Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-28T08:20:30.693Z Has data issue: false hasContentIssue false
  • English
  • Français

Retinotopic organization of the superior colliculus in relation to the retinal distribution of afferent ganglion cells

Published online by Cambridge University Press:  02 June 2009

D.M. Berson  and
J.J. Stein
D.M. Berson
Affiliation:
Department of Neuroscience, Division of Biology and Medicine, Brown University, Providence
J.J. Stein
Affiliation:
Department of Neuroscience, Division of Biology and Medicine, Brown University, Providence
Get access Rights & Permissions [Opens in a new window]

Abstract

Sensory representations in the brain exhibit topographic variations in magnification. These variations have been thought to reflect regional differences in the density of innervation at the sensory receptor surface. In the primate visual cortex, for example, local magnification factors have been reported to be proportional to the corresponding densities of retinal ganglion cells. We sought to learn whether this principle also operates in a second major retinofugal pathway—the projection to the superior colliculus. In cats, we first used retrograde transport to determine the retinal distributions of the ganglion cells that project to the colliculus. Then, we compared the numbers of colliculopetal ganglion cells in selected retinal sectors to the areas of the corresponding collicular representations. Collicular areal magnification was not simply proportional to the density of afferent ganglion cells, being instead at least 5-fold greater than expected in the representation of the central visual field. These data imply that incoming retinal afferents are more widely spaced in the central regions of the tectal map than in the map's periphery. Such variations in afferent density appear to play as large a role as the distribution of ganglion cells in determining the metric of the collicular map.

Keywords

MagnificationRetinotopic organizationSuperior colliculusW cellsGamma cellsCat
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 4 , July 1995 , pp. 671 - 686
Copyright
Copyright © Cambridge University Press 1995

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

Azzopardi, P. & Cowey, A. (1993). Preferential representation of the fovea in the primary visual cortex. Nature 361, 719–721.CrossRefGoogle ScholarPubMed
Berman, A. (1968). The Brainstem of the Cat: A Cytoarchiteclonic Atlas with Stereotaxic Coordinates. Madison, Wisconsin: University of Wisconsin Press.Google Scholar
Berman, N. & Cynader, M. (1972). Comparison of receptive field organization of the superior colliculus in Siamese and normal cats. Journal of Physiology (London) 224, 363–389.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, 1035–1051.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, 1861–1873.CrossRefGoogle ScholarPubMed
Berson, D.M., Lu, J. & Stein, J.J. (1990). Topographic variations in W-cell input to cat superior colliculus. Experimental Brain Research 79, 459–466.CrossRefGoogle ScholarPubMed
Bishop, P.O., Kozak, W. & Vakkur, G.J. (1962). Some quantitative aspects of the cat's eye: Axis and plane of reference, visual field coordinates and optics. Journal of Physiology (London) 163, 466–502.CrossRefGoogle ScholarPubMed
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology (London) 240, 397–419.CrossRefGoogle ScholarPubMed
Capuano, U. & McIlwain, J.T. (1981). Reciprocity of receptive field images and point images in the superior colliculus of the cat. Journal of Comparative Neurology 196, 13–23.CrossRefGoogle ScholarPubMed
Clark, W.E.L. (1941). The laminar organization and cell content of the lateral geniculate body in the monkey. Journal of Anatomy 74, 419–433.Google Scholar
Dacey, D.M. (1989). Monoamine-accumulating ganglion cell type of the cat's retina. Journal of Comparative Neurology 288, 59–80.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1993). The mosaic of midget ganglion cells in the human retina. Journal of Neuroscience 13, 5334–5355.CrossRefGoogle ScholarPubMed
Dow, B.M., Snyder, R.G., Vautin, R.G. & Bauer, R. (1981). Magnification factor and receptive field size in foveal striate cortex of macaque. Experimental Brain Research 44, 213–228.CrossRefGoogle Scholar
Dräger, U.C. & Hubel, D.H. (1976). Topography of visual and somatosensory projections to mouse superior colliculus. Journal of Neurophysiology 39, 91–101.CrossRefGoogle ScholarPubMed
Farmer, S.G. & Rodieck, R.W. (1982). Ganglion cells of the cat accessory optic system: Morphology and retinal topography. Journal of Comparative Neurology 205, 190–198.CrossRefGoogle ScholarPubMed
Feldon, S., Feldon, P. & Kruger, L. (1970). Topography of the retinal projection upon the superior colliculus of the cat. Vision Research 10, 135–143.CrossRefGoogle ScholarPubMed
Fischer, B. (1973). Overlap of receptive field centers and representation of the visual field in the cat's optic tract. Vision Research 13, 2113–2120.CrossRefGoogle ScholarPubMed
Graybiel, A.M. (1975). Anatomical organization of retinotectal afferents in the cat: An autoradiographic study. Brain Research 145, 365–374.CrossRefGoogle Scholar
Hanker, J.S., Yates, P.E., Meltz, C.B. & Rustioni, A. (1977). A new specific sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Journal of Histochemistry and Cytochemistry 9, 789–792.CrossRefGoogle ScholarPubMed
Harting, J.K. & Guillery, R.W. (1976). Organization of retinocollicular pathways in the cat. Journal of Comparative Neurology 166, 133–144.CrossRefGoogle ScholarPubMed
Hubel, D.H., LeVay, S. & Wiesel, T.N. (1975). Mode of termination of retinotectal fibers in macaque monkey: An autoradiographic study. Brain Research 96, 25–40.CrossRefGoogle ScholarPubMed
Hughes, A. (1971). Topographical relationships between the anatomy and physiology of the rabbit visual system. Documenta Ophthalmologica, Den Haag 30, 33–159.CrossRefGoogle ScholarPubMed
Hughes, A. (1981). Population magnitudes and distribution of the major modal classes of cat retinal ganglion cells as estimated from HRP filling and a systematic survey of the soma diameter spectra for classical neurones. Journal of Comparative Neurology 197, 303–340.CrossRefGoogle Scholar
Humphrey, N.K. (1974). Vision in a monkey without striate cortex: A case study. Perception 3, 241–255.CrossRefGoogle Scholar
Jacobson, M. (1962). The representation of the retina on the optic tectum of the frog. Correlation between retinotectal magnification factor and retinal ganglion cell count. Quarterly Journal of Experimental Physiology 47, 170–178.CrossRefGoogle ScholarPubMed
Katz, L.C., Burkhalter, A. & Dreyer, W.J. (1984). Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310, 498–500.CrossRefGoogle ScholarPubMed
Kelly, J.P. & Gilbert, C.D. (1975). The projections of different morphological types of ganglion cells in the cat retina. Journal of Comparative Neurology 163, 65–80.CrossRefGoogle ScholarPubMed
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A Golgi study. Vision Research 21, 1081–1114.CrossRefGoogle ScholarPubMed
LaBossiere, E. (1976). Histological Processing for the Neural Sciences. Springfield, Illinois: Charles C. Thomas.Google Scholar
Lee, K.J. & Woolsey, T.A. (1975). A proportional relationship between peripheral innervation density and cortical neuron number in the somatosensory system of the mouse. Brain Research 99, 349–353.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.CrossRefGoogle ScholarPubMed
Malpeli, J.G. & Baker, F.H. (1975). The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta. Journal of Comparative Neurology 161, 569–594.CrossRefGoogle ScholarPubMed
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. (1978). Cat superior colliculus: Extracellular potentials related to W-cell synaptic actions. Journal of Neurophysiology 41, 1343–1358.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1983). Representation of the visual streak in visuotopic maps of the cat's superior colliculus: Influence of the mapping variable. Vision Research 23, 507–516.CrossRefGoogle ScholarPubMed
McIlwain, J.T. & Lufkin, R.B. (1976). Distribution of direct Y-cell. inputs to the cat's superior colliculus: Are there spatial gradients? Brain Research 103, 133–138.CrossRefGoogle Scholar
Mize, R.R. (1983). Patterns of convergence and divergence of retinal and cortical synaptic terminals in the cat superior colliculus. Experimental Brain Research 51, 88–96.CrossRefGoogle ScholarPubMed
Myerson, J., Manis, P.B., Miezin, R.M. & Allman, J.M. (1977). Magnification in striate cortex and the retinal ganglion cell layer of the owl monkey: A quantitative comparison. Science 198, 855–857.CrossRefGoogle ScholarPubMed
Perry, V.H. & Cowey, A. (1985). The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors. Vision Research 25, 1795–1810.CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490–495.Google ScholarPubMed
Picanço-Diniz, C.W., Silveira, L.C.L., de Carvalho, M.S.P. & Oswaldo-Cruz, E. (1991). Contralateral visual field representation in area 17 of the cerebral cortex of the agouti: A comparison between the cortical magnification factor and retinal ganglion cell distribution. Neuroscience 44, 325–333.CrossRefGoogle ScholarPubMed
Pollack, J.G. & Hickey, T.L. (1979). The distribution of retinocollicular axon terminals in rhesus monkey. Journal of Comparative Neurology 185, 587–602.CrossRefGoogle ScholarPubMed
Pu, M. & Berson, D.M. (1992). A method for reliable and permanent intracellular staining of retinal ganglion cells. Journal of Neuroscience Methods 41, 45–51.CrossRefGoogle ScholarPubMed
Rolls, E.T. & Cowey, A. (1970). Topography of the retinal and striate cortex and its relationship to visual acuity in rhesus monkeys and squirrel monkeys. Experimental Brain Research 10, 298–310.CrossRefGoogle ScholarPubMed
Sanderson, K.J. (1971). Visual field projection columns and magnification factors in the lateral geniculate nucleus of the cat. Experimental Brain Research 13, 159–177.CrossRefGoogle ScholarPubMed
Schein, S.J. & de Monasterio, F.M. (1987). Mapping of retinal and geniculate neurons onto striate cortex of macaque. Journal of Neuroscience 7, 996–1009.CrossRefGoogle ScholarPubMed
Schneider, G.E. (1969). Two visual systems. Science 163, 895–902.CrossRefGoogle ScholarPubMed
Silveira, L.C.L., Perry, V.H. & Yamada, E.S. (1993). The retinal ganglion cell distribution and the representation of the visual field in area 17 of the owl monkey, Aotus trivirgalus. Visual Neuroscience 10, 887–897.CrossRefGoogle Scholar
Snider, R.S. & Neimer, W.T. (1961). A Stereotaxic Atlas of the Cat Brain. Chicago, Illinois: University of Chicago Press.Google Scholar
Sparks, D.L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: Role of primate superior colliculus. Physiological Reviews 66, 118–171.CrossRefGoogle ScholarPubMed
Stein, J.J. & Berson, D.M. (1993). Is geniculate magnification scaled to ganglion-cell density in the cat? Society for Neuroscience Abstracts 19, 529.Google Scholar
Stein, J.J. & Berson, D.M. (1995). On the distribution of gamma cells in the cat retina. Visual Neuroscience 12, 000–000.CrossRefGoogle ScholarPubMed
Stein, J.J., Johnson, S.A. & Berson, D.M. (1994). Distribution and coverage of beta cells in the cat retina. Society for Neuroscience Abstracts 20, 1576.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. New York: Plenum.CrossRefGoogle Scholar
Tigges, J., Bos, J. & Tigges, M. (1977). An autoradiographic investigation of the subcortical visual system in chimpanzee. Journal of Comparative Neurology 172, 367–380.CrossRefGoogle ScholarPubMed
Tolhurst, D.J. (1989). Cortical magnification and peripheral innervation density. In Seeing Contour and Colour, ed. Kulkowski, J.J., Dickinson, C.M. & Murray, I.J., pp. 671–677. Oxford: Pergamon Press.Google Scholar
Trevarthen, C.V. (1968). Two mechanisms of vision in primates. Psychologische Forschung 31, 299–337.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213–235.CrossRefGoogle ScholarPubMed
Vakkur, G.J., Bishop, P.O. & Kozak, W. (1963). Visual optics in the cat, including posterior nodal distance and retinal landmarks. Vision Research 3, 289–314.CrossRefGoogle 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
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447–480.CrossRefGoogle ScholarPubMed
Wässle, H., Levick, W.R. & Cleland, B.G. (1975). The distribution of the alpha type of ganglion cells in the cat's retina. Journal of Comparative Neurology 159, 419–437.CrossRefGoogle ScholarPubMed
Wässle, H., Grünert, U., Röhrenbeck, J. & Boycott, B.B. (1989). Cortical magnification factor and the ganglion cell density of the primate retina. Nature 341, 643–646.CrossRefGoogle ScholarPubMed
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
Wilson, J.R. & Sherman, S.M. (1976). Receptive-field characteristics of neurons in cat striate cortex: Changes with visual field eccentricity. Journal of Neurophysiology 39, 512–533.CrossRefGoogle ScholarPubMed
Wilson, M.E. & Toyne, M.J. (1970). Retino-tectal and cortico-tectal projections in Macaca mulatta. Brain Research 24, 395–406.CrossRefGoogle ScholarPubMed
Woolsey, C.N., Marshall, W.H. & Bard, P. (1942). Representation of cutaneous tactile sensibility in the cerebral cortex of the monkey as indicated by evoked potentials. Bulletin of the Johns Hopkins Hospital 70, 399–441.Google Scholar