Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T17:12:31.943Z Has data issue: false hasContentIssue false
  • English
  • Français

The number, morphology, and distribution of retinal ganglion cells and optic axons in the Australian lungfish Neoceratodus forsteri (Krefft 1870)

Published online by Cambridge University Press:  24 April 2006

HELENA J. BAILES ,
ANN E.O. TREZISE  and
SHAUN P. COLLIN
HELENA J. BAILES
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, QLD 4072, Australia
ANN E.O. TREZISE
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, QLD 4072, Australia
SHAUN P. COLLIN
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, QLD 4072, Australia
Get access Rights & Permissions [Opens in a new window]

Abstract

Australian lungfish Neoceratodus forsteri may be the closest living relative to the first tetrapods and yet little is known about their retinal ganglion cells. This study reveals that lungfish possess a heterogeneous population of ganglion cells distributed in a horizontal streak across the retinal meridian, which is formed early in development and maintained through to adult stages. The number and complement of both ganglion cells and a population of putative amacrine cells within the ganglion cell layer are examined using retrograde labelling from the optic nerve and transmission electron-microscopic analysis of axons within the optic nerve. At least four types of retinal ganglion cells are present and lie predominantly within a thin ganglion cell layer, although two subpopulations are identified, one within the inner plexiform and the other within the inner nuclear layer. A subpopulation of retinal ganglion cells comprising up to 7% of the total population are significantly larger (>400 μm2) and are characterized as giant or alpha-like cells. Up to 44% of cells within the retinal ganglion cell layer represent a population of presumed amacrine cells. The optic nerve is heavily fasciculated and the proportion of myelinated axons increases with body length from 17% in subadults to 74% in adults. Spatial resolving power, based on ganglion cell spacing, is low (1.6–1.9 cycles deg−1, n = 2) and does not significantly increase with growth. This represents the first detailed study of retinal ganglion cells in sarcopterygian fish, and reveals that, despite variation amongst animal groups, trends in ganglion cell density distribution and characteristics of cell types were defined early in vertebrate evolution.

Keywords

Visual streakSpatial resolving powerAmacrine cellsOptic nerveDipnoi
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 2 , March 2006 , pp. 257 - 273
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Ali, M.A. & Anctil, M. (1973). Retina of the South American lungfish Lepidosiren paradoxa Fitzinger. Canadian Journal of Zoology 51, 969–972.CrossRefGoogle Scholar
Bailes, H.J., Robinson, S.R., Trezise, A.E.O., & Collin, S.P. (2006). Morphology, characterization and distribution of retinal photoreceptors in the Australian lungfish Neoceratodus forsteri (Krefft, 1870). Journal of Comparative Neurology 494, 381–397.CrossRefGoogle Scholar
Ball, A.K. & Dickson, D.H. (1983). Displaced amacrine and ganglion cells in the newt retina. Experimental Eye Research 36, 199–213.CrossRefGoogle Scholar
Bennis, M., El Hassni, M., Rio, J.-P., Lecren, D., Repérant, J., & Ward, R. (2001). A quantitative study of the optic nerve of the chameleon. Brain, Behavior and Evolution 58, 49–60.CrossRefGoogle Scholar
Bernhardt, R. (1989). Axonal path-finding during the regeneration of the goldfish optic pathway. Journal of Comparative Neurology 284, 119–134.CrossRefGoogle Scholar
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology 240, 397–419.CrossRefGoogle Scholar
Bozzano, A. & Catalan, I.A. (2002). Ontogenetic changes in the retinal topography of the European hake, Merluccius merluccius: Implications of feeding and depth distribution. Marine Biology 141, 549–559.Google Scholar
Bozzano, A. & Collin, S.P. (2000). Retinal ganglion cell topography in elasmobranchs. Brain, Behavior and Evolution 55, 191–208.CrossRefGoogle Scholar
Brooks, S. & Kind, P. (2001). Ecology and demographics of lungfish (Neoceratodus forsteri) and general fish communities in the Burnett River, Queensland, with reference to the impacts of Walla Weir and future infrastructure development. Queensland Department of Primary Industries Report, Brisbane, Australia.
Cameron, D.A. (1995). Asymmetric retinal growth in the adult teleost green sunfish (Lepomis cyanellus). Visual Neuroscience 12, 95–102.CrossRefGoogle Scholar
Cima, C. & Grant, P. (1982). Development of the optic nerve in Xenopus laevis: II. Gliogenesis, myelination and metamorphic remodelling. Journal of Embryology and Experimental Morphology 77, 251–267.Google Scholar
Cleland, B.G., Levick, W.R., & Wässle, H. (1975). Physiological identification of a morphological class of cat retinal ganglion cells. Journal of Physiology 248, 151–171.CrossRefGoogle Scholar
Coleman, L.-A., Dunlop, S.A., & Beazley, L.D. (1984). Patterns of cell division during visual streak formation in the frog Limnodynastes dorsalis. Journal of Embryology and Experimental Morphology 83, 119–135.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 Scholar
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.CrossRefGoogle Scholar
Collin, S.P. (1999). Behavioural ecology and retinal cell topography. In Adaptive Mechanisms in the Ecology of Vision, ed. Archer, S.N., Djamgoz, M.B.A., Loew, E.R., Partridge, J.C. & Vallerga, S., pp. 509–535. Dordrecht: Kluwer Academic Publishers.CrossRef
Collin, S.P. & Collin, H.B. (1988). Topographic analysis of the retinal ganglion cell layer and optic nerve in the sandlance Limnichthyes fasciatus (Creeiidae, Perciformes). Journal of Comparative Neurology 278, 226–241.CrossRefGoogle Scholar
Collin, S.P., Hoskins, R.V., & Partridge, J.C. (1998). Seven retinal specializations in the tubular eye of the deep-sea pearleye, Scopelarchus michaelsarsi: A case study in visual optimization. Brain, Behavior and Evolution 51, 291–314.CrossRefGoogle Scholar
Collin, S.P. & Northcutt, R.G. (1993). The visual system of the Florida garfish, Lepisosteus platyrhinchus (Ginglymodi). III. Retinal ganglion cells. Brain, Behavior and Evolution 42, 295–320.Google Scholar
Collin, S.P. & Pettigrew, J.D. (1988a). 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
Collin, S.P. & Pettigrew, J.D. (1988b). Retinal topography in reef teleosts. II. Some species with prominent horizontal streaks and high-density areae. Brain, Behavior and Evolution 31, 283–295.Google Scholar
Collin, S.P. & Pettigrew, J.D. (1988c). Retinal ganglion cell topography in teleosts: A comparison between Nissl-stained material and retrograde labelling from the optic nerve. Journal of Comparative Neurology 276, 412–422.Google Scholar
Collin, S.P. & Pettigrew, J.D. (1989). Quantitative comparison of the limits on visual spatial resolution set by the ganglion cell layer in twelve species of reef teleosts. Brain, Behavior and Evolution 34, 184–192.Google Scholar
Cook, J.E. & Becker, D.L. (1991). Regular mosaics of large displaced and non-displaced ganglion-cells in the retina of a cichlid fish. Journal of Comparative Neurology 306, 668–684.CrossRefGoogle Scholar
Cook, J.E., Becker, D.L., & Kapila, R. (1992). Independent mosaics of large inner- and outer-stratified ganglion cells in the goldfish retina. Journal of Comparative Neurology 318, 355–366.CrossRefGoogle Scholar
Cook, J.E. & Noden, A.J. (1998). Somatic and dendritic mosaics formed by large ganglion cells in the retina of the common house gecko (Hemidactylus frenatus). Brain, Behavior and Evolution 51, 263–283.CrossRefGoogle Scholar
Cook, J.E. & Sharma, S.C. (1995). Large retinal ganglion cells in the channel catfish (Ictalurus punctatus): Three types with distinct dendritic stratification patterns form similar but independent mosaics. Journal of Comparative Neurology 362, 331–349.CrossRefGoogle Scholar
Dean, B. (1906). Notes on the living specimens of the Australian lungfish, Ceratodus forsteri, in the Zoological Society's collection. Proceedings of the Zoological Society of London 168–178.Google Scholar
Dogiel, A.S. (1891). Über die nervösen Elemente in der Retina des Menschen. Archiv für Mikroskopische Anatomie 40, 29–38.Google Scholar
Dunlop, S.A. & Beazley, L.D. (1981). Changing retinal ganglion cell distribution in the frog Heleioporus eyrei. Journal of Comparative Neurology 202, 221–236.CrossRefGoogle Scholar
Dunlop, S.A. & Beazley, L.D. (1984). A morphometric study of the retinal ganglion cell layer and optic nerve from metamorphosis in Xenopus laevis. Vision Research 24, 417–427.CrossRefGoogle Scholar
Dunn-Meynell, A. & Sharma, S.C. (1986). The visual system of the channel catfish (Ictalurus punctatus). I. Retinal ganglion cell morphology. Journal of Comparative Neurology 247, 32–55.Google Scholar
Dunn-Meynell, A. & Sharma, S.C. (1987). The visual system of the channel catfish (Ictalurus punctatus). II. The morphology associated with the optic papillae and retinal ganglion-cell distribution. Journal of Comparative Neurology 257, 166–175.Google Scholar
Easter, S.S.J. (1992). Retinal growth in foveated teleosts: Nasotemporal asymmetry keeps the fovea in temporal retina. Journal of Neuroscience 12, 2381–2392.Google Scholar
Ebbesson, S.O.E. & Meyer, D.L. (1981). Efferents to the retina have multiple sources in teleost fish. Science 214, 924–926.CrossRefGoogle Scholar
Fleischhauer, K. & Wartenberg, H. (1967). Elektronmikroskopische Untersuchungen über das Wachstum der Nervenfasern und über das Auftreten von Markscheiden im Corpus callosum der Katze. Zeitschrift für Zellforschung und Mikroskopische Anatomie 83, 568–581.CrossRefGoogle Scholar
Frank, B.D. & Hollyfield, J.G. (1987). Retinal ganglion cell morphology in the frog, Rana pipiens. Journal of Comparative Neurology 266, 413–434.CrossRefGoogle Scholar
Fritzsch, B. & Collin, S.P. (1990). Dendritic distribution of two populations of ganglion cells and the retinopetal fibers of the silver lamprey (Ichthyomyzon unicuspis). Visual Neuroscience 4, 533–545.CrossRefGoogle Scholar
Fritzsch, B. & Himstedt, W. (1981). Pretectal neurons project to the salamander retina. Neuroscience Letters 24, 13–17.CrossRefGoogle Scholar
Giolli, R.A. & Towns, L.C. (1980). A review of axon collateralization in the mammalian visual system. Brain, Behavior and Evolution 17, 364–390.CrossRefGoogle Scholar
Graydon, M.L. & Giorgi, P.P. (1984). Topography of the retinal ganglion cell layer of Xenopus. Journal of Anatomy 139, 145–157.Google Scholar
Grigg, G.C. (1965). Studies on the Queensland lungfish, Neoceratodus forsteri (Krefft). III. Aerial respiration in relation to habits. Australian Journal of Zoology 13, 413–421.CrossRefGoogle Scholar
Hart, N.S. (2002). Vision in the peafowl (Aves: Pavo cristatus). Journal of Experimental Biology 205, 3925–3935.Google Scholar
Hildebrand, C., Remahl, S., Persson, H., & Bjartmer, C. (1992). Myelinated nerve fibres in the CNS. Progress in Neurobiology 40, 319–384.Google Scholar
Hirt, B. & Wagner, H.J. (2005). The organization of the inner retina in a pure-rod deep-sea fish. Brain, Behavior and Evolution 65, 157–167.CrossRefGoogle Scholar
Hitchcock, P. & Easter, S. (1986). Retinal ganglion cells in goldfish: A qualitative classification into four morphological types, and a quantitative study of the development of one of them. Journal of Neuroscience 6, 1037–1050.Google Scholar
Hsaio, K. (1984). Bilateral branching contributes minimally to the enhanced ipsilateral projection in monocular Syrian golden hamsters. Journal of Neuroscience 4, 368–373.Google Scholar
Hueter, R.E. (1991). Adaptations for spatial vision in sharks. Journal of Experimental Zoology Supplement 5, 130–141.Google Scholar
Hughes, A. (1977). The topography of vision in mammals of contrasting lifestyles: Comparative optics and retinal organization. In Handbook of Sensory Physiology: The Visual System in Vertebrates, ed. Crescitelli, F., pp. 615–756. Berlin: Springer-Verlag.
Hughes, A. (1981). Population magnitudes and distribution of the major modal classes of cat retinal ganglion cell as estimated from HRP filling and a systematic survey of the soma diameter spectra for classical neurons. Journal of Comparative Neurology 197, 303–339.CrossRefGoogle 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.
Hursh, J.B. (1939). Conduction velocity and diameter of nerve fibers. American Journal of Physiology 127, 131–139.Google Scholar
Ito, H. & Murakami, T. (1984). Retinal ganglion cells in two teleost species, Sebasticus marmoratus and Navodon modestus. Journal of Comparative Neurology 229, 80–96.CrossRefGoogle Scholar
Ito, H., Yoshimoto, M., Albert, J.S., Yamamoto, N., & Sawai, N. (1999). Retinal projections and retinal ganglion cell distribution patterns in a sturgeon (Acipenser transmontanus), a non-teleost actinopterygian fish. Brain, Behavior and Evolution 53, 127–141.CrossRefGoogle Scholar
Johns, P.R. & Easter, S.S.J. (1977). Growth of the adult goldfish eye. II. Increase in retinal cell numbers. Journal of Comparative Neurology 176, 331–342.Google Scholar
Joss, J.M.P. (1998). Are extant lungfish neotenic? Clinical and Experimental Pharmacology and Physiology 25, 733–735.Google Scholar
Joss, J.M.P. & Joss, G. (1995). Breeding Australian lungfish in captivity. In Reproductive Physiology of Fish, ed. Thomas, F.W.G.P., pp. 121, Austin, Texas: Fish Symposium 95.
Kalinina, A.V. (1976). Quantity and topography of frog's retinal ganglion cells. Vision Research 16, 929–934.CrossRefGoogle Scholar
Kemp, A. (1986). The Biology of the Australian Lungfish, Neoceratodus forsteri (Krefft 1870). Journal of Morphology Supplement 1, 181–198.CrossRefGoogle Scholar
Kemp, A., Anderson, T., Tomley, A., & Johnson, I. (1981). The use of the Australian lungfish (Neoceratodus forsteri) for the control of submerged aquatic weeds. In 5th International Conference on Weed Control, ed. C.S.I.R.O., pp. 155–158. Melbourne, Australia: C.S.I.R.O.
Kock, J.-H. & Reuter, T. (1978). Retinal ganglion cells in the crucian carp (Carassius carassius). I. Size and number of somata in eyes of different size. Journal of Comparative Neurology 179, 535–548.Google Scholar
Linke, R. & Roth, G. (1990). Optic nerves in plethodontid Salamanders (Amphibia, Urodela): Neuroglia, fiber spectrum and myelination. Anatomy and Embryology 181, 37–48.CrossRefGoogle Scholar
Little, G.J. & Giorgi, P.P. (1984). Ultrastructure of the optic nerve of the Queensland lungfish Neoceratodus forsteri. Journal of Anatomy 139, 188.Google Scholar
Mangrum, W.I., Dowling, J.E., & Cohen, E.D. (2002). A morphological classification of ganglion cells in the zebrafish retina. Visual Neuroscience 19, 767–779.CrossRefGoogle Scholar
Matthiessen, L. (1880). Untersuchungen über den Aplanatismus und die Periscopie der Kristallinsen in den Augen der Fische. Pflügers Archiv 21, 287–307.CrossRefGoogle Scholar
Maturana, H.R., Lettvin, J.Y., McCulloch, W.S., & Pitts, W.H. (1960). Anatomy and physiology of vision in the frog (Rana pipiens). Journal of General Physiology 43, 129–175.CrossRefGoogle Scholar
Mednick, A.S., Berk, M.F., & Springer, A.D. (1988). Asymmetric distribution of cells in the inner nuclear and cone mosaic layers of the goldfish retina. Neuroscience Letters 94, 241–246.CrossRefGoogle Scholar
Mednick, A.S. & Springer, A.D. (1988). Asymmetric distribution of retinal ganglion cells in goldfish. Journal of Comparative Neurology 268, 46–59.Google Scholar
Müller, B. & Peichl, L. (1989). Topography of cones and rods in the tree shrew retina. Journal of Comparative Neurology 282, 581–594.CrossRefGoogle Scholar
Munk, O. (1964). The eye of Calamoichthyes calabaricus Smith, 1865 (Polypteridae, Pisces) compared with the eye of other fishes. Videnskabelige Meddellelser Dansk Naturhistorisk Forening 127, 113–125.Google Scholar
Munk, O. (1969). On the visual cells of some primitive fishes with particular regard to the classification of rods and cones. Videnskabelige Meddellelser Dansk Naturhistorisk Forening 132, 25–30.Google Scholar
Nguyen, V.-S. & Straznicky, C. (1989). The development and the topographic organization of the retinal ganglion layer in Bufo marinus. Experimental Eye Research 75, 345–353.Google Scholar
Northcutt, G.R. (1977). Retinofugal projections in the lepidosirenid lungfishes. Journal of Comparative Neurology 174, 553–574.CrossRefGoogle Scholar
Northcutt, G.R. (1980). Retinal projections in the Australian lungfish. Brain Research 185, 85–90.CrossRefGoogle Scholar
Peichl, L. & Wässle, H. (1981). Morphological identification of on- and off-centre brisk transient (Y) cells in the cat retina. Proceedings of the Royal Society B (London) 212, 139–156.CrossRefGoogle Scholar
Pettigrew, J.D., Dreher, B., Hopkins, C.S., McCall, M.J., & Brown, M. (1988). Peak density and distribution of ganglion-cells in the retinae of microchiropteran bats—Implications for visual-acuity. Brain, Behavior and Evolution 32, 39–56.CrossRefGoogle Scholar
Pfeiffer, W. (1968). Retina und retinomotorik der Dipnoi und Brachiopterygii. Zeitschrift für Zellforschung und Mikroskopische Anatomie 89, 62–72.CrossRefGoogle Scholar
Playford, D.E. & Dunlop, S.A. (1993). A biphasic sequence of myelination in the developing optic nerve of the frog. Journal of Comparative Neurology 333, 83–93.CrossRefGoogle Scholar
Pow, D.V. (1994). Taurine, amino-acid transmitters, and related molecules in the retina of the Australian lungfish Neoceratodus forsteri—A light-microscopic immunocytochemical and electron-microscopic study. Cell and Tissue Research 278, 311–326.CrossRefGoogle Scholar
Provis, J.M. (1979). The distribution and size of ganglion cells in the retina of the pigmented rabbit: A quantitative analysis. Journal of Comparative Neurology 185, 121–138.CrossRefGoogle Scholar
Rahmann, H.G. (1979). Ontogeny of visual acuity of rainbow trout under normal conditions and light deprivation. Behaviour 68, 315–322.CrossRefGoogle Scholar
Ramón y Cajal, S. (1892). La rétine des vertébrés. La Cellule 9, 121–133.Google Scholar
Rasband, W.S. (1997–2005). Image J. Bethesda, Maryland, U.S.A.: U.S. National Institutes of Health.
Reiner, A. (1981). A projection of displaced ganglion cells and giant ganglion cells to the accessory optic nuclei in 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
Repérant, J., Miceli, D., Vesselkin, N.P., & Molotchnikoff, S. (1989). The centrifugal visual system of vertebrates: A century-old search reviewed. International Review of Cytology 118, 115–171.CrossRefGoogle Scholar
Ritchie, J.M. (1984). Physiological basis of conduction in myelinated nerve fibers. In Myelin, ed. Morell, P., pp. 117–146. New York: Plenum Press.
Robinson, S.R. (1994). Early vertebrate color-vision. Nature 367, 121.Google Scholar
Rochon-Duvigneaud, A. (1941). L'oeil de Lepidosiren paradoxa. Comptes Rendus Hebdomadaires des Séances de l'Académie des Sciences 212, 307–309.Google Scholar
Rochon-Duvigneaud, A. (1943). Les yeux et la vision des vertébrés. Paris: Masson.
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: Properties, types, genera, pathways and trans-species comparisons. Brain, Behavior and Evolution 23, 121–164.Google Scholar
Shamim, K.M., Scalia, F., Toth, P., & Cook, J.E. (1997a). Large retinal ganglion cells that form independent, regular mosaics in the ranid frogs Rana esculenta and Rana pipiens. Visual Neuroscience 14, 1109–1127.Google Scholar
Shamim, K.M., Toth, P., Becker, D.L., & Cook, J.E. (1999). Large retinal ganglion cells that form independent, regular mosaics in the bufonoid frogs Bufo marinus and Litoria moorei. Visual Neuroscience 16, 861–879.Google Scholar
Shamim, K.M., Toth, P., & Cook, J.E. (1997b). Large retinal ganglion cells in the pipid frog Xenopus laevis form independent, regular mosaics resembling those of teleost fishes. Visual Neuroscience 14, 811–826.Google Scholar
Shand, J. (1997). Ontogenetic changes in retinal structure and visual acuity: A comparative study of coral-reef teleosts with differing post-settlement lifestyles. Environmental Biology of Fishes 49, 307–322.CrossRefGoogle Scholar
Shand, J., Chin, S.M., Harman, A.M., Moore, S., & Collin, S.P. (2000). Variability in the location of the retinal ganglion cell area centralis is correlated with ontogenetic changes in feeding behaviour in the black bream Acanthopagrus butcheri (Sparidae, Teleostei). Brain, Behavior and Evolution 55, 176–190.CrossRefGoogle Scholar
Sillman, A.J. & Dahlin, D.A. (2003). The photoreceptors and visual pigments of sharks and sturgeons. In The Senses of Fishes: Adaptations for the Reception of Natural Stimuli, ed. Kapoor, B.G. & von der Emde, G., pp. 31–52. New Delhi, India: Narosa Publishing House.
Simpson, R., Kind, P., & Brooks, S. (2002). Trials of the Queensland Lungfish. Nature Australia Winter36–43.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.Google Scholar
Stensaas, L.J. (1977). The ultrastructure of astrocytes, oligodendrocytes, and microglia in the optic nerve of urodele amphibians (A. punctatum, T. pyrrhogaster, T. viridescens). Journal of Neurocytology 6, 269–286.Google Scholar
Stone, J. (1981). The Wholemount Handbook. Sydney, Australia: Maitland.
Straznicky, C. & Straznicky, I.T. (1988). Morphological classification of retinal ganglion cells in adult Xenopus laevis. Anatomy and Embryology 178, 143–153.CrossRefGoogle Scholar
Straznicky, K. & Gaze, R.M. (1971). The growth of the retina in Xenopus laevis: An autoradiographic study. Journal of Embryology and Experimental Morphology 26, 67–79.Google Scholar
Sun, W.Z., Li, N., & He, S.G. (2002). Large-scale morphological survey of mouse retinal ganglion cells. Journal of Comparative Neurology 451, 115–126.CrossRefGoogle Scholar
Taban, M., Heller, K.B., Hsu, H.Y., & Sadun, A.A. (2005). Bifurcating axons account for the increase in axonal population in posterior human optic nerve. Neuro-Ophthalmology 29, 109–114.CrossRefGoogle Scholar
Tapp, R.L. (1974). Axon numbers and distribution, myelin thickness, and the reconstruction of the compound action potential in the optic nerve of the teleost: Eugerres plumieri. Journal of Comparative Neurology 153, 267–274.CrossRefGoogle Scholar
Tasaki, I. (1982). Physiology and Electrochemistry of Nerve Fibers. New York: Academic Press.
Tóth, P. & Straznicky, C. (1989). The morphological characterization and distribution of displaced ganglion cells in the anuran retina. Visual Neuroscience 3, 551–561.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 Scholar
Uemura, M., Somiya, H., Moku, M., & Kawaguchi, K. (2000). Temporal and mosaic distribution of large ganglion cells in the retina of a daggertooth aulopiform deep-sea fish (Anotopterus pharao). Philosophical Transactions of the Royal Society B (London) 355, 1161–1166.CrossRefGoogle Scholar
Van der Meer, H.J. (1995). Visual resolution during growth in a cichlid fish: A morphological and behavioural case study. Brain, Behavior and Evolution 45, 25–33.CrossRefGoogle Scholar
Vaney, D.I. & Hughes, A. (1976). The rabbit optic nerve: Fiber diameter spectrum, fibre count, and comparison with a retinal ganglion cells count. Journal of Comparative Neurology 170, 241–251.CrossRefGoogle Scholar
Veenman, C.L., Reiner, A., & Honig, M.G. (1992). Biotinylated dextran amine as an anterograde tracer for single-labelling and double-labelling studies. Journal of Neuroscience Methods 41, 239–254.CrossRefGoogle Scholar
Vesselkin, N.P., Reperant, J., Kenigfest, N.B., Miceli, D., Ermakova, T.V., & Rio, J.P. (1984). An anatomical and electrophysiological study of the centrifugal visual system in the lamprey (Lampetra fluviatilis). Brain Research 292, 41–56.CrossRefGoogle Scholar
Walls, G. (1942). The Vertebrate Eye and its Adaptive Radiation. New York: Hafner Publishing Company.CrossRef
Wässle, H., Peichl, L., & Boycott, B.B. (1981). Morphology and topography of ON- and OFF-alpha cells in the cat retina. Proceedings of the Royal Society B (London) 212, 157–175.CrossRefGoogle Scholar
Watt, C.B., Glazebrook, P.A., & Florack, V.J. (1994). Localization of substance P and GABA in retinotectal ganglion cells of the larval tiger salamander. Visual Neuroscience 11, 355–362.CrossRefGoogle Scholar
Watt, M., Evans, C.S., & Joss, J.M.P. (1999). Use of electroreception during foraging by the Australian lungfish. Animal Behaviour 58, 1039–1045.CrossRefGoogle Scholar
Wetts, R., Serbezija, G.N., & Fraser, S.E. (1989). Cell lineage analysis reveals multipotent precursors in the ciliary margin of the frog retina. Developmental Biology 136, 254–263.CrossRefGoogle Scholar
Wirsig-Wiechmann, C.R. & Basinger, S.F. (1988). FMRFamide-immunoreactive retinopetal fibers in the frog, Rana pipiens: Demonstration by lesion and immunocytochemical techniques. Brain Research 449, 116–134.CrossRefGoogle Scholar
Wong, R.O.L. & Hughes, A. (1987). The morphology, number, and distribution of a large population of confirmed displaced amacrine cells in the adult cat retina. Journal of Comparative Neurology 255, 159–177.CrossRefGoogle Scholar
Zygar, C.A., Lee, M.J., & Fernald, R.D. (1999). Nasotemporal asymmetry during teleost retinal growth: Preserving an area of specialization. Journal of Neurobiology 41, 435–442.3.0.CO;2-9>CrossRefGoogle Scholar