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A light- and electron-microscopic investigation of the optic tectum of the frog, Rana pipiens, I: The retinal axons

Published online by Cambridge University Press:  02 June 2009

Thomas E. Hughes
Thomas E. Hughes
Affiliation:
Duke University Medical Center, Department of Anatomy, Durham
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Abstract

There are several different groups of ganglion cells in the retina of the frog. Although their axons are thought to terminate in different layers of the optic tectum, little is known about the morphology of their terminal arbors or their synaptic targets. The present paper reports the results of a layer-by-layer study of horseradish peroxidase labeled retinal axons in the optic tectum of Rana pipiens. Light and electron microscopy was used to study the axon's laminar distribution, patterns of arborization, and synaptic contacts.

Labeled retinal axons were found in all of the superficial layers of the tectum (A-G). From layer to layer, the retinal axons differed markedly in the diameter of their parent axons (0.2−3.0 μm) and in the morphology and horizontal extent of their terminal arbors.

Five classes of synaptic terminals could be distinguished in the tectum. The retinal terminals belonged to class characterized by round, medium-sized synaptic vesicles. They made synaptic contact with dendrites and other axon terminals in each of the layers. They were always the presynaptic component. The postsynaptic dendrites were often the vertically oriented processes of cells located in the deeper layers. The postsynaptic terminals belonged to a class distinguished by their flat, medium-sized vesicles. These terminals in turn contacted what appeared to be dendrites. In layer eight, the retinal axons were often large, spoon-shaped boutons that ended in apposition with the somata of the layer.

Keywords

Horseradish peroxidaseMorphologyLaminaeSynapses
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 6 , June 1990 , pp. 499 - 518
Copyright
Copyright © Cambridge University Press 1990

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References

Adams, J.C. (1977). Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2, 141–145.CrossRefGoogle ScholarPubMed
Behan, M. (1981). Identification and distribution of retinocollicular terminals in the car: an electron microscopic autoradiographic analysis. Journal of Comparative Neurology 199, 1–15.CrossRefGoogle Scholar
Bellonci, J. (1888). Uber die centrale Endigung des nervus Opticus bei den Vertebraten. Zeitschrift für Wissenschaftliche Zoologie 47, 1–46.Google Scholar
Bishop, G.H. (1933). Fiber groups in the optic nerve. American Journal of Physiology 106, 461–474.CrossRefGoogle Scholar
Bowling, D.B. & Michael, C.R. (1984). Terminal patterns of single, physiologically characterized optic tract fibers in the cat's lateral geniculate nucleus. Journal of Neuroscience 4, 198–216.CrossRefGoogle ScholarPubMed
Cohen, C. & Longley, W. (1966). Tropomyosin paracrystals formed by divalent cations. Science 152, 794–796.CrossRefGoogle ScholarPubMed
Dacey, D.M. & Ulinski, P.S. (1986). Optic tectum of the Eastern garter snake (Thamnophis sirtalis), IV: Morphology of afferents from the retina. Journal of Comparative Neurology 245, 301–318.CrossRefGoogle ScholarPubMed
Dennison, M.E. (1971). Electron stereoscopy as a means of classifying synaptic vesicles. Journal of Cell Science 8, 525–539.CrossRefGoogle ScholarPubMed
Fite, K.V. & Scalia, F. (1976). Central visual pathways in the frog. In The Amphibian Visual System: A Multidisciplinary Approach, ed. Fite, K., pp. 87–118. New York: Academic Press.CrossRefGoogle Scholar
Fukuda, Y. & Stone, J. (1974). Retinal distribution and central projections of Y, X, and W cells of the cat's retina. Journal of Neurophysiology 37, 749–772.CrossRefGoogle Scholar
Gaupp, E. (1899). Ecker's, A. und Wiedersheim's, R. “Analomie des Frosches,” Zweite Abteilung. Lehre vom Nervensystem. Braunschweig: R. Vieweg, 548pp.Google Scholar
Grant, A.C. (1989). The nature of electrical transients recorded in the neuropil of the frog's optic tectum. Ph.D. Thesis, Massachusetts Institute of Technology.Google Scholar
Gruberg, E.R. & Udin, S.B. (1978). Topographic projections between the nucleus isthmi and the tectum of the frog (Rana pipiens). Journal of Comparative Neurology 179, 487–500.CrossRefGoogle ScholarPubMed
Gruberg, E.R., Wallace, M.T. & Waldeck, R.F. (1989). The relationship between isthmotectal fibers and other tectopedal systems in the leopard frog. Journal of Comparative Neurology 288(1), 39–50.CrossRefGoogle ScholarPubMed
Hartline, H.K. (1938). The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. American Journal of Physiology 121, 400–415.CrossRefGoogle Scholar
Henley, J.M., Lindstrom, J.M. & Oswald, R.E. (1986). Acetylcholine receptor synthesis in retina and transport to optic tectum in goldfish. Science 232, 1627–1629.CrossRefGoogle ScholarPubMed
Herrick, C.J. (1925). The amphibian forebrain, III: The optic tracts and centers of Amblystoma and the frog. Journal of Comparative Neurology 39, 433–489.CrossRefGoogle Scholar
Hoffman, K-P. (1973). Conduction velocity in pathways from retina to superior colliculus in the cat: a correlation with receptive-field properties. Journal of Neurophysiology 36, 409–424.CrossRefGoogle Scholar
Hughes, T.E. (1990). A light- and electron-microscopic investigation of the optic tectum of the frog Rana pipiens, II: The neurons that give rise to the crossed tecto-bulbar pathway. Visual Neuroscience 4, 519–531.CrossRefGoogle Scholar
Hughes, T.E. & Hall, W.C. (1986). The transneuronal transport of horseradish peroxidase in the visual system of the frog (Rana pipiens). Neuroscience 17, 507–518.CrossRefGoogle ScholarPubMed
Ito, H., Vanegas, H., Murakami, T. & Morita, Y. (1984). Diameters and terminal patterns of retinofugal axons in their target areas: an HRP study in two teleosts (Sebastiscus and Navodon). Journal of Comparative Neurology 230, 179–197.CrossRefGoogle ScholarPubMed
Keyser, K.T., Hughes, T.E., Whiting, P.J., Lindstrom, J.M. & Karten, H.J. (1988). Cholinoceptive neurons in the retina of the chick: an immunohistochemical study of the nicotinic acetylcholine receptors. Visual Neuroscience 1, 349–366.CrossRefGoogle ScholarPubMed
Khalil, S.H. & Lazar, Gy. (1977). Nucleus isthmi of the frog: structure and tecto-isthmic projection. Acta Morphologica Academiae Scientiarum Hungaricae 25, 51–59.Google ScholarPubMed
Kiro, C.M. (1948). A comparative histology of the midbrain of amphibians. In Collection in Memory of A.A. Zavarzin. Moscow: U.S.S.R. Academy of Sciences Press (in Russian), pp. 54–80.Google Scholar
Knapp, H., Scalia, F. & Riss, W. (1965). The optic tracts of Rana pipiens. Acta Neurologica Scandinavica 41, 325–355.CrossRefGoogle Scholar
Kuljis, R.O. & Karten, H.J. (1988). Neuroactive peptides as markers of retinal ganglion cell populations that differ in anatomical organization and function. Visual Neuroscience 1, 73–81.CrossRefGoogle Scholar
Law, M.I. & Constantine-Paton, M. (1982). A banded distribution of retinal afferents within layer 9A of the normal frog optic tectum. Brain Research 247, 201–208.CrossRefGoogle ScholarPubMed
Lázár, G. (1978). Application of cobalt-filling technique to show retinal projections in the frog. Neuroscience 3, 725–736.CrossRefGoogle ScholarPubMed
Lázár, G. & Székely, G. (1967). Golgi studies on the optic center of the frog. Journal für Hirnforschung 9, 329–344.Google ScholarPubMed
Lázár, G. & Székely, G. (1969). Distribution of optic terminals in the different optic centers of the frog. Brain Research 16, 1–14.CrossRefGoogle ScholarPubMed
Lázár, G., Toth, P., Csank, G. & Kicliter, E. (1983). Morphology and location of tectal projection neurons in frogs: a study with HRP and cobalt filling. Journal of Comparative Neurology 215, 108–120.CrossRefGoogle ScholarPubMed
Matsumoto, D.E. & Scalia, F. (1981). Long-term survival of centrally projecting axons in the optic nerve of the frog following destruction of the retina. Journal of Comparative Neurology 202, 135–155.CrossRefGoogle ScholarPubMed
Maturana, H.R. (1958). The fine structure of the optic nerve and tectum of anurans. An electron-microscopic study. Ph.D. Thesis; Harvard University.Google Scholar
Maturana, H.R. (1959). Number of fibers in the optic nerve and the number of ganglion cells in the retina of anurans. Nature 183, 1406–1407.CrossRefGoogle ScholarPubMed
Maturana, H.R., Lettvin, J.T., 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
McIlwain, J.T. (1978). Cat superior colliculus: extracellular potentials related to W-cell synaptic actions. Journal of Neurophysiology 41, 1343–1458.CrossRefGoogle ScholarPubMed
McIlwain, J.T. & Lufkin, R.B. (1976). Distribution of direct Y-cell inputs to the cat's superior colliculus: are there spatial gradients? Brain Research 103, 133–138.CrossRefGoogle Scholar
Mize, R.R. (1983). Variations in the retinal synapses of the cat superior colliculus revealed using quantitative electron-microscopic autoradiography. Brain Research 269, 211–221.CrossRefGoogle Scholar
Mize, R.R. (1988). Immunocytochemical localization of gamma-aminobutyric acid (GABA) in the cat superior colliculus. Journal of Comparative Neurology 276, 169–187.CrossRefGoogle ScholarPubMed
Peters, A., Palay, S.L. & Webster, H.deF. (1976). The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Philadelphia: W.B. Saunders Co., p.148.Google Scholar
Potter, H.D. (1969). Structural characteristics of cell and fiber populations in the optic tectum of the frog (Rana catesbeiana). Journal of Comparative Neurology 136, 203–232.CrossRefGoogle ScholarPubMed
Potter, H.D. (1972). Terminal arborizations of retinotectal axons in the bullfrog. Journal of Comparative Neurology 144, 269–284.CrossRefGoogle ScholarPubMed
Ramón, P. (1890). Investigaciones de histologia comparada en los centros opticos de distintos vertebrados (These). In Memoria Leida Ante EI Claustro de la Facultad de Medicina de Ia Universidad Central. Madrid: G. Gutierrez, pp. 1–47.Google Scholar
Ramón, P. (1946). El cerebros de los batracios. Trabajos del Instituto Cajal de investigaciones biologicas 38, 41–111.Google Scholar
Rodieck, R.W. (1979). Visual pathways. Annual Review of Neuroscience 2, 193–225.CrossRefGoogle ScholarPubMed
Sachs, G.M. & Schneider, G.E. (1984). The morphology of optic tract axons arborizing in the superior colliculus of the hamster. Journal of Comparative Neurology 230, 155–167.CrossRefGoogle ScholarPubMed
Sargent, P.B., Pike, S.H., Nadel, D.B. & Lindstrom, J.M. (1989). Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathways, and optic tectum of the frog. Journal of Neuroscience 9, 565–573.CrossRefGoogle ScholarPubMed
Scalia, F. (1973). Autoradiographic demonstration of optic nerve fibers in the stratum zonale of the frog's tectum. Brain Research 58, 484–488.CrossRefGoogle ScholarPubMed
Scalia, F. & Colman, D.R. (1974). Aspects of the central projection of the optic nerve in the frog as revealed by anterograde migration of horseradish peroxidase. Brain Research 79, 496–504.CrossRefGoogle ScholarPubMed
Scalia, F., Knapp, H., Halpern, M. & Riss, W. (1968). New observations on the retinal projection in the frog. Brain Behavior and Evolution 1, 324–353.CrossRefGoogle Scholar
Scott, T.M. (1973). Degeneration of optic nerve terminals in the frog tectum. Journal of Anatomy (London) 114, 261–269.Google ScholarPubMed
Setalo, G. & Székely, G., (1967). The presence of membrane specializations indicative of somato-dendritic synaptic junctions in the optic tectum of the frog. Experimental Brain Research 4, 237–242.CrossRefGoogle ScholarPubMed
Stirling, R.V. & Merrill, E.G. (1987). Functional morphology of frog retinal ganglion cells and their central projections: the dimming detectors. Journal of Comparative Neurology 258, 477–495.CrossRefGoogle ScholarPubMed
Stone, J. (1983). Parallel Processing in the Visual System: The Classification of Retinal Ganglion Cells and its Impact on the Neurobiology of Vision. New York: Plenum Press.CrossRefGoogle Scholar
Straus, W. (1982). Imidazole increases the sensitivity of the cytochemical reaction for peroxidase with diaminobenzidine at a neutral pH. Journal of Histochemistry and Cytochemistry 30, 491–493.CrossRefGoogle Scholar
Sur, M. & Sherman, S.M. (1982). Retinogeniculate terminations in cats: morphological differences between X and Y cell axons. Science 218, 389–391.CrossRefGoogle ScholarPubMed
Swanson, L.W., Simmons, D.M., Whiting, P.J. & Lindstrom, J. (1987). Immunohistochemical localization of neuronal nicotinic receptors in the rodent central nervous system. Journal of Neuroscience 7, 334–342.CrossRefGoogle ScholarPubMed
Székely, G. & Lázár, G. (1976). Cellular and synaptic architecture of the optic tectum. In Frog Neurobiology, ed. Llinás, R. & Precht, W., pp. 407–433. Berlin: Springer Verlag.CrossRefGoogle Scholar
Székely, G., Setalo, G. & Lázár, G. (1973). Fine structure of the frog's optic tectum: optic fiber termination layers. Journal für Himforschung 14, 189–225.Google Scholar
Wilczynski, W. & Northcutt, R.G. (1977). Afferents to the optic tectum of the leopard frog: an HRP study. Journal of Comparative Neurology 173, 219–230.CrossRefGoogle Scholar
Witpaard, J. & TerKeurs, H.E.D.J. (1975). A reclassification of retinal ganglion cells in the frog, based upon tectal endings and response properties.Vision Research 15, 1333–1338.CrossRefGoogle ScholarPubMed
Wlassak, R. (1893). Die optischen Leitungsbahnen des Frosches. Archiv für A natomie und Physiologie, Physiologische Abtheilung (Supplement-Band), 1–28.Google Scholar