Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-24T03:03:28.178Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphology of retinogeniculate axons in the macaque

Published online by Cambridge University Press:  02 June 2009

Michael Conley  and
David Fitzpatrick
Michael Conley
Affiliation:
Departments of Psychology and Neurobiology, Duke University, Durham
David Fitzpatrick
Affiliation:
Departments of Psychology and Neurobiology, Duke University, Durham
Get access Rights & Permissions [Opens in a new window]

Abstract

The size, pattern of terminal arborizations, and laminar specificity of individual retinogeniculate axons were studied in the macaque following injections of HRP into the optic tract. Axons that terminated in the magnocellular layers had significantly larger fiber diameters and wider terminal fields than those that terminated in the parvocellular layers. Terminal fields of magnocellular fibers spanned most of the width of their target layer, whereas those of parvocellular fibers were restricted to approximately one-half the width of their target layers; almost all terminal fields were oriented along lines of projection. All of the optic tract fibers that we examined terminated in only one layer of the lateral geniculate nucleus (GL), including a population of fine caliber fibers that project to the intercalated layers, and none had collateral projections outside the GL. The results suggest that each layer – magnocellular, parvocellular, and intercalated – receives projections from a morphologically distinct population of optic tract fibers.

Keywords

Optic tract axonsLateral geniculate nucleusMacaque
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 3 , March 1989 , pp. 287 - 296
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

Adams, J. (1981). Heavy-metal intensification of DAB-based HRP reaction product. Journal of Histochemistry and Cytochemistry 29, 775.CrossRefGoogle ScholarPubMed
Bowling, D.B. & Michael, C.R. (1980). Projections of single, physiologically characterized optic tract fibers in cat. Nature 286, 899–902.CrossRefGoogle ScholarPubMed
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
Boycott, B.B. & Wassle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397–419.CrossRefGoogle ScholarPubMed
Bunt, A.H., Hendrickson, A.E., Lund, J.S., Lund, R.D. & Fuchs, A.F. (1975). Monkey retinal ganglion cells: morphometric analysis and tracing of axonal projections, with a consideration of the per-oxidase technique. Journal of Comparative Neurology 164, 265–286.CrossRefGoogle Scholar
Campos-Ortega, J.A. & Hayhow, W.A. (1970). A new lamination pattern in the lateral geniculate nucleus of primates. Brain Research 20, 335–339.CrossRefGoogle ScholarPubMed
Campos-Ortega, J.A., Glees, P. & Neuhoff, V. (1968). Ultrastructural analysis of individual layers in the lateral geniculate body of the monkey. Zeitschrift für Zellforschung 87, 82–100.CrossRefGoogle ScholarPubMed
Cleland, B.G., Dubin, M.W. & Levick, W.R. (1971). Sustained and transient neurons in the cat's retinal and lateral geniculate nucleus. Journal of Physiology (London) 217, 473–496.CrossRefGoogle ScholarPubMed
Colonnier, M. & Guillery, R.W. (1964). Synaptic organization in the lateral geniculate nucleus of the monkey. Zeitschrift für Zellforschung 62, 333–355.CrossRefGoogle ScholarPubMed
Conley, M., Birecree, E. & Casagrande, V.A. (1985). Neuronal classes and their relation to functional and laminar organization of the lateral geniculate nucleus: a Golgi study of the prosimian primate, Galago crassicaudatus. Journal of Comparative Neurology 242, 561–583.CrossRefGoogle ScholarPubMed
Conley, M., Penny, G.R. & Diamond, I.T. (1987). Terminations of individual optic tract fibers in the lateral geniculate nuclei of Galago crassicaudatus and Tupaia belangeri. Journal of Comparative Neurology 256, 71–87.CrossRefGoogle ScholarPubMed
DeMonasterio, F.M. (1978). Properties of concentrically organized X and Y ganglion cells of macaque retina. Journal of Neurophysiology 41, 1394–1417.CrossRefGoogle Scholar
DeMonasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology 251, 167–195.CrossRefGoogle Scholar
DeMonasterio, F.M., Gouras, P. & Tolhurst, D.J. (1976). Spatial summation, response pattern, and conduction velocity of ganglion cells of the rhesus monkey retina. Vision Research 16, 674–678.CrossRefGoogle Scholar
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurons in lateral geniculate nucleus of macaque. Journal of Physiology (London) 357, 219–240.CrossRefGoogle ScholarPubMed
Dreher, B., Fukuda, Y. & Dodieck, 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.CrossRefGoogle ScholarPubMed
Fitzpatrick, D., Itoh, K. & Diamond, I.T. (1983). The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neuroscience 3, 673–702.CrossRefGoogle ScholarPubMed
Friedlander, M.J., Lin, C.-S, Stanford, L.R. & Sherman, S.M. (1981). Morphology of functionally identified neurons in the lateral geniculate nucleus of the cat. Journal of Neurophysiology 46, 80–129.CrossRefGoogle ScholarPubMed
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
Giolli, R.A. & Tigges, J. (1970). The primary optic pathways and nuclei in primates. In Advances in Primatology, Vol. 1, ed. Noback, C.R. & Montagno, W., pp. 29–54. New York: Appleton-Century-Crofts.Google Scholar
Glees, P. & le Gros Clark, W.E. (1941). The termination of optic fibres in the lateral geniculate body of the monkey. Journal of Anatomy (London) 75, 295–310.Google ScholarPubMed
Glees, P., Hasan, M. & Tischner, K. (1967). The cytological distribution of “osmiophilic bodies” in the normal and degenerating lateral geniculate nucleus of the monkey. Acta Neuropathologie 8, 285–291.CrossRefGoogle Scholar
Gouras, P. (1969). Antidromic responses of orthodromically identified ganglion cells in monkey retina. Journal of Physiology (London) 204, 407–419.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1966). A study of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. Journal of Comparative Neurology 128, 21–50.CrossRefGoogle ScholarPubMed
Guillery, R.W. (1967). Patterns of synaptic interconnections in the dorsal lateral geniculate nucleus of the cat and monkey: a brief review. Vision Research (Suppl.) 3, 211–227.Google Scholar
Guillery, R.W. & Colonnier, M. (1970). Synaptic patterns in the dorsal lateral geniculate nucleus of the monkey. Zeitschrift für Zellfor-schung 103, 90–108.CrossRefGoogle ScholarPubMed
Hamos, J.E., Van Horn, S., Raczkowski, D. & Sherman, S.M. (1987). Synaptic circuits involving an individual retinogeniculate axon in the cat. Journal of Comparative Neurology 259, 165–192.CrossRefGoogle ScholarPubMed
Harting, J.K., Casagrande, V.A. & Weber, J.T. (1978). The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate axons. Brain Research 150, 593–599.CrossRefGoogle ScholarPubMed
Hubel, D.H., Wiesel, T.N. & Levay, S. (1977). Plasticity of ocular dominance columns in monkey striate cortex. Philosophical Transactions of the Royal Society B (London) 278, 377–409.Google ScholarPubMed
Kaas, J.H., Huerta, M.F., Weber, J.T. & Harting, J.K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. Journal of Comparative Neurology 182, 517–554.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.E. (1982). X and Y cells in the lateral geniculate nucleus of macaque monkeys. Journal of Physiology (London) 330, 125–143.CrossRefGoogle ScholarPubMed
Kaplan, E. & Shapley, R.E. (1986). The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proceedings of the National Academy of Sciences of the U.S.A. 83, 2755–2757.CrossRefGoogle ScholarPubMed
Lachica, E.A. & Casagrande, V.A. (1988). Development of primate retinogeniculate axon arbors. Visual Neuroscience 1, 103–124.CrossRefGoogle ScholarPubMed
le Gros Clark, W.E. (1942). The visual centers of the brain and their connexions. Physiological Reviews 22, 205–232.CrossRefGoogle Scholar
le Gros Clark, W.E. & Penman, G.G. (1934). The projection of the retina in the lateral geniculate body. Proceedings of the Royal Society B (London) 114, 291–314.Google Scholar
Lennie, P. (1980). Parallel visual pathways. Vision Research 20, 560–594.CrossRefGoogle ScholarPubMed
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in Old-World monkey: morphology and central projections. Science 213, 1139–1142.CrossRefGoogle ScholarPubMed
Marrocco, R.T. (1976). Sustained and transient cells in monkey lateral geniculate nucleus: conduction velocities and response properties. Journal of Neurophysiology 39, 340–353.CrossRefGoogle ScholarPubMed
Malpeli, J.G. & Baker, F.H. (1975). The representation of the visual field in the lateral geniculate nucleus of Macaco mulatto. Journal of Comparative Neurology 161, 569–594.CrossRefGoogle Scholar
Mason, C.A. & Robson, J.A. (1978). Morphology of retinogeniculate axons in the cat. Neuroscience 4, 79–97.CrossRefGoogle Scholar
Michael, C.R. (1984). Monkey geniculate cells and retinal afferents of the same physiological class have similar arborization patterns. Investigative Ophthalmology and Visual Science (Suppl.) 25, 164.Google Scholar
Michael, C.R. (1988). Retinal afferent arborization patterns, dendritic field orientations, and segregation of function in the lateral geniculate nucleus of the monkey. Proceedings of the National Academy of Science of the U.S.A. 85, 4914–4918.CrossRefGoogle ScholarPubMed
Ogden, T.E. & Miller, R.F. (1966). Studies of the optic nerve of the rhesus monkey: nerve fiber spectrum and physiological properties. Vision Research 6, 485–506.CrossRefGoogle ScholarPubMed
Perry, V.H., Oehler, R. & Cowey, A. (1984). Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey. Neuroscience 12, 1101–1123.CrossRefGoogle Scholar
Potts, A.M., Hodges, D., Shelman, C.B., Frity, K.J., Levy, N.S. & Magnall, Y. (1972). Morphology of the primate optic nerve. I. Method and total fiber count. Investigative Ophthalmology 11, 981–988.Google ScholarPubMed
Reese, B.E. & Cowey, A. (1988). Segregation of functionally distinct axons in the monkey's optic tract. Nature 331, 350–351.CrossRefGoogle ScholarPubMed
Reese, B.E. & Guillery, R.W. (1987). Distribution of axons according to diameter in the monkey's optic tract. Journal of Comparative Neurology 260, 453–459.CrossRefGoogle ScholarPubMed
Robson, J.A. (1981). Dendritic and axonal morphology in the dorsal lateral geniculate nucleus of macaque monkeys. Society of Neuroscience Abstracts 7, 459.Google Scholar
Rodieck, R.W. (1979). Visual pathways. Annual Review of neuroscience 2, 193–225.CrossRefGoogle ScholarPubMed
Saini, K.D. & Garey, L.J. (1981). Morphology of neurons in the lateral geniculate nucleus of the monkey. Experimental Brain Research 42, 235–248.Google ScholarPubMed
Saito, H.-A. (1983). Morphology of physiologically identified X-, Y-, and W-type retinal ganglion cells of the cat. Journal of Comparative Neurology 221, 279–288.CrossRefGoogle Scholar
Schiller, P.H. & Colby, C.L. (1983). The responses of single cells in the lateral geniculate nucleus of the rhesus monkey to color and luminance contrast. Vision Research 23, 1631–1641.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate laminae of the rhesus monkey. Journal of Neurophysiology 41, 788–797.CrossRefGoogle ScholarPubMed
Shapley, R., Kaplan, E. & Soodak, R. (1981). Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque. Nature 292, 543–545.CrossRefGoogle ScholarPubMed
Stanford, L.R. & Sherman, S.M. (1984). Structure/function relationships of retinal ganglion cells in the cat. Brain Research 297, 381–386.CrossRefGoogle ScholarPubMed
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells. A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 37, 722–748.CrossRefGoogle ScholarPubMed
Stone, J., Dreher, B. & Leventhal, A. (1979). Hierarchical and parallel mechanisms is the organization of visual cortex. Brain Research Reviews 1, 345–394.CrossRefGoogle Scholar
Sur, M. & Sherman, S.M. (1982). Retinogeniculate terminations in the cat: morphological differences between X- and Y-cell axons. Science 218, 389–391.CrossRefGoogle Scholar
Sur, M., Esguerra, M., Garraghty, P.E., Kritzer, M.F. & Sherman, S.M. (1987). Morphology of physiologically identified retinogeniculate X- and Y-axons in the cat. Journal of Neurophysiology 58, 1–32.CrossRefGoogle ScholarPubMed
Szentagothai, J. (1973). Neuronal And synaptic architecture of the lateral geniculate nucleus. In Handbook of Sensory Physiology, Vol. VII/3, Central Processing of Visual Information, Part B, ed. Jung, R., pp. 141–176. Berlin: Springer-Verlag.Google Scholar
Wiesel, T.N. & Hubel, D.H. (1966). Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. Journal of Neurophysiology 29, 1115–1156.CrossRefGoogle ScholarPubMed
Wilson, J.R. & Hendrickson, A.E. (1981). Neuronal and synaptic structure of the dorsal lateral geniculate nucleus in normal and monocularly deprived Macaca monkeys. Journal of Comparative Neurology 197, 517–539.CrossRefGoogle ScholarPubMed