Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-26T20:06:20.727Z Has data issue: false hasContentIssue false
  • English
  • Français

Subdivisions of the visual system labeled with the Cat-301 antibody in tree shrews

Published online by Cambridge University Press:  02 June 2009

Neeraj Jain ,
Todd M. Preuss  and
Jon H. Kaas
Neeraj Jain
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Todd M. Preuss
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Jon H. Kaas
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Get access Rights & Permissions [Opens in a new window]

Abstract

The monoclonal antibody Cat-301 was used to stain neurons and neuropil in the visual thalamus and cortex of tree shrews —small, highly visual mammals that are closely related to primates. Previously, this antibody has been found to label neurons associated with the Y-cell stream of processing in cats and the magnocellular or M-cell stream in macaque monkeys. In tree shrews, the antibody selectively labeled layers 1, 2, 4, and 5 of the dorsal lateral geniculate nucleus, layers that are likely to contain neurons previously classified as Y-cells. Of the two layers that contain W-cells, layer 3 was unlabeled and layer 6 was lightly labeled. In area 17, layer 3c was densely stained, as in cats and macaque monkeys. The external half of layer 5 was also densely stained, in contrast to cats where the internal half of layer 5 is stained and macaques where layer 5 is sparsely stained. Area 18 was characterized by dense, uniform staining of inner layer 3 and outer layer 5, but no pattern of alternating light and dense bands crossed the width of area 18 as in macaques. Dense labeling of these same sublayers occurred in cortical areas TA and TD just lateral to area 18. Area TD may be the homologue of area MT of primates, which also stains densely with Cat-301 in macaques. These results indicate that Cat-301 differentially labels layers and areas in the visual system of tree shrews, and raise intriguing issues of comparison among tree shrews, primates, and cats.

Keywords

TupaiaStriate cortexExtrastriate cortexLateral geniculate nucleusPrimate
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 4 , July 1994 , pp. 731 - 741
Copyright
Copyright © Cambridge University Press 1994

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

Berman, N.E.J. & Payne, B.R. (1989). Modular organization of On and Off responses in the cat lateral geniculate nucleus. Neuroscience 32, 721–737.Google Scholar
Bowling, D.B. & Caverhill, J.I. (1989). On/Off organization in cat lateral geniculate nucleus sublaminae vs. columns. Journal of Comparative Neurology 283, 161–168.Google Scholar
Brodmann, K. (1909). Vergleichende Lokelisationlehre der Grosshirnrinde in ihren Prinzipien daegestellt auf Grund des Zellenbaues. Leipzig: J.A.Barth.Google Scholar
Bullier, J. & Henry, G.H. (1979). Laminar distribution of first order neurons and afferent terminals in cat striate cortex. Journal of Neurophysiology 42, 1271–1281.Google Scholar
Campbell, C.B.G. (1966). The relationships of the tree shrews. The evidence of the nervous system. Evolution 20, 276–281.Google Scholar
Casagrande, V.A., Guillery, R.W. & Harting, J.K. (1978). Differential effects of monocular deprivation seen in different layers of the lateral geniculate nucleus. Journal of Comparative Neurology 179, 469–486.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Norton, T.T. (1991). Lateral geniculate nucleus: A review of its physiology and function. In Electrophysiology of Vision, ed. Leventhal, A.G., pp. 41–84. London: MacMillon Press.Google Scholar
Casagrande, V.A. & Kaas, J.H. (1994). The afferent, intrinsic and efferent connections of primary visual cortex in primates. In Cerebral Cortex, Vol 10, Primary Visual Cortex in Primates, ed. Peters, A. & Rockland, K. (in press).Google Scholar
Casseday, J.H., Jones, D.R. & Diamond, I.T. (1979). Projection from the cortex to tectum in the tree shrew, Tupaia glis. Journal of Comparative Neurology 185, 253.Google Scholar
Clark, W.E. Le Gros (1959). The Antecedents of Man. Edinburgh: Edinburgh University Press.Google Scholar
Conley, M., Fitzpatrick, D. & Diamond, I.T. (1984). The laminar organization of the lateral geniculate body and the striate cortex in the tree shrew (Tupaia glis). Journal of Neuroscience 4, 171–197.Google Scholar
Conley, M. & Friederich-Ecsy, B. (1993). Functional organization of the ventral lateral geniculate complex of the tree shrew (Tupaia belangeri): II. Connections with the cortex, thalamus and brain stem. Journal of Comparative Neurology 328, 21–42.Google Scholar
Conway, J.L. & Schiller, P.H. (1983). Laminar organization of tree shrew dorsal lateral geniculate nucleus. Journal of Neurophysiology 50, 1330–1342.Google Scholar
Cronin, J.E. & Sarich, V.M. (1980). Tupaiid and archonta phylogeny: The macromolecular evidence. In Comparative Biology and Evolutionary Relationships of Tree Shrews, ed. Luckett, W.P., pp. 293–312. New York: Plenum Press.Google Scholar
Cusick, C.G., Gould, H.J. III & Kaas, J.H. (1984). Interhemispheric connections of visual cortex of owl monkeys (Aotus trivirgatus), marmosets (Callithrix jacchus) and galagos (Galago crassicaudatus). Journal of Comparative Neurology 230, 311–336.Google Scholar
Cusick, C.G., MacAvoy, M.G. & Kaas, J.H. (1985). Interhemispheric connections of cortical sensory areas in tree shrews. Journal of Comparative Neurology 235, 111–128.CrossRefGoogle ScholarPubMed
DeYoe, E.A. & Van Essen, D.C. (1985). Segregation of efferent connections and receptive-field properties in visual area V2 of the macaque. Nature 317, 58–71.Google Scholar
DeYoe, E.A. & Van Essen, D.C. (1988). Concurrent processing streams in monkey visual cortex. Trends in Neurosciences 11, 219–226.Google Scholar
DeYoe, E.A., Hockfield, S., Garren, H. & Van Essen, D.C. (1990). Antibody labeling of functional subdivisions in visual cortex: Cat-301 immunoreactivity in striate and extrastriate cortex of the macaque monkey. Visual Neuroscience 5, 67–81.CrossRefGoogle ScholarPubMed
Diamond, I.T. & Hall, W.C. (1969). Evolution of neocortex. Science 164, 251–262.Google Scholar
Diamond, I.T., Conley, M., Itoh, K. & Fitzpatrick, D. (1985). Laminar organization of geniculo-cortical projections in Galago senegalensis and Aotus trivirgatus. Journal of Comparative Neurology 242, 584–610.CrossRefGoogle Scholar
Dreher, B., Fukuda, Y. & Rodieck, R.W. (1976). Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of Old-World primates. Journal of Physiology (London) 258, 433–452.Google Scholar
Economo, C. von, & Koskinas, C.N. (1925). Die Cytoarchetektonik der Hirnrinde des erwachsene Menschen. Berlin: Springer.Google Scholar
Ferster, D. & LeVay, S. (1978). The axonal arborisations of lateral geniculate neurons in the striate cortex of the cat. Journal of Comparative Neurology 182, 923–944.CrossRefGoogle ScholarPubMed
Gallyas, F. (1979). Silver staining of myelin by means of physical development. Neurological Research 1, 203–209.Google Scholar
Garey, L.J. (1971). A light and electron microscopic study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proceedings of the Royal Society B (London) 179, 41–63.Google Scholar
Guimaraes, A., Zaremba, S. & Hockfield, S. (1990). Molecular and morphological changes in the cat lateral geniculate nucleus and visual cortex induced by visual deprivation are revealed by monoclonal antibodies Cat-304 and Cat-301. Journal of Neuroscience 16, 3014–3024.CrossRefGoogle Scholar
Hassler, R. (1966). Comparative anatomy of the central visual system in day and night active primates. In Evolution of the Forebrain, ed. Hassler, R. & Stephan, H., pp. 419–434. Stutart: Thieme.CrossRefGoogle Scholar
Hendry, S.H.C., Hockfield, S., Jones, E.G. & McKay, R. (1984). Monoclonal antibody that identifies subset of neurons in the central visual system of monkey and cat. Nature 307, 267–269.Google Scholar
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, 518–542.Google Scholar
Henry, G.H. (1991). Afferent inputs, receptive field properties and morphological cell types in different layers. In Visual and Visual Dys function, Vol. 4, The Neural Basis of Visual Function, ed. Leventhal, A.G., pp. 223–240. London: MacMillon Press.Google Scholar
Hockfield, S. & McKay, R.D.G. (1983). A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proceedings of the National Academy of Sciences of the U.S.A. 80, 5758–5761.CrossRefGoogle ScholarPubMed
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 Symposium on Quantitative Biology 48, 877–889.Google Scholar
Hockfield, S. & Sur, M. (1990). Monoclonal antibody Cat-301 identifies Y-cells in the dorsal lateral geniculate nucleus of the cat. Journal of Comparative Neurology 300, 320–330.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Livingstone, M.S. (1987). Segregation of form, color and stereopsis in primate area 18. Journal of Neuroscience 7, 3378–3415.Google Scholar
Jain, N., Preuss, T.M. & Kaas, J.H. (1993). Distribution of Cat-301 immunoreactivity in visual cortex and lateral geniculate of tree shrews. Society for Neuroscience Abstracts 19, 332.Google Scholar
Kaas, J.H., Hall, W.C., Killackey, H. & Diamond, l.T. (1972). Visual cortex of the tree shrew (Tupaia glis): Architectonic subdivisions and representations of the visual field. Brain Research 42, 491–496.CrossRefGoogle ScholarPubMed
Kaas, J.H. & Krubitzer, L.A. (1991). The organization of extrastriate visual cortex. In Neuroanatomy of Visual Pathways and their Retinotopic Organization, Vision and Visual Dysfunction, Vol. 3, ed. Dreher, B. & Robinson, S.R., pp. 302–359. London: MacMillon Press.Google Scholar
Kaas, J.H. & Preuss, T.M. (1993). Archonton affinities as reflected in the visual system. In Mammalian Phylogeny, ed. Szalay, F., Novacek, M. & McKenna, M., pp. 115–128. New York: Springer Verlag.Google Scholar
Kaplan, E. & Shapley, R. (1982). X- and Y-cells in the lateral geniculate nucleus of macaque monkey. Journal of Physiology (London) 330, 125–143.Google Scholar
Kawamura, S. & Diamond, I.T. (1978). The laminar origin of descending projections from the cortex of the thalamus in Tupaia glis. Brain Research 153, 333–339.Google Scholar
Kratz, K.E., Sherman, S.M. & Kalil, R. (1979). Lateral geniculate nucleus in dark reared cats: Loss of Y-cells without changes in cell size. Science 203, 1353–1355.Google Scholar
Krubitzer, L.A. & Kaas, J.H. (1989). Cortical integration of parallel pathways in the visual system of primates. Brain Research 478, 161–165.Google Scholar
LaChica, E.A., Beck, P. & Casagrande, V.A. (1992). Parallel path ways in macaque monkey striate cortex: Anatomically defined columns in layer III. Proceedings of the National Academy of Sciences of the U.S.A. 89, 3566–3570.Google Scholar
LeVay, S. & McConnel, S.K. (1982). ON and OFF layers in the lateral geniculate nucleus of the mink. Nature 300, 350–351.Google Scholar
Livingstone, M.S. & Hubel, D.H. (1987). Connections between layer 4B of area 17 and thick cytochrome-oxidase stripes of area 18 in the squirrel monkey. Journal of Neuroscience 7, 3371–3377.Google Scholar
Luckett, W.P. (1980). The suggested evolutionary relationships and classification of tree shrews. In Comparative Biology and Evolutionary Relationships of Tree Shrews, ed. Luckett, W.P., pp. 3–31. New York: Plenum Press.Google Scholar
Lund, J.H., Henry, G.H., McQueen, C.L. & Harvey, A.R. (1979). Anatomical organization of the primary visual cortex (area 17) of the cat; a comparison with area 17 of the macaque monkey. Journal of Comparative Neurology 184, 599–618.Google Scholar
Lund, J.S., Fitzpatrick, D. & Humphrey, A.L. (1985). The striate visual cortex of the tree shrew. In Cerebral Cortex, Vol 3, Visual Cortex, ed. Peters, A. & Jones, E.G., pp. 157–205. New York: Plenum Press.Google Scholar
MacPhee, R.D.E. (1993). Summary. In Primates and Their Relatives in Phylogenetic Perspective, ed. MacPhee, R.D.E., pp. 363–373. New York: Plenum Press.Google Scholar
McKay, R.D.G. & Hockfield, S. (1982). Monoclonal antibodies distinguish antigenically discrete neuronal types in the vertebrate central nervous system. Proceedings of the National Academy of Sciences of the U.S.A. 79, 6747–6751.Google Scholar
Müller, B. & Peichl, L. (1989). Topography of cones and rods in the tree shrew retina. Journal of Comparative Neurology 282, 581–594.Google Scholar
Norton, T.T., Casagrande, V.A. & Sherman, S.M. (1977). Loss of Y-cells in the lateral geniculate nucleus of monocularly deprived tree shrews. Science 197, 784–786.Google Scholar
Norton, T.T. & Casagrande, V.H. (1982). Laminar organization of receptive field properties in lateral geniculate nucleus of bush baby (Galago crassicaudatus). Journal of Neurophysiology 47, 715–741.CrossRefGoogle ScholarPubMed
Norton, T.T., Irvin, G.E., Casagrande, V.A., Sesma, M.A. & Petry, H.M. (1988). Contrast sensitivity functions of W-, X-, and Y-like relay cells in the lateral geniculate nucleus of bush baby (Galago crassicaudatus). Journal of Neurophysiology 59, 1639–1656.CrossRefGoogle Scholar
Sesma, M.A., Casagrande, V.A. & Kaas, J.H. (1984). Cortical connections of area 17 in tree shrews. Journal of Comparative Neurology 230, 337–351.Google Scholar
Shapley, R. & Perry, V.H. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neurosciences 9, 224–235.CrossRefGoogle Scholar
Sherman, S.M., Hoffman, K.P. & Stone, J. (1972). Loss of a specific cell type from the dorsal lateral geniculate in visually deprived cats. Journal of Neurophysiology 35, 532–541.Google Scholar
Sherman, S.M., Norton, T.T. & Casagrande, V.A. (1975). X- and Y-cells in the dorsal lateral geniculate nucleus of tree shrew (Tupaiaglis). Brain Research 93, 152–157.Google Scholar
Sherman, S.M., Wilson, J.R., Kaas, J.H. & Webb, S.V. (1976). X- and Y-cells in the dorsal lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). Science 192, 975–977.Google Scholar
Shipp, S. & Zeki, S. (1985). Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex. Nature 315, 322–324.Google Scholar
Stone, J. (1983). Parallel processing in The Visual System: The Classification of Retinal Ganglion Cells and its Impact on the Neurobiology of Vision, pp. 438. New York: Plenum Press.Google Scholar
Stryker, M.P. & Zahs, K.R. (1983). ON and OFF sublaminae in the lateral geniculate nucleus of the ferret. Journal of Neuroscience 3, 1943–1951.Google Scholar
Sur, M., Weller, R.E. & Kaas, J.H. (1980). Representation of body surface in somatosensory area I of tree shrews (Tupaia glis). Journal of Comparative Neurology 194, 71–95.Google Scholar
Sur, M., Frost, D.O. & Hockfield, S. (1988). Expression of a surface associated antigen on Y-cells in the cat lateral geniculate nucleus is regulated by visual experience. Journal of Neuroscience 8, 874–882.Google Scholar
Tootell, R.B.H., Hamilton, S.H. & Silverman, M.S. (1985). Topography of cytochrome oxidase activity in the primate striate cortex. Journal of Neuroscience 5, 2786–2800.CrossRefGoogle Scholar
Weller, R.E. & Kaas, J.H. (1982). The organization of the visual system in Galago: Comparisons with monkeys. In The Lesser Bush baby (Galago) as an Animal Model: Selected Topics, ed. Haines, D.E., pp. 107–135. Florida: CRC Press.Google Scholar
Weller, R.E. & Kaas, J.H. (1985). Cortical projections of dorsolateral visual area in owl monkeys: The prestriate relay to inferior temporal cortex. Journal of Comparative Neurology 234, 35–59.Google Scholar
Wong-Riley, M.T.T. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 11–28.CrossRefGoogle ScholarPubMed