Retinal Research, ed. Osborne, N.N. & Chader, G., pp. 243–313. New York: Pergamon Press.Google Scholar
Karten, H.J., Fite, K.V. & Brecha, N. (1977). Specific projection of displaced ganglion cells upon the accessory optic system in the pigeon (Columbia livia). Proceedings of the National Academy of Sciences of the U.S.A. 74, 1753–1756.CrossRefGoogle ScholarPubMed
Kleerekoper, H. (1972). The sense organs. In The Biology of Lampreys, Vol. 2, ed. Hardisty, M.W. & Potter, I.C., pp. 373–404. New York: Academic Press.Google Scholar
Kohl, C. (1892). Rudimentäre Wirbeltieraugen. Zoologica 13, 48–51.Google Scholar
Linden, R. (1987). Displaced ganglion cells in the retina of the rat. Journal of Comparative Neurology 258, 138–143.CrossRefGoogle ScholarPubMed
Marenghi, G. (1900). Contributo alla fina organizzazione della retina. Anatomischer Anzeiger 18, 12–16.Google Scholar
Mariani, A.P. (1982). Biplexiform cells: ganglion cells of the primate retina that contact photoreceptors. Science 216, 1134–1136.CrossRefGoogle ScholarPubMed
Mednick, A.S. & Springer, A.D. (1988). Asymmetric distribution of retinal ganglion cells in the goldfish. Journal of Comparative Neurology 268, 49–59.Google Scholar
Munk, O. (1968). The eyes of Amia and Lepisosteus (Pisces, Holostei) compared with the brachiopterygian and teleostean eyes. Videnskbelige Meddelelser Fra Dansk Naturhistorisk Forening i Kobenhabvn 131, 109–127.Google Scholar
Münz, H. & Claas, B. (1981). Centrifugal innervation of the retina in cichlid and poecilid fishes. A horseradish peroxidase study. Neuroscience Letters 22, 223–226.Google Scholar
Peichl, L. (1989). Alpha and delta ganglion cells in the rat retina. Journal of Comparative Neurology 286, 120–139.CrossRefGoogle ScholarPubMed
Perry, V.H., Henderson, Z. & Linden, R. (1983). Postnatal changes in the retinal ganglion cell and optic axon population in the pigmented rat. Journal of Comparative Neurology 219, 356–368.CrossRefGoogle ScholarPubMed
Prada, F.A., Chmielewski, C.E., Dorado, M.E., Prada, C. & Génis-Gálvez, J.M. (1989). Displaced ganglion cells in the chick retina. Neuroscience Research 6, 329–339.CrossRefGoogle ScholarPubMed
Ramoa, A.S., Campbell, G. & Shatz, C.J. (1988). Dendritic growth and remodeling of cat retinal ganglion cells during fetal and postnatal development. Journal of Neuroscience 8, 4239–4261.Google Scholar
Retzius, G. (1893). Das Gehirn und das Auge von Myxine. Biologische Untersuchungen, Neue Folge 5, 55–68.Google Scholar
Rodieck, R.W. (1973). The Vertebrate Retina. Principles of Structure and Function. San Francisco: Freeman.Google Scholar
Rovainen, C.M. (1974). Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey. Journal of Comparative Neurology 154, 207–223.Google Scholar
Rovainen, C.M. (1982). Neurophysiology. In The Biology of Lampreys, ed. Hardisty, W.M. & Potter, I.C., pp. 1–136. London: Academic Press.Google Scholar
Rubinson, K. & Cain, H. (1989). Neural differentiation in the retina of the larval sea lamprey (Petromyzon marinus). Visual Neuroscience 3, 241–248.Google Scholar
Sandell, J.H. & Masland, R.H. (1988). Photoconversion of some fluorescent markers to a diaminobenzidine product. Journal of Histochemistry and Cytochemistry 36, 555–559.Google Scholar
Slonaker, J.R. (1897). A comparative study of the area of acute vision in vertebrates. Journal of Morphology 13, 445–492.Google Scholar
Stell, W.K. & Witkovsky, P. (1973). Retinal structure in the smooth dogfish, Mustelus canis: General description and light microscopy of giant ganglion cells. Journal of Comparative Neurology 148, 1–32.CrossRefGoogle ScholarPubMed
Teranishi, T., Negishi, K. & Kato, S. (1982). Two types of light-induced response recorded from horizontal cells in the river lamprey retina. Neuroscience Letters 33, 41–46.CrossRefGoogle ScholarPubMed
Tonosaki, A., Washioka, H., Hara, M., Ishikawa, M. & Watanabe, H. (1987). Gap junctions and synaptic relations of horizontal cells in lamprey retina. Neuroscience Research (Suppl.) 6, S107–S118.Google ScholarPubMed
Tóth, P. & Straznicky, C. (1989). Biplexiform ganglion cells in the retina of Xenopus laevis. Brain Research 499, 378–382.CrossRefGoogle ScholarPubMed
Tretjakoff, D.K. (1916). The sense organs of the lamprey (Lampetra fluviatilis). Thesis, University of Novorossijsk, Odessa.Google 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.Google Scholar
Vesselkin, N.P., Ermakova, T.V., Reperant, J., Kosareva, A.A. & Kenigfest, N.B. (1980). The retinofugal and retinopetal study using radioautographic and HRP methods. Brain Research 195, 453–460.Google Scholar
Vesselkin, N.P., Reperant, J., Kenigfest, N.B., Rio, J.P., Miceli, D. & Shupliakov, O.V. (1989). Centrifugal innervation of the lamprey retina. Light- and electron-microscopic and electrophysiological investigations. Brain Research 493, 51–65.Google Scholar