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Ganglion cell types of the turtle retina that project to the optic tectum: Intracellular HRP injections of retrogradely, rhodamine-marked cell bodies

  • Gloria D. Guiloff (a1) and Helga Kolb (a1)
Abstract

The turtle retina has been shown to have a variety of different morphological ganglion cell types as well as distinct physiological ganglion cell types. The major projection of the retina to the brain in nonmammalian vertebrates is to the optic tectum. In this study, we address the question of which retinal ganglion cell types project to the optic tectum in the turtle.

Fluorescent rhodamine-labeled microspheres were used to trace the retinal ganglion cell projection to the superficial layers of the optic tectum. The fluorescent ganglion cell somata, retrogradely marked by transport from the contralateral optic tectum, were impaled with micropipettes containing rhodamine-horseradish peroxidase solution and this dye was iontophoresed into the cells under visual control.

Most of the morphological ganglion cell types described in Golgi studies (Kolb, 1982; Kolb et al., 1988) were stained. Thus, the small cell types G1, G2, G3, G5, G6, and G7; the medium-sized types G10, G11, G12, G13, and G14; and the large-sized types G15, G16, G19, G20, and G21 project to the optic tectum in the turtle. We have added a new type, G2a, which proves to have some differences from the original G2 in branching pattern. We were unable to stain the small type G4, the medium-sized types G8 and G9, and the large cell types G17 and G18; this suggests that they might not project to the superficial layers of the dorsolateral optic tectum, at least, in the turtle.

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Abrahams, V.C. & Rose, P.K. (1975). The spinal course and distribution of fore and hind limb muscle afferent projections to the superior colliculus of the cat. Journal of Physiology (London) 247, 117130.
AmmermÜller, J., Guiloff, G., Normann, R. & Kolb, H. (1990). A ‘puff and advance’ technique for visually controlled staining of turtle retinal ganglion cells. Journal of Neuroscience Methods 32, 235243.
Amthor, F.R., Oyster, C.W. & Takahashi, E.S. (1984). Morphology of on-off direction selective ganglion cells in the rabbit retina. Brain Research 298, 187190.
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989a). Morphologies of rabbit retinal ganglion cells with concentric receptive fields. Journal of Comparative Neurology 280, 7296.
Amthor, F.R., Takahashi, E.S. & Oyster, C.W. (1989b). Morphologies of rabbit retinal ganglion cells with complex receptive fields. Journal of Comparative Neurology 280, 97121.
Barlow, H.B. (1953). Summation and inhibition of the frog's retina. Journal of Physiology 119, 69.
Bass, A.H. (1977). Effects of lesions of the optic tectum on the abilities of turtles to locate food stimuli. Brain, Behavior, and Evolution 14, 251260.
Bass, A.H., Pritz, M.B. & Northcutt, R.G. (1973). Effects of telencephalic and tectal ablations on visual behavior in the side-necked turtle Podocnemius unifilis. Brain Research 55, 455460.
Bowling, D.B. (1976). Properties of ganglion cells in the retina of the turtle. Ph.D. Dissertation, University of Colorado.
Bowling, D.B. (1980). Light responses of ganglion cells in the retina of the turtle. Journal of Physiology (London) 299, 173196.
Bowling, D.B. & Michael, C.R. (1980). Projections of single physiologically characterized optic tract fibres in cat. Nature 286, 899902.
Brening, R.K. & Rodieck, R.W. (1986). Morphology of the cat ganglion cells that project to the superior colliculus. Investigative Ophthalmology and Visual Science (Suppl.) 27, 223.
Brown, K.T. (1969). A linear area centralis extending across the turtle retina and stabilized to the horizon by non-visual cues. Vision Research 9, 10531062.
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, 210218.
Criswell, M.H. (1987). Cellular mechanisms of movement detection and directionality in the turtle retina. Doctoral dissertation, Indiana University, Bloomington.
Cuenca, N. & Kolb, H. (1989). Morphology and distribution of neurons immunoreactive for substance P in the turtle retina. Journal of Comparative Neurology 290, 391411.
Davydova, T.V., Goncharova, U.V. & Boyko, U.P. (1976). Retinotectal system of the tortoise Testudo horsfieldi, Gray (Morphofunctional study in the norm and after enucleation). Journal fūr Hirnforschung 17, 463488.
de Voe, R.D., Carras, P.L., Criswell, M.H. & Guy, R.G. (1989). Not by ganglion cells alone: directional selectivity is widespread in identified cells of the turtle retina. In Neurobiology of the Inner Retina, Vol. 31, ed. Weiler, R. & Osborne, N.N. pp. 235246. NATO ASI Series, Series H: Cell Biology.
Fukuda, Y., Hsiao, C.-F., Watanabe, M. & Ito, H. (1984). Morphological correlates of physiologically identified Y-, X-, and W-cells in cat retina. Journal of Neurophysiology 52, 9991013.
Fulbrook, J.E. (1982). Motion sensitivity of optic nerve axons in turtle, Pseudemys scripta elegans. Doctoral Dissertation, University of Delaware.
Fulbrook, J.E. & Granda, A.M. (1977). Receptive field properties of retinal ganglion cells in turtle. Society for Neuroscience Abstracts 3, 560.
Giolli, R.A. & Towns, L.C. (1980). A review of axon collateralization in the mammalian visual system. Brain, Behavior, and Evolution 17, 364390.
Granda, A.M. & Fulbrook, J.E. (1989). Classification of turtle retinal ganglion cells. Journal of Neurophysiology 62, 723737.
Guiloff, G.D., AmmermÜller, J. & Kolb, H. (1989). Morphology of ganglion cells that project to the optic tectum in the retina of the turtle. Investigative Ophthalmology and Visual Science (Suppl.) 30 (3), 348.
Guiloff, G.D., Chandler, N. & Kolb, H. (1990). The synaptic circuitry of a turtle retinal ganglion cell that projects to the optic tectum. Investigative Ophthalmology and Visual Science (Suppl.) 31 (4), 210.
Guiloff, G.D. & Jones, J. (1987). Electron microscopic study of the turtle inner plexiform layer. Investigative Ophthalmology and Visual Science (Suppl.) 28 (3), 261.
Guiloff, G.D., Jones, J. & Kolb, H. (1988). Organization of the inner plexiform layer of the turtle retina: an electron microscopic study. Journal of Comparative Neurology 212, 280292.
Guiloff, G.D., Maturana, H.R. & Varela, F.J. (1987). Cytoarchitecture of the avian ventral lateral geniculate nucleus. Journal of Comparative Neurology 264, 509526.
Hartline, H.K. (1938a). The discharge of impulses in the optic nerve of Pecten in response to illumination of the eye. Journal of Cellular and Comparative Physiology 11, 465478.
Hartline, H.K. (1938b). The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. American Journal of Physiology 121, 400415.
Jay, M.F. & Sparks, D.L. (1982). Auditory and saccade-related activity in the superior colliculus of the monkey. Society for Neuroscience Abstracts 8, 951.
Jensen, R.J. & De Voe, R.D. (1982). Ganglion cells and (dye-coupled) amacrine cells in the turtle retina that have possible synaptic connections. Brain Research 240, 146150.
Jensen, R.J. & De Voe, R.D. (1983). Comparisons of directionally selective with other ganglion cells of the turtle retina: intracellular recording and staining. Journal of Comparative Neurology 217, 271287.
Kolb, H. (1982). The morphology of the bipolar cells, amacrine cells and ganglion cells in the retina of the turtle Pseudemys šcripta elegans. Philosophical Transactions of the Royal Society B (London) 298, 355393.
Kolb, H., Perlman, I. & Normann, R.A. (1988). Neural organization of the retina of the turtle Clemys caspica: a light microscopic and Golgi study. Visual Neuroscience 1, 4772.
Maeda, M., Shibazaki, T. & Yoshida, K. (1979). Labyrinthine and visual inputs to superior colliculus neurons. In Progress in Brain Research, Vol. 50, ed. Granit, R. & Pompeiano, O., pp. 735743. Amsterdam: Elsevier.
Marchlafava, P.L. (1979). The responses of retinal ganglion cells to stationary and moving visual stimuli. Vision Research 19, 12031211.
Marchlafava, P.L. (1983). The organization of inputs establishes two functional and morphologically identifiable classes of ganglion cells in the retina of the turtle. Vision Research 23, 325338.
Marchlafava, P.L. & Wagner, H.G. (1981). Interactions leading to colour opponency in ganglion cells of the turtle retina. Proceedings of the Royal Society B (London) 211, 261267.
Marchlafava, P.L. & Weiler, R. (1980). Intracellular analysis and structural correlates of the organization of inputs to ganglion cells in the retina of the turtle. Proceedings of the Royal Society B (London) 208, 103113.
Mrosovsky, N., Granda, A.M. & Hay, T. (1979). Seaward orientation of hatchling turtles: turning systems in the optic tectum. Brain, Behavior, and Evolution 16, 203221.
Muller, J.E., Ammermuller, J. & Kolb, H. (1991). Synaptic inputs to physiologically defined turtle retinal ganglion cells. Visual Neuroscience 7, 409429.
Nelson, R., FamigliettiE.V., Jr. E.V., Jr. & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for on- and off- center ganglion cells in cat retina. Journal of Neurophysiology 41, 472483.
Northcutt, R.G. (1978). Forebrain and midbrain organization in lizards and its possible evolutionary significance. In The Behavior and Neurology of Lizards, ed. Greenberg, N. & Maclean, P.D., pp. 1164. Rockville, Maryland: NIMH.
Peichl, L., Buhl, E.H. & Boycott, B.B. (1987). Alpha ganglion cells in the rabbit retina. Journal of Comparative Neurology 263, 2541.
Peterson, E.H. (1978). Size classes of ganglion cells which project to the optic tectum in the turtle, Pseudemys scripta. Anatomical Records 190, 509510.
Peterson, E.H. & Ulinski, P.S. (1979). Quantitative studies of retinal ganglion cells in a turtle, Pseudemys scripta elegans, Number, I. and distribution of ganglion cells. Journal of Comparative Neurology 186, 1742.
Peterson, E.H. & Ulinski, P.S. (1982). Quantitative studies of retinal ganglion cells in a turtle, Pseudemys scripta elegans. II. Size spectrum of ganglion cells and its regional variation. Journal of Comparative Neurology 208, 157168.
Reiner, A. (1981). A projection of displaced ganglion cells and giant ganglion cells to the accessory optic nuclei in turtle. Brain Research 204, 403409.
Schwartz, E.A. (1973). Organization of ON-OFF cells in the retina of turtle. Journal of Physiology (London) 230, 114.
Sinoman, E.L. & Scalia, F. (1990). Quantitative study of the tectally projecting retinal ganglion cells in the adult frog. I. The size of the contralateral and ipsilateral projections. Journal of Comparative Neurology 302, 792809.
Sjostrom, A.M. & Ulinski, P.S. (1985). Morphology of retinogeniculate terminals in the turtle, Pseudemys scripta elegans. Journal of Comparative Neurology 238, 107120.
Stanford, L.R. (1987). X-cells in the cat retina: relationships between the morphology and physiology of a class of cat retinal ganglion cells. Journal of Neurophysiology 58, 940964.
Stein, B.E. & Gaither, N.S. (1981). Sensory representation in reptilian optic tectum: some comparisons with mammals. Journal of Comparative Neurology 202, 6087.
Tauchi, M. & Masland, R.H. (1984). The shape and arrangement of the cholinergic neurons in the rabbit retina. Proceedings of the Royal Society B (London) 223, 101199.
Ulinski, P.S. (1977). Tectal afferents in the banded water snake, Natrix sipedon. Journal of Comparative Neurology 173, 251274.
Ulinski, P.S. (1980). Functional morphology of the vertebrate visual system: an essay on the evolution of complex systems. American Zoology 20, 229246.
Vaney, D.I. (1986). Morphological identification of serotonin-accumulating neurons in the living retina. Science 233, 444446.
Watanabe, M. & Rodieck, R.W. (1989). Parasol and midget ganglion cells of the primate retina. Journal of Comparative Neurology 289, 434454.
Weiler, R. & Ammermüller, J. (1986). Immunocytochemical localization of serotonin in intracellularly analyzed and dye-injected ganglion cells of the turtle retina. Neuroscience Letters 72, 147152.
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Visual Neuroscience
  • ISSN: 0952-5238
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