Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T05:50:18.011Z Has data issue: false hasContentIssue false
  • English
  • Français

Parameters affecting the loss of ganglion cells of the retina following ablations of striate cortex in primates

Published online by Cambridge University Press:  02 June 2009

Rosalyn E. Weller  and
Jon H. Kaas
Rosalyn E. Weller
Affiliation:
Department of Psychology, University of Alabama at Birmingham, Birmingham
Jon H. Kaas
Affiliation:
Department of Psychology, Vanderbilt University, Nashville
Get access Rights & Permissions [Opens in a new window]

Abstract

Partial lesions of striate cortex were made in newborn and adolescent or young adult macaque monkeys, one newborn squirrel monkey, and adult squirrel and owl monkeys. After survival times ranging from 3 1/2 weeks to 8 years, the retinas were examined for transneuronal retrograde ganglion cell loss and retinal projections to the dorsal lateral geniculate nucleus, and other targets were examined for changes. After lesions in infant macaque monkeys and long postoperative survivals, nearly 80% of the ganglion cells were lost in the altered portions of the retinas. The degeneration appeared to be exclusively of ganglion cells projecting to the parvocellular layers of the lateral geniculate nucleus, and the loss of this class of cell appeared to be complete or nearly complete for the affected portions of the retina. Cases with shorter survivals showed that nine-tenths of the potential loss occurred within 6 months, and about half of the potential loss took place within one month. In cases where lesions were placed in adolescent and young adult macaque monkeys, the loss also was of ganglion cells projecting to the parvocellular layers. However, the rate of cell loss was slower so that little or no cell loss was apparent after six months, and only one-third to three-fourths of the potential loss occurred within 12–14 months. A cell loss of 22% was measured in the altered portions of the retina of a squirrel monkey lesioned as an infant and surviving for 6 months, but no regions of ganglion cell loss were apparent in the retinas of owl and squirrel monkeys lesioned as adults and surviving as long as two or more years.

We conclude that nearly 80% of the ganglion cells project to the parvocellular layers in macaque monkeys, and that the ultimate survival of these ganglion cells depends on the presence of target neurons in the parvocellular layers. Age is important in that the loss of ganglion cells proceeds rapidly in infant macaque monkeys, but slowly in older animals. Infant New World monkeys, judging from one squirrel monkey, are also susceptible to ganglion cell loss, although apparently at a rate comparable to older macaque monkeys. Finally, adult New World monkeys do not appear to be susceptible to ganglion cell loss. These age and species differences in rates of loss and susceptibility to loss challenge a “sustaining collateral” hypothesis proposed earlier (Weller et al., 1979), and suggest alternatives and modifications.

Keywords

MonkeysLateral geniculate nucleusTransneuronal degenerationRetrograde degeneration
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 4 , October 1989 , pp. 327 - 349
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

Allman, J.M. & Kaas, J.H. (1971). Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). Brain Research 35, 89–106.CrossRefGoogle ScholarPubMed
Barde, Y.-A., Edgar, D. & Thoenen, H. (1983). New neurotrophic factors. Annual Review of Physiology 45: 601–612.CrossRefGoogle ScholarPubMed
Bleier, R. (1969). Retrograde transsynaptic cellular degeneration in mammillary and ventral tegmental nuclei following limbic decortication in rabbits of various ages. Brain Research 15, 365–393.Google Scholar
Bunt, A.H., Hendrickson, A.E., Lund, J.S. & Lund, R.D. (1975). Monkey retinal ganglion cells: morphometric analysis and tracing of axonal projections with a consideration of the peroxidase technique. Journal of Comparative Neurology 164, 265–286.CrossRefGoogle ScholarPubMed
Bunt, A.H. & Minckler, D.S. (1977). Displaced ganglion cells in the retina of the monkey. Investigative Ophthalmology and Visual Science 16, 95–98.Google ScholarPubMed
Callahan, E.C., Tong, L. & Spear, P.D. (1984). Critical period for the marked loss of retinal X cells following visual cortex damage in cats. Brain Research 323, 302–306.CrossRefGoogle ScholarPubMed
Chow, K.-L. & Dewson, J.H. (1966). Numerical estimates of neurons and glia in lateral geniculate body during retrograde degeneration. Journal of Comparative Neurology 128, 63–74.CrossRefGoogle Scholar
Connolly, M. & Van Essen, D.C. (1984). The representation of the visual field in parvicellular and magnocellular laminae of the lateral geniculate nucleus in the macaque monkey. Journal of Comparative Neurology 226, 544–564.Google Scholar
Cowan, W. (1970). Anterograde and retrograde transneuronal degeneration in the central and peripheral nervous system. In Contemporary Research Methods in Neuroanatomy, ed. Nauta, W. & Ebbesson, S., New York: Springer-Verlag, pp. 217–251.Google Scholar
Cowan, W.M., Gottlieb, D.I., Hendrickson, A.E., Price, J.L. & Woolsey, T.A. (1972). The autoradiographic demonstration of axonal connections in the central neurons systems. Brain Research 37, 21–51.CrossRefGoogle Scholar
Cowan, W.M., Fawcett, J.W., O'Leary, P.D.M. & Stanfield, B.B. (1984). Regressive events in neurogenesis. Science 225, 1258–1265.Google Scholar
Cowey, A. (1964). Projection of the retina onto striate and prestriate cortex in the squirrel monkey (Saimiri sciureus). Journal of Neurophysiology 27, 366–396.CrossRefGoogle Scholar
Cowey, A. (1974). Atrophy of retinal ganglion cells after removal of striate cortex in rhesus monkey. Perception 3, 257–260.CrossRefGoogle ScholarPubMed
Cunningham, T.J., Huddleston, C. & Murray, M. (1979). Modification of neuron numbers in the visual system of the rat. Journal of Comparative Neurology 184, 423–434.CrossRefGoogle ScholarPubMed
deMonasterio, F.M. (1978 a). Properties of concentrically organized X and Y ganglion cells of macaque retina. Journal of Neurophysiology 41, 1394–1417.Google Scholar
deMonasterio, F.M. (1978 b). Properties of ganglion cells with atypical receptive-field organization in retina of macaques. Journal of Neurophysiology 41, 1435–1449.CrossRefGoogle Scholar
Diamond, I.T. & Utley, J.D. (1963). Thalamic retrograde degeneration study of sensory cortex in opposum. Journal of Comparative Neurology 120, 129–160.CrossRefGoogle Scholar
Dineen, J.T. & Hendrickson, A.E. (1981). Age-correlated differences in the amount of retinal degeneration after striate cortex lesions in monkeys. Investigative Ophthalmology and Visual Science 21, 749–752.Google Scholar
Dineen, J.T., Hendrickson, A.E. & Keating, E.G. (1982). Alterations of retinal inputs following striate cortex removal in adult monkey. Experimental Brain Research 47, 446–456.Google 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
Eysel, U.T. & Peichl, L. (1985). Regenerative capacity of retinal axons in the cat, rabbit, and guinea pig. Experimental Neurology 88, 757–766.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, 749–772.Google Scholar
Garey, L.J. & Saini, K.D. (1981). Golgi study of the normal development of neurons in the lateral geniculate nucleus of the monkey. Experimental Brain Research 44, 117–128.CrossRefGoogle ScholarPubMed
Gills, J.P. & Wadsworth, J.A.C. (1967). Retrograde transsynaptic degeneration of the inner nuclear layer of the retina. Investigative Ophthalmology 6, 437–448.Google Scholar
Gouras, P. (1968). Identification of cone mechanisms in monkey ganglion cells. Journal of Physiology (London) 199, 533–547.CrossRefGoogle ScholarPubMed
Gouras, P. (1969). Antidromic responses of orthodromically identified ganglion cells in monkey retina. Journal of Physiology (London) 204, 407–419.Google Scholar
Haddock, J.N. & Berlin, L. (1950). Transsynaptic degeneration in the visual system. Archives of Neurology (Chicago) 64, 66–73.Google Scholar
Hamori, J., Pasik, P. & Pasik, T. (1983). Differential frequency of P cells and I cells in magnocellular and parvocellular laminae of monkey lateral geniculate nucleus. An ultrastructural study. Experimental Brain Research 52, 57–66.CrossRefGoogle ScholarPubMed
Hendrickson, A., Wilson, M.E. & Toyne, M.J. (1970). The distribution of optic nerve fibers in Macaca mulatto. Brain Research 23, 425–427.CrossRefGoogle Scholar
Hendrickson, A. & Dincen, J.T. (1982). Hypertrophy of neurons in dorsal lateral geniculate nucleus following striate cortex lesions in infant monkeys. Neuroscience Letters 30, 217–222.Google Scholar
Illing, R.-B. (1980). Axonal bifurcation of cat retinal ganglion cells as demonstrated by retrograde double labeling with fluorescent dyes. Neuroscience Letters 19, 125–130.CrossRefGoogle ScholarPubMed
Illing, R.-B. & Wässle, H. (1981). The retinal projection to the thalamus in the cat: a quantitative investigation and a comparison with the retinotectal pathway. Journal of Comparative Neurology 202, 265–285.Google Scholar
Irvin, G.E., Norton, T.T., Sesma, M.A. & Casagrande, V.A. (1986). W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Research 362, 254–270.Google Scholar
Jacobson, M. (1970). Developmental Neurobiology. New York: Holt, Rinehart & Winston, Inc.Google Scholar
Kaas, J.H., Guillery, R.W. & Allman, J.M. (1972). Some principles of organization in the dorsal lateral geniculate nucleus. Brain Behavior and Evolution 6, 253–299.CrossRefGoogle ScholarPubMed
Kaas, J.H. & Huerta, M.F. (1988). The subcortical visual system of primates. In Comparative Primate Biology, Vol. 4: Neurosciences. ed. Steklis, H.P., Alan R. Liss, Inc., pp. 327–391.Google Scholar
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
Kalil, R.E. & Behan, M. (1987). Synaptic reorganization in the dorsal lateral geniculate nucleus following damage to visual cortex in newborn or adult cats. Journal of Comparative Neurology 257, 216–236.Google Scholar
Kalil, R.E. & Scott, G.L. (1979). Development of retinogeniculate synapses in the dorsal lateral geniculate nucleus of the cat. Society for Neuroscience Abstracts 5, 791.Google Scholar
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
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1985). Central projections of cat retinal ganglion cells. Journal of Comparative Neurology 237, 216–226.Google Scholar
Leventhal, A.G., Ault, S.J. & Vitek, D.J. (1988). The naso-temporal division in primate retina: the neural bases of macular sparing and splitting. Science 240, 66–67.CrossRefGoogle Scholar
Linden, R. & Perry, V.H. (1983). Massive retinotectal projection in rats. Brain Research 272, 145–149.CrossRefGoogle ScholarPubMed
Malpeli, J.G. & Baker, F.H. (1975). The representation of the visual field in the lateral geniculate nucleus of Macaca mulatto. Journal of Comparative Neurology 161, 569–594.CrossRefGoogle Scholar
Mason, C.A. (1982). Development of terminal arbors of retinogeniculate axons in the kitten, II: Electron-microscopical observations. Neuroscience 7, 561–582.Google Scholar
Matthews, M.R. (1964). Further observations on transneuronal degeneration in the lateral geniculate nucleus of the macaque monkey. Journal of Physiology (London) 98, 255–263.Google Scholar
Michael, C.R. (1988). Retinal afferents, arborization patterns, dendritic field orientations, and the segregation of function in the lateral geniculate nucleus of the monkey. Proceedings of the National Academy of Sciences of the U.S.A. 85, 4914–4918.Google Scholar
Mihailovic, L.T., Dragoslava, C. & Dekleva, N. (1971). Changes in the numbers of neurons and glial cells in the lateral geniculate nucleus of the monkey during retrograde cell degeneration. Journal of Comparative Neurology 142, 223–230.Google Scholar
Montero, U.M. & Zempel, J. (1986). The proportion and size of GABA-immunoreactive neurons in the magnocellular and parvocellular layers of the lateral geniculate nucleus of the rhesus monkey. Experimental Brain Research 62, 215–223.CrossRefGoogle ScholarPubMed
Norton, T.T. & Casagrande, V.A. (1982). Laminar organization of receptive-field properties in the lateral geniculate nucleus of bushbaby (Galago crassicaudatus). Journal of Neurophysiology 47, 715–741.Google Scholar
Payne, B.R., Pearson, H.E. & Cornwell, P. (1984). Transneuronal degeneration of beta retinal ganglion cells in the cat. Proceedings of the Royal Society B (London) 222, 15–32.Google Scholar
Pearson, H.E., Labar, D.R., Payne, B.R., Cornwell, P. & Aggarwal, N. (1981). Transneuronal retrograde degeneration in the cat retina following neonatal ablation of visual cortex. Brain Research 212, 470–475.Google Scholar
Perry, V.H. & Cowey, A. (1979). The effects of unilateral cortical and tectal lesions on retinal ganglion cells in rats. Experimental Brain Research 35, 85–95.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1981). The morphological correlates of X- and Y-like retinal ganglion cells in the retina of monkeys. Experimental Brain Research 43, 426–428.Google Scholar
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 1125–1137.Google Scholar
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, 1101–1124.CrossRefGoogle Scholar
Rodieck, R.W. (1988). The primate retina. In Comparative Primate Biology, Vol. 4: Neurosciences, Alan R. Liss, Inc., pp. 127–150.Google Scholar
Rodieck, R.W. & Brening, R.K. (1983). Retinal ganglion cells: properties, types, genera, pathways, and trans-species comparison. Brain Behavior and Evolution 23, 121–164.Google Scholar
Rodieck, R.W., Binmoeller, K.F. & Dineen, J.D. (1985). Parasol and midget ganglion cells of the human retina. Journal of Comparative Neurology 233, 115–132.Google Scholar
Rolls, E.T. & Cowey, A. (1970). Topography of the retina and striate cortex and its relationship to visual acuity in rhesus monkeys and squirrel monkeys. Experimental Brain Research 10, 298–310.Google Scholar
Rose, J.E. & Woolsey, C.N. (1958). Cortical connections and functional organization of the thalamic auditory system of the cat. In Biological and Biochemical Bases of Behavior, ed. Harlow, H.F. & Woolsey, C.N., Madison: University of Wisconsin Press.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1978). Functional specificity of lateral geniculate nucleus laminae of the rhesus monkey. Journal of Neurophysiology 41, 788–797.Google Scholar
Shapley, R. & Perry, V.P. (1986). Cat and monkey retinal ganglion cells and their visual functional roles. Trends in Neurosciences 9, 229–235.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. Science 192, 415–417.CrossRefGoogle ScholarPubMed
Spear, P.D. (1985). Neural mechanisms of compensation following neonatal visual cortex damage. In Synoptic Plasticity, ed. Cotman, C.W., New York: The Guilford Press, pp. 111–167.Google Scholar
Stelzner, D.J. & Keating, E.G. (1977). Lack of intralaminar sprouting of retinal axons in monkey LGN. Brain Research 126, 201–210.Google Scholar
Stone, J. (1978). The number and distribution of ganglion cells in the cat's retina. Journal of Comparative Neurology 180, 753–772.Google Scholar
Stone, J. (1983). Parallel Processing in the Visual System. New York: Plenum Press.Google Scholar
Stone, J. & Johnston, E. (1981). The topography of primate retina: a study of the human, bushbaby, New- and Old-World monkeys. Journal of Comparative Neurology 196, 205–223.Google Scholar
Stone, J., Leicester, J. & Sherman, S.M. (1973). The nasotemporal division of the monkey's retina. Journal of Comparative Neurology 150, 333–348.Google Scholar
Sur, M. & Sherman, S.M. (1982). Retinogeniculate terminations in cats: morphological differences between X- and Y-cell axons. Science 218, 389–391.Google Scholar
Sur, M., Esguerra, M., Garraghty, P.E., Kritzer, M.F. & Sherman, S.M. (1987). Morphology of physiological identified retinogeniculate X and Y axons in the cat. Journal of Neurophysiology 58, 1–32.CrossRefGoogle ScholarPubMed
Talbot, S.A. & Marshall, W.H. (1941). Physiological studies on neural mechanisms of visual localization and discrimination. American Journal of Ophthalmology 24, 1255–1264.Google Scholar
Tigges, M. & Tigges, J. (1970). The retinofugal fibers and their terminal nuclei in Galago crassicaudatus (primates). Journal of Comparative Neurology 138, 87–102.Google Scholar
Tong, L., Spear, P.D., Kalil, R.E. & Callahan, E.C. (1982). Loss of retinal X cells in cats with neonatal or adult visual cortex damage. Science 217, 72–75.CrossRefGoogle ScholarPubMed
Van Buren, J.M. (1963 a). Transsynaptic retrograde degeneration in the visual system of primates. Journal of Neurology, Neurosurgery, and Psychiatry 26, 402–407.CrossRefGoogle Scholar
Van Buren, J.M. (1963 b). The Retinal Ganglion Cell Layer. Springfield, Illinois: Charles C. Thomas.Google Scholar
Van Essen, D.C., Newsome, W.T. & Maunsell, J.H.R. (1984). The visual-field representation in striate cortex of the macaque monkey: asymmetries, anisotropies, and individual variability. Vision Research 24, 429–448.CrossRefGoogle ScholarPubMed
Vaney, D.I., Peichl, L., Wässle, H. & Illing, R.B. (1981). Almost all ganglion cells in the rabbit retina project to the superior colliculus. Brain Research 212, 447–453.Google Scholar
Walsh, F.B. (1947). Clinical Neuro-Ophthalmology. Baltimore, Maryland: The Williams & Wilkins Company.Google Scholar
Wässle, H. & Illing, R.B. (1980). The retinal projection to the superior colliculus in the cat: a quantitative study with HRP. Journal of Comparative Neurology 190, 333–356.CrossRefGoogle Scholar
Webb, S.V. & Kaas, J.H. (1976). The sizes and distribution of ganglion cells in the retina of the owl monkey (Aotus trivirgatus). Vision Research 16, 1247–1254.CrossRefGoogle ScholarPubMed
Weber, J.T., Huerta, M.F., Kaas, J.H. & Harting, J.K. (1983). The projections of the lateral geniculate nucleus of the squirrel monkey: studies of the interlaminar zones and the S layers. Journal of Comparative Neurology 213, 135–145.Google Scholar
Weller, R.E. & Kaas, J.H. (1977). Evidence for selective loss of X-cell input to the dorsal lateral geniculate nucleus of monkeys with long-term ablations of striate cortex. Society for Neuroscience Abstracts 3, 581.Google Scholar
Weller, R.E., Kaas, J.H. & Wetzel, A.B. (1979). Evidence for the loss of X cells of the retina after long-term ablation of visual cortex in monkeys. Brain Research 160: 134–138.Google Scholar
Weller, R.E. & Kaas, J.H. (1980). Loss of retinal ganglion cells and altered retinogeniculate projections in monkeys with striate cortex lesions. ARVO Abstracts 20, 2.Google Scholar
Weller, R.E. & Kaas, J.H. (1982). Retinal degeneration and loss of retinogeniculate projections in infant and adult monkeys surviving variable times after lesions of striate cortex. ARVO Abstracts 22, 46.Google Scholar
Weller, R.E. & Kaas, J.H. (1984). Developmental changes in susceptibility to retinal ganglion cell loss after lesions of visual cortex in primates and other mammals. In Development of Visual Pathways in Mammals, ed. Stone, J., Dreher, B. & Rapport, D.H., New York: Alan R. Liss, Inc., 289–302.Google Scholar
Weller, R.E., Kaas, J.H. & Ward, J. (1981). Preservation of retinal ganglion cells and normal patterns of retinogeniculate projections in prosimian primates with long-term ablations of striate cortex. Investigative Ophthalmology and Visual Science 20, 139–148.Google Scholar
Wilkes, M., Zingaro, G. & Murphy, E.H. (1985). Survival of the ganglion cell population in the rabbit retina following neonatal visual cortex ablation. Developmental Brain Research 21, 293–297.Google Scholar
Winfield, D.A. & Powell, T.P.S. (1980). An electron-microscopical study of the postnatal development of the lateral geniculate nucleus in the normal kitten after eyelid suture. Proceedings of the Royal Society B (London) 221, 411–436.Google Scholar
Winfield, D.A., Hiorns, R.W. & Powell, T.P.S. (1980). A quantitative electron-microscopical study of the postnatal development of the lateral geniculate nucleus in normal kittens and in kittens with eyelid suture. Proceedings of the Royal Society B (London) 210, 211–234.Google Scholar
Wong-Riley, M.T.T. (1972). Changes in the dorsal lateral geniculate nucleus of the squirrel monkey after unilateral ablation of visual cortex. Journal of Comparative Neurology 146, 519–548.Google Scholar