Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-26T00:26:51.891Z Has data issue: false hasContentIssue false
  • English
  • Français

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

Published online by Cambridge University Press:  02 June 2009

Thomas E. Hughes
Thomas E. Hughes
Affiliation:
Duke University Medical Centecr, Department of Anatomy, Durham
Get access Rights & Permissions [Opens in a new window]

Abstract

The superficial layers of the frog's optic tectum, Potter's (1969) layers A-G, comprise a complex neuropil made up of many afferent axons, the somata of a few neurons, and many dendrites from the neurons located in the deeper layers. Different types of retinal axons are believed to terminate in different layers (Maturana et al., 1960; Kuljis & Karten, 1988; Sargent et al., 1989), but little is known about the relationships between each type of input and the dendrites of the deep tectal neurons that extend into these superficial layers. The present study used the method of retrograde transport of horseradish peroxidase to study the synaptic contacts on the dendrites of the neurons that give rise to the crossed tecto-bulbar pathway. These cells have apical dendrites that ascend through the superficial retino-recipient layers.

The somata of the cells that give rise to the crossed tecto-bulbar pathway are located in the superficial half of layer 6, preferentially clustered along the caudal, lateral, and rostral margins of the tectum. The somata of these cells range from 8−30 ¼m in diameter. Their axons are large (2−4 ¼m in diameter) myelinated fibers that arise from either their somata or proximal dendrites. Their axons travel within the deep medullary layer to leave the tectum at the lateral margin. Their dendritic arbors extend obliquely through the superficial layers to reach layer B where they turn and extend within the layer for up to 0.5 mm. The somata of these cells receive only a scant synaptic input. In contrast, their dendrites receive input in every layer, but the nature of this input varies from layer to layer. Synaptic terminals that resemble retinal ganglion cell boutons contact the labeled dendrites in layers B, F, and G. This indicates that the dendrites may receive monosynaptic input from several types of retinal ganglion cells. Terminals with small, flattened vesicles also contact the dendrites of these cells in each layer. In layer F and below, the terminals with flattened vesicles constitute 15% of the contacts; above layer F they constitute only 5−8% of the contacts. Terminals with medium-sized, flattened vesicles also contact the dendrites of these cells in every layer and constitute a large proportion of their input (33−95%). The latter terminals resemble those that are often postsynaptic to retinal terminals.

Keywords

Horseradish peroxidaseMorphologySynapsesLaminae
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 6 , June 1990 , pp. 519 - 531
Copyright
Copyright © Cambridge University Press 1990

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

Adams, J.C. (1977). Technical considerations on the use of HRP as a neuronal marker. Neuroscience 2, 141–145.CrossRefGoogle Scholar
Antal, M., Matsumoto, N. & Székely, G. (1986). Tectal neurons of the frog: intracellular recording and labeling with cobalt electrodes. Journal of Comparative Neurology 246, 238–253.CrossRefGoogle ScholarPubMed
Ariëns Kappers, C.U., Huber, G.C. & Crosby, E.C. (1967). The Comparative Anatomy of the Nervous System of Vertebrates, Including Man. New York: Hafner.Google Scholar
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, 251–260.CrossRefGoogle ScholarPubMed
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, 455–460.CrossRefGoogle ScholarPubMed
Behan, M., Appel, P.P. & Graper, M.J. (1989). Ultrastructural study of large efferent neurons in the superior colliculus of the cat after retrograde labeling with horseradish peroxidase. Journal of Comparative Neurology 270, 171–184.CrossRefGoogle Scholar
Castiglioni, A.J., Gallaway, M.C. & Coulter, J.D. (1978). Spinal projections from the midbrain of the monkey. Journal of Comparative Neurology 178, 329–346.CrossRefGoogle ScholarPubMed
Chalupa, L.M. (1984). Visual physiology of the mammalian superior colliculus. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 775–818. New York: Plenum Press.CrossRefGoogle Scholar
Contestabile, A. (1976). Comparative survey on enzyme localization, ultrastructural arrangement, and functional organization in the optic tectum of nonmammalian vertebrates. Experientia (Basel) 32, 1223–1229.CrossRefGoogle Scholar
Contestabile, A. & Mussoni, I. (1976). Histochemical remarks on monoamine oxidase and acetylcholinesterase in some regions of amphibian brain. Experientia (Basel) 32, 94–96.CrossRefGoogle ScholarPubMed
Dacey, D.M. & Ulinski, P.S. (1986 a). Optic tectum of the Eastern garter snake, Thamnophis sirtalis, I: Efferent pathways. Journal of Comparative Neurology 245, 1–28.CrossRefGoogle ScholarPubMed
Dacey, D.M. & Ulinski, P.S. (1986 b). Optic tectum of the Eastern garter snake, Thamnophis sirtalis, II: Morphology of efferent cells. Journal of Comparative Neurology 245, 198–237.CrossRefGoogle ScholarPubMed
Desan, P.H., Gruberg, E.R., Grewell, K.M. & Eckenstein, F. (1987). Cholinergic innervation of the optic tectum in the frog (Rana pipiens). Brain Research 413, 344–349.CrossRefGoogle ScholarPubMed
Ebbesson, S.O.E. (1981). Projections of the optic tectum and the mesencephalic nucleus of the trigeminal nerve in the tegu lizard (Tupinambis nigropunctatus). Cell and Tissue Research 216, 151–165.CrossRefGoogle ScholarPubMed
Edwards, S.B. (1980). The deep cell layers of the superior colliculus: their reticular characteristics and structural organization. In The Reticular Formation Revisited, ed. Hobson, J.A. & Brazier, M.A.B., pp. 193–209. New York: Raven Press.Google Scholar
Edwards, S.B. & Henkel, C.K.. (1978). Superior colliculus connections with the extraocular motor nuclei in the cat. Journal of Comparative Neurology 179, 451–468.CrossRefGoogle ScholarPubMed
Ewert, J.-P. (1967 a). Aktivierung der verhaltensfolge beim beutefang der erdkrote (Bufo bufo L.) durch elektrische mittelhirnreizung. Zeitschrift für Vergleichende Physiologie 54, 455–481.CrossRefGoogle Scholar
Ewert, J.-P. (1967 b). Elektrische reizung des retinalen projektionsfeldes im mittelhirn der erdkrote (Bufo bufo L.). Pflugers Archive für die Gesamte Physiologie des Menschen und der Tiere 295, 90–98.CrossRefGoogle ScholarPubMed
Finkenstädt, Th., Ebbesson, S.O.E. & Ewert, J.P. (1983). Projections to the midbrain tectum in Salamandra salamandra. Cell and Tissue Research 234, 39–55.CrossRefGoogle Scholar
Foster, R.E. & Hall, W.C. (1975). The connections and laminar organization of the optic tectum in a reptile (Iguana iguana). Journal of Comparative Neurology 163, 397–426.CrossRefGoogle Scholar
Gaupp, E. (1899). Ecker's, A. & Wiedersheim, 's Anatomie des Frosches, Zweite Abteilung. Lehre vom Nervensystem. Braunschweig: R. Vieweg, 548 pp.Google Scholar
Grace, A.A. & Linás, R. (1985). Morphological artifacts induced in intracellularly stained neurons by dehydration: circumvention using rapid dimethyl sulfoxide clearing. Neuroscience 16, 461–475.CrossRefGoogle ScholarPubMed
Grobstein, P., Comer, C. & Kostyk, S.K. (1983). Frog prey capture behavior: between sensory maps and directed motor output. In Advances in Vertebrate Neuroethology, ed. Ewert, J.-P., Capranica, R.R. & Ingle, D.J., pp. 211–246. New York: Plenum Press.Google Scholar
Gruberg, E.R. & Lettvin, J.Y. (1980). Anatomy and physiology of a binocular system in the frog (Rana pipiens). Brain Research 192, 313–325.CrossRefGoogle ScholarPubMed
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
Grüsser, O.-J. & Grüsser-Cornehls, U. (1976). Neurophysiology of the anuran visual system. In Frog Neurobiology, ed. Llinás, R. & Precht, W., pp. 297–385. New York: Springer-Verlag.CrossRefGoogle Scholar
Hall, W.C. & May, P.J. (1983). The anatomical basis for sensorimotor transformation in the superior colliculus. In Contributions to Sensory Physiology, Vol. 8, ed. Neff, W.D., pp. 1–40. New York: Academic Press.Google Scholar
Herrick, C.J. (1925). The amphibian forebrain, III: The optic tract and centers of Amblystoma and the frog. Journal of Comparative Neurology 36, 433–489.CrossRefGoogle Scholar
Herrick, C.J. (1948). The Brain of the Tiger Salamander. Illinois: University of Chicago Press.Google Scholar
Huerta, M.F. & Harting, J.K. (1984). The mammalian superior colliculus: studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 687–774. New York: Plenum Press.CrossRefGoogle Scholar
Hughes, T.E. (1990) A light- and electron-microscopic investigation of the optic tectum of the frog, Rana pipiens, I: The retinal axons. Visual Neuroscience 4, 499–518.CrossRefGoogle ScholarPubMed
Hughes, T.E., Ingle, D.J. & Hall, W.C. (1984). The relationship between the optic nerve fibers and tectal efferent cells in the optic tectum of Rana pipiens. Society for Neuroscience Abstracts 10, 61.Google 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
Ingle, D.J. (1982). Organization of visuomotor behavior in vertebrates. In Analysis of Visual Behavior, ed. Ingle, D.J., Goodale, M.A. & Mansfield, R.J.M., pp. 67–109. Cambridge: MIT Press.Google Scholar
Karten, H.J. (1965). Projections of the optic tecturn of the pigeon (Columba livia). Anatomical Record 151, 369.Google 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
Lázár, G. (1969). Efferent pathways of the optic tectum in the frog. Acta Biologica Academiae Scientiarum Hungaricae 20, 171–183.Google 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., 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
Lettvin, J.Y., Maturana, H.R., Pitts, W.H. & McCulloch, W.S. (1961). Two remarks on the visual system of the frog. In Sensory Communication, ed. Rosenblith, W.A., pp. 757–776. Cambridge, Massachusetts: MIT Press.Google Scholar
Lu, S.M., Lin, C.-S., Behan, M., Cant, N.B. & Hall, W.C. (1985). Glutamate decarboxylase immunoreactivity in the intermediate grey layer of the superior colliculus in the cat. Neuroscience 16, 123–131.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
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
May, P.J. & Hall, W.C. (1984). Relationships between the nigrotectal pathway and the cells of origin of the predorsal bundle. Journal of Comparative Neurology 226, 357–376.CrossRefGoogle ScholarPubMed
McDonald, J.W., Cline, H.T., Constantine-Paton, M., Maragos, W.F., Johnston, M.V. & Young, A.B. (1989). Quantitative auto-radiographic localization of NMDA, QuisQualte, and PCP receptors in the frog tectum. Brain Research 482, 155–158.CrossRefGoogle Scholar
McIlwain, J.T. (1975). Visual receptive fields and their images in superior colliculus of the cat. Journal of Neurophysiology 38, 219–230.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1982). Lateral spread of neural excitation during microstimulation in intermediate gray layer of cat's superior colliculus. Journal of Neurophysiology 47, 167–178.CrossRefGoogle Scholar
McIlwain, J.T. & Berson, D.M. (1982). Retinal y-cell activation of deep-layer cells in superior colliculus of the cat. Journal of Neurophysiology 47, 700–714.Google Scholar
Mooney, R.D., Klein, B.G. & Rhoades, R.W. (1985). Correlations between the structural and functional characteristics of the neurons in the superficial laminae and the hamster's superior colliculus. Journal of Neuroscience 11, 2989–3009.CrossRefGoogle Scholar
Moschovakis, A.K. & Karabelas, A.B. (1985). Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus. Journal of Comparative Neurology 239, 276–308.CrossRefGoogle ScholarPubMed
Moschovakis, A.K., Krabelas, A.B. & Hjghstein, S.M. (1988). Structure-function relationships in the primate superior colliculus, 1: Morphological classification of efferent neurons. Journal of Neurophysiology 60, 232–262.CrossRefGoogle ScholarPubMed
Murray, E.A. & Coulter, J.D. (1982). Organization of tectospinal neurons in the cat and rat superior colliculus. Brain Research 243, 210–214.CrossRefGoogle Scholar
Northcutt, R.G. (1983). Evolution of the optic tectum in ray-finned fishes. In Fish Neurobiology, Vol. 2, ed. Davis, R.E. & Northcutr, R.G., pp. 1–42. Ann Arbor: University of Michigan Press.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
Redgrave, P., Odekunle, A. & Dean, P. (1986). Tectal cells of origin of predorsal bundle in rat: location and segregation from ipsilateral descending pathway. Experimental Brain Research 63, 279–293.CrossRefGoogle ScholarPubMed
Reiner, A. & Karten, H.J. (1982). Laminar distribution of the cells of origin of the descending tectofugal pathways in the pigeon (Columba livia). Journal of Comparative Neurology 204, 165–187.CrossRefGoogle ScholarPubMed
Rhoades, R.D. & Dellacroce, D.R. (1980). Cells of origin of the tectospinal tract in the golden hamster: an anatomical and electrophysiological investigation. Experimental Neurology 67, 163–180.CrossRefGoogle ScholarPubMed
Rhoades, R.W., Mooney, R.D., Klein, B.G., Jacquen, M.F., Szczepanik, A.M. & Chiaia, N.L. (1986). The structural and functional characteristics of tectospinal neurons in the golden hamster. Journal of Comparative Neurology 255, 451–465.CrossRefGoogle Scholar
Rubinson, K. (1968). Projections of the tectum opticum of the frog. Brain Behavior and Evolution 1, 529–561.CrossRefGoogle Scholar
Sargent, P.B., Pike, S.H., Nadel, D.B. & Lindstrom, J.M. (1989). Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathway, and optic tectum of the frog. Journal of Neuroscience 9, 565–573.CrossRefGoogle ScholarPubMed
Schroeder, D.M. (1981). Tectal projections of an infrared sensitive snake (Crotalus viridis). Journal of Comparative Neurology 195, 447–500.Google ScholarPubMed
Scott, T.M. (1973). Degeneration of optic nerve terminals in the frog tectum. Journal of Anatomy 114, 261–269.Google ScholarPubMed
Sereno, M.I. (1985). Tectoreticular pathways in the turtle, Pseudemys scripta, I: Morphology of tectoreticular axons. Journal of Comparative Neurology 233, 48–90.CrossRefGoogle ScholarPubMed
Sereno, M.I. & Ulinski, P.S. (1985). Tectoreticular pathways in the turtle, Pseudemys scripta, II: Morphology of tectoreticular cells. Journal of Comparative Neurology 233, 91–114.CrossRefGoogle ScholarPubMed
Shen, S.C., Greenfield, P. & Boell, E.J. (1955). The distribution of cholinesterase in the frog brain. Journal of Comparative Neurology 102, 717–743.CrossRefGoogle ScholarPubMed
Smeets, W.J.A.J. (1981). Efferent tectal pathways in two chondrichthyans, the shark Scyliorhinus conicula and the ray Raja clavata. Journal of Comparative Neurology 195, 13–24.CrossRefGoogle Scholar
Sood, P.P. (1978). Chemo-architectonics of the optic tectum of the frog (Rana tigrina). Cellular and Molecular Biology 23, 195–206.Google 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
Székely, G., Setalo, G. & Lázár, G. (1973). Fine structure of the frog's optic tectum: optic fiber termination layers. Journal für Hirnforschung 14, 189–225.Google Scholar
Ten Donkeilaar, H.J.. (1976). Descending pathways from the brain stem to the spinal cord in some reptiles, II: Course and site of termination. Journal of Comparative Neurology 167, 443–464.CrossRefGoogle Scholar
Ulinski, P.S. (1977). Tectal efferents in the banded water snake (Natrix sipedon). Journal of Comparative Neurology 173, 251–274.CrossRefGoogle ScholarPubMed
Welker, E., Hoogland, P.V. & Lohman, A.H.M. (1983). Tectal connections in Python reticulatus. Journal of Comparative Neurology 220, 347–354.CrossRefGoogle ScholarPubMed
Wilczynski, W. & Northcutt, R.G. (1977). Afferents to the optic tectum in the leopard frog: An HRP study. Journal of Comparative Neurology 173, 219–229.CrossRefGoogle Scholar