Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-27T22:22:59.377Z Has data issue: false hasContentIssue false

Cat-301 antibody selectively labels neurons in the Y-innervated laminae of the cat superior colliculus

Published online by Cambridge University Press:  02 June 2009

R. Ranney Mine
Affiliation:
Department of Anatomy and Neurobiology, College of Medicine, University of Tennessee Health Science Center, Memphis
Susan Hockfield
Affiliation:
Section on Neuroanatomy, Yale University, New Haven

Abstract

Cat-301 is a monoclonal antibody which recognizes a cell surface associated antigen of selected neurons in the central nervous system (CNS). In the visual system, cat-301 selectively labels Y-like cells in several visual structures, including portions of the lateral geniculate nucleus complex and visual cortex. The cat superior colliculus (SC) also receives Y input and contains cells driven by Y input which are selectively distributed in the deep superficial gray and deeper laminae. If cat-301 is selective to the Y-cell system in SC, labeled cells should be restricted to those laminae. To test this hypothesis, we have examined quantitatively the laminar distribution, percentage, size, and morphology of cells in SC labeled by the cat-301 antibody. Cat-301 labeled a variety of cells in the cat SC. Labeled cells were found within the deep portion of the superficial gray layer (6.6%), optic layer (27.6%), intermediate gray layer (26.9%), and the deep gray and white layers (38.5%). By contrast, only 2 of 667 labeled cells (0.3%) were found within that part of the upper superficial gray layer innervated exclusively by W input and thought to contain only W-driven cells. When considered as a percentage of the total cell population, cat-301 labeled cells represented less than 3% of cells in the superficial gray layer and approximately 15% in the deeper layers. Neurons labeled by cat-301 were all of medium to large size (mean average diameter = 33.3μm; range = 15–84μm) and included vertical fusiform and stellate cells in the upper layers and the very large neurons found in the intermediate gray and deeper layers. These results provide further evidence that the cat-301 antibody selectively recognizes the Y channel of the cat visual system.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1989

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

Abramson, B.P. & Chalupa, L.M. (1988). Multiple pathways from the superior colliculus to the extrageniculate visual thalamus of the cat. Journal of Comparative Neurology 271, 397418.Google Scholar
Beckstead, R.M. & Frankfurter, A. (1983). A direct projection from the retina to the intermediate gray layer of the superior colliculus demonstrated by anterograde transport of horseradish peroxidase in monkey, cat, and rat. Experimental Brain Research 52, 261268.Google Scholar
Behan, M. (1981). Identification and distribution of retinocollicular terminals in the cat: an electron microscopic autoradiographic analysis. Journal of Comparative Neurology 199, 115.CrossRefGoogle Scholar
Behan, M. (1984). An EM-autoradiographic analysis of the projection from cortical areas 17, 18, and 19 to the superior colliculus in the cat. Journal of Comparative Neurology 225, 591604.CrossRefGoogle Scholar
Berson, D.M. (1985). Cat lateral suprasylvian cortex: Y-cell inputs and corticotectal projection. Journal of Neurophysiology 53, 544556.CrossRefGoogle ScholarPubMed
Berson, D.M. (1987). Retinal W-cell input to the upper superficial gray layer of the cat's superior colliculus; a conduction-velocity analysis. Journal of Neurophysiology 58, 10351051.CrossRefGoogle Scholar
Berson, D.M. (1988). Convergence of retinal W-cell and corticotectal input to cells of the cat superior colliculus. Journal of Neurophysiology 60, 18611873.Google Scholar
Berson, D.M. & McIlwain, J.T. (1982). Retinal Y-cell activation of deep-layer cells in superior colliculus of the cat. Journal of Neurophysiology 47, 700714.CrossRefGoogle ScholarPubMed
Berson, D.M. & McIlwain, J.T. (1983). Visual cortical inputs to deep layers of cat's superior colliculus. Journal of Neurophysiology 50, 11431155.CrossRefGoogle ScholarPubMed
Bowling, D.B. & Michael, C.R. (1980). Projection patterns of single physiologically characterized optic tract fibers in cat. Nature 286, 899902.Google Scholar
Caldwell, R.B. & Mize, R.R. (1981). Superior colliculus neurons which project to the cat lateral posterior nucleus have varying morphologies. Journal of Comparative Neurology 203, 5366.Google Scholar
Crabtree, J.W., Spear, P.D., McCall, M.A., Jones, K.R. & Kornguth, S.E. (1986). Contributions of Y- and W-cell pathways to response properties of cat superior colliculus neurons: comparison of antibody- and deprivation-induced alterations. Journal of Neurophysiology 56, 11571173.Google Scholar
Fitzpatrick, D., Penny, G.R. & Schmechel, D.E. (1984). Glutamic acid decarboxylase-immunoreactive neurons and terminals in the lateral geniculate nucleus of the cat. Journal of Neuroscience 4, 18091829.Google Scholar
Freeman, B. & Singer, W. (1983). Direct and indirect visual inputs to superficial layers of cat superior colliculus: a current source-density analysis of electrically evoked potentials. Journal of Neurophysiology 49, 10751091.Google 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, 749772.CrossRefGoogle Scholar
Garey, L.J., Jones, E.G. & Powell, T.P.S. (1968). Interrelationships of striate and extrastriate cortex with the primary relay sites of the visual pathway. Journal of Neurology, Neurosurgery, and Psychiatry 31, 135157.Google ScholarPubMed
Grantyn, R., Grantyn, A. & Schierwagen, A. (1983). Passive membrane properties, afterpotentials, and repetitive firing of superior colliculus neurons studied in the anesthetized cat. Experimental Brain Research 50, 377391.Google ScholarPubMed
Graybiel, A.M. (1975). Anatomical organization of retinotectal afferents in the cat: an autoradiographic study. Brain Research 96, 123.Google Scholar
Gurski, M.R., Beitz, A.J., Madl, J.E. & Mize, R.R. (1987). Localization of glutamate in the cat superior colliculus: an immunocytochemical study. Investigative Ophthalmology and Visual Science (Suppl.) 28, 21.Google Scholar
Harrell, J.V., Caldwell, R.B. & Mize, R.R. (1982). The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat. Experimental Brain Research 46, 234242.Google Scholar
Harting, J.K. & Guillery, R.W. (1976). Organization of retinocollicular pathways in the cat. Journal of Comparative Neurology 166, 133144.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Hockfield, S., Jones, E.G. & McKay, R. (1984). Monoclonal antibody that identifies subsets of neurones in the central visual system of monkey and cat. Nature 307, 267269.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G., Hockfield, S. & McKay, R.D.G. (1988). Neuronal populations stained with the monoclonal antibody cat-301 in the mammalian cerebral cortex and thalamus. Journal of Neuroscience 8, 518542.Google Scholar
Hockfield, S. & McKay, R. (1983). A surface antigen expressed by a subset of neurons in the vertebrate CNS. Proceedings of the National Academy of Sciences of the U.S.A. 80, 57585761.Google Scholar
Hockfield, S., McKay, R.D., Hendry, S.H.C. & Jones, E.G. (1983). A surface antigen that identifies ocular dominance columns in the visual cortex and laminar features of the lateral geniculate nucleus. Cold Spring Harbor Symposia 48, 877889.Google Scholar
Hoffmann, 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, 409424.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. 687773. New York: Plenum Press.CrossRefGoogle Scholar
Itoh, K., Conley, M. & Diamond, I.T. (1981). Different distributions of large and small ganglion cells in the cat after HRP injections of single layers of the lateral geniculate body and the superior colliculus. Brain Research 207, 147152.CrossRefGoogle ScholarPubMed
Kawamura, S. & Kobayrashi, E. (1975).Identification of laminar origin of some tecto-thalamic fibers in the cat. Brain Research 91, 281285.Google Scholar
Kawamura, K., Sprague, J.M. & Niimi, K. (1974). Corticofugal projections from the visual cortices to the thalamus, pretectum, and superior colliculus in the cat. Journal of Comparative Neurology 158, 339362.Google Scholar
Kawamura, S., Fukushima, N., Hattori, S. & Kudo, M. (1980). Laminar segregation of cells of origin of ascending projections from the superficial layers of the superior colliculus. Brain Research 184, 486490.Google Scholar
Macavoy, M.G., Hockfield, S. & Sur, M. (1985). Development of antigen expression in a possible Y-cell pathway through the cat lateral geniculate nucleus and visual cortex. Neuroscience Abstracts 11, 224.Google Scholar
McIlwain, J.T. (1978). Cat superior colliculus: extracellular potentials related to W-cell synaptic actions. Journal of Neurophysiology 41, 13431358.Google Scholar
McIlwain, J.T. & Fields, H.L. (1971). Interactions of cortical and retinal projections on single neurons of the cat's superior colliculus. Journal of Neurophysiology 34, 763772.Google Scholar
McIlwain, J.T. & Lufkin, R.M. (1976). Distribution of direct Y-cell inputs to the cat's superior colliculus: are there spatial gradients? Brain Research 103, 133138.Google Scholar
Mize, R.R. (1983 a). Variations in the retinal synapses of the cat superior colliculus revealed using quantitative electron microscope autoradiography. Brain Research 269, 211221.Google Scholar
Mize, R.R. (1983 b). Patterns of convergence and divergence of retinal and cortical synaptic terminals in the cat superior colliculus. Experimental Brain Research 51, 8896.Google Scholar
Mize, R.R. (1985 a). A microcomputer plotter for use with light and electron microscopes. In The Microcomputer in Cell and Neurobiology Research, ed. Mize, R.R., pp. 111134. New York: Elsevier Science Publishers.Google Scholar
Mize, R.R. (1985 b). Morphometric measurement using a computerized digitizing system. In The Microcomputer in Cell and Neurobiology Research, ed. Mize, R.R., pp. 177216. New York: Elsevier Science Publishers.Google Scholar
Mize, R.R. (1988). Immunocytochemical localization of gamma-aminobutyric acid (GABA) in the cat superior colliculus. Journal of Comparative Neurology 276, 169187.Google Scholar
Mize, R.R. (1989). Enkephalin-like immunoreactivity in the cat superior colliculus: distribution, ultrastructure, and co-localization with GABA. Journal of Comparative Neurology 285, 133155.Google Scholar
Mize, R.R. & Horner, L.H. (1984). Retinal synapses of the cat medial interlaminar nucleus and ventral lateral geniculate nucleus differ in size and synaptic organization. Journal of Comparative Neurology 224, 579590.Google Scholar
Mize, R.R. & White, D.A. (1989). [3H]-muscimol labels neurons in both the superficial and deep layers of cat superior colliculus. Neuroscience Letters 104, 3137.Google Scholar
Mize, R.R., Spencer, R.F. & Sterling, P. (1981). Neurons and glia in cat superior colliculus accumulate [3H]-gamma-aminobutyric acid (GABA). Journal of Comparative Neurology 202, 385396.Google Scholar
Mize, R.R., Spencer, R.F. & Sterling, P. (1982). Two types of GABA-accumulating neurons in the superficial gray layer of the cat superior colliculus. Journal of Comparative Neurology 206, 180192.Google Scholar
Mize, R.R., Spencer, R.F. & Horner, L.H. (1986). Quantitative comparison of retinal synapses in the dorsal and ventral (parvicellular) C laminae of the cat dorsal lateral geniculate nucleus. Journal of Comparative Neurology 248, 5773.CrossRefGoogle ScholarPubMed
Nagata, T. & Hayashi, Y. (1978). Innervation by W-type retinal ganglion cells of colliculus neurons projecting to pulvinar nuclei in cats. Experientia 35, 336338.CrossRefGoogle Scholar
Ogawa, T. & Takahashi, Y. (1981). Retinotectal connectivities within the superficial layers of the cat's superior colliculus. Brain Research 217, 111.Google Scholar
Rowe, M.H. & Stone, J. (1977). Naming of neurons: classification and naming of cat retinal ganglion cells. Brain, Behavior, and Evolution 14, 185216.Google Scholar
Segal, R.L. & Beckstead, R.M. (1984). The lateral suprasylvian corticotectal projection in cats. Journal of Comparative Neurology 225, 259275.Google Scholar
Sherman, S.H., Kass, J.H. & Webb, S.V. (1976). W and Y cells in the dorsal lateral geniculate nucleus of owl monkey (Aotus trivirgatus). Science 192, 475477.CrossRefGoogle Scholar
Sherman, S.M. & Spear, P.D. (1982). Organization of visual pathways in normal and visually deprived cats. Physiological Reviews 62, 738855.CrossRefGoogle ScholarPubMed
Sterling, P. (1971). Receptive fields and synaptic organization of the superficial gray layer of the cat superior colliculus. Vision Research (Suppl.) 3, 309328.Google Scholar
Sur, M., Hockfield, S., Macavoy, M., Garraghty, P., Kritzer, M. & McKay, R. (1984). A monoclonal antibody that may identify Y cells in the cat lateral geniculate nucleus. Society for Neuroscience Abstracts 10, 297.Google Scholar
Sur, M., Frost, D.O. & Hockfield, S. (1988). Expression of a surfaceassociated antigen on Y cells in the cat lateral geniculate nucleus is regulated by visual experience. Journal for Neuroscience 8, 874882.CrossRefGoogle Scholar
Updyke, B.V. (1977). Topographic organization of the projections from cortical areas 17, 18, and 19 onto the thalamus, pretectum, and superior colliculus in the cat. Journal of Comparative Neurology 173, 81122.Google Scholar
Van Essen, D. & Maunsell, J. (1983). Hierarchical organization and functional streams in the visual cortex. Trends in Neuroscience 6, 370375.Google Scholar
Zaremba, S., Waldvogel, E. & Hockfield, S. (1985). Monoclonal antibody cat-301: recognition of a surface antigen on subsets of cells in human central visual areas and biochemical purification of the antigen from guinea pig brain. Society for Neuroscience Abstracts 11, 1106.Google Scholar
Zaremba, S., Guimaraes, A., Kalb, R.G. & Hockfield, S. (1989). Characterization of an activity-dependent, neuronal surface proteoglycan identified with monoclonal antibody cat-301. Neuron 2, 12071219.Google Scholar