Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-10T10:33:20.121Z Has data issue: false hasContentIssue false
  • English
  • Français

Corticofugal influences on visual responses in cat superior colliculus: The role of NMDA receptors

Published online by Cambridge University Press:  02 June 2009

K. E. Binns  and
T. E. Salt
K. E. Binns
Affiliation:
Department of Visual Science, Institute of Ophthalmology, University College, London, UK
T. E. Salt
Affiliation:
Department of Visual Science, Institute of Ophthalmology, University College, London, UK
Get access Rights & Permissions [Opens in a new window]

Abstract

The role of N-methyl-D-aspartate (NMDA) receptors in the mediation of cortical inputs to visual neurones in the superficial layers of the superior colliculus (SSC) has been investigated. Extracellular recording with iontophoresis in the SSC of cortically intact cats has demonstrated that visual responses of most neurones were reduced by iontophoretic application of the NMDA receptor antagonist D-2-amino-5-phosphonopentanoate (APS). Following inactivation of areas 17 and 18 of the visual cortex with topical lignocaine, the visual responses of 11, previously AP5-sensitive, neurones were no longer reduced by APS ejection. The cortical input is generally assumed to influence the directional responses of visual neurones in SSC. However, detailed study of the directional bias showed that the degree of directional tuning in SSC neurones was similar to that of retinal ganglion cells, as previously described by others. Moreover, inactivation of the visual cortex with topical lignocaine did not alter the directional bias of SSC neurones. Likewise, the directional bias of SSC neurones was not reduced by iontophoretic ejection of APS in the SSC. These data imply that NMDA receptors have an important role in mediating the cortical input to the SSC. However, cortical input does not appear to be responsible for conferring directional bias upon SSC neurones' visual responsiveness.

Keywords

VisionExcitatory amino acid receptorsOrientation tuning
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 4 , July 1996 , pp. 683 - 694
Copyright
Copyright © Cambridge University Press 1996

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

Adey, W.R. (1974). Biophysical and metabolic bases of cooling effects on cortical membrane potentials in the cat. Experimental Neurology 42, 113–140.CrossRefGoogle ScholarPubMed
Behan, M. (1981). Identification and distribution of retinocollicular terminals in the cat: An electron microscopic autoradiographic analysis. Journal of Comparative Neurology 199, 1–15.CrossRefGoogle Scholar
Berman, N. & Cynader, M. (1972). Comparison of the receptive field organization of the superior colliculus in Siamese and normal cats. Journal of Physiology (London) 224, 363–389.CrossRefGoogle ScholarPubMed
Berman, N. & Cynader, M. (1975). Receptive fields in cat superior colliculus after visual cortex lesions. Journal of Physiology (London) 245, 261–270.CrossRefGoogle ScholarPubMed
Berson, D.M. (1988). Retinal and cortical inputs to cat superior colliculus: Composition, convergence and laminar specificity. Progress Brain Research 75, 17–26.CrossRefGoogle ScholarPubMed
Binns, K.E. & Salt, T.E. (1994). Excitatory amino acid receptors participate synaptic transmission of visual responses in the superficial layers of the cat superior colliculus. European Journal of Neuroscience 6, 161–169.CrossRefGoogle ScholarPubMed
Binns, K.E. & Salt, T.E. (1995 a). Excitatory amino acid receptors modulate habituation of the response to visual stimulation in the cat superior colliculus. Visual Neuroscience 12, 563–571.CrossRefGoogle ScholarPubMed
Binns, K.E. & Salt, T.E. (1995 b). N-Methyl-D-aspartate (NMDA) receptors and cortical influences on visual responses in the superior colliculus (SC) of the anaesthetised cat. Journal of Physiology (London) 485, 11P.Google Scholar
Casanova, C., Michaud, Y., Morin, C., McKinley, P.A. & Molotch-Nikoff, S. (1992). Visual responsiveness and direction selectivity of cells in area 18 during local reversible inactivation of area 17 cats. Visual Neuroscience 9, 581–593.CrossRefGoogle Scholar
Cleland, B.C. & Levick, W.R. (1974). Properties of rarely encountered types of retinal ganglion cells in the cat's retina and an overall classification. Journal of Physiology (London) 240, 457–492.CrossRefGoogle Scholar
Davies, J., Francis, A.A., Jones, A.W. & Watkins, J.C. (1981). 2-Amino-5-phosphonvalerate (2-AP5) a potent and selective antagonist of amino acid-induced and synaptic excitation. Neuroscience Letters 21, 77–81.CrossRefGoogle Scholar
Davies, J., Evans, R.H., Herrling, P.L., Jones, A.W., Olverman, H.J., Pook, P. & Watkins, J.C. (1986). CPP, a new and potent and selective NMDA antagonist. Depression of central neurones responses, affinity for 3H D-AP5 binding sites on membranes and anticonvulsant activity. Brain Research 382, 169–173.CrossRefGoogle ScholarPubMed
Dreher, B. & Hoffman, K.P. (1973). Properties of excitatory and inhibitory regions in the receptive fields of single units of the cat's superior colliculus. Experimental Brain Research 16, 333–353.CrossRefGoogle ScholarPubMed
Einstein, G. & Fitzpatrick, D. (1991). Distribution and morphology of area 17 neurones that project to cat extrastriate cortex. Journal of Comparative Neurology 303, 132–149.CrossRefGoogle Scholar
Ferrer, J.M.R., Kato, N. & Price, D.J. (1992). Organization of association projections from area 17 to areas 18, 19 and to supra sylvian areas the cat's visual cortex. Journal of Comparative Neurology 316, 261–278.CrossRefGoogle Scholar
Fosse, V.M., Heggelund, P., Iversen, E. & Fonnum, F. (1984). Effects of area 17 ablation on neurotransmitter parameters efferents to area 18, lateral geniculate body, pulvinar and superior colliculus in the cat. Neuroscience Letters 52, 323–328.CrossRefGoogle ScholarPubMed
Gartside, l.B. & Lippold, O.C.J. (1967). The production of persistent changes the level of neural activity by brief local cooling of the cerebral cortex of the rat. Journal of Physiology (London) 189, 475–487.CrossRefGoogle ScholarPubMed
Guido, W., Tong, L. & Spear, P.O. (1990). Afferent bases of spatial and temporal frequency processing by neurones in the cat's posteromedial lateral supra sylvian cortex. Journal of Neurophysiology 64, 1636–1651.CrossRefGoogle Scholar
Harting, J.K., Updyke, B.V. & Van Lieshout, D.P. (1992). Corticotectal projections in the cat: Anterograde transport studies of twenty-five cortical areas. Journal of Comparative Neurology 324, 379–414.CrossRefGoogle ScholarPubMed
Heurta, M.F. & Harting, J.K. (1984). The mammalian superior colliculus: Study of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., (pp. 687–773). New York: Plenum Press.CrossRefGoogle Scholar
Jones, H.E. & Sillito, A.M. (1994). Directional asymmetries in the length response profiles of cells in the feline dorsal lateral geniculate nucleus. Journal of Physiology (London) 479.3, 475–486.CrossRefGoogle ScholarPubMed
Leventhal, A.G. & Schall, J.D. (1983). Structural basis of orientation sensitivity of cat retinal ganglion cells. Journal of Comparative Neurology 220, 465–475.CrossRefGoogle ScholarPubMed
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology (London) 329, 243–261.CrossRefGoogle ScholarPubMed
Lund-Karlsen, R. & Fonnum, F. (1978). Evidence for glutamate as a neurotransmitter corticofugal fibres to the dorsal lateral geniculate and superior colliculus in rats. Brain Research 151, 457–467.CrossRefGoogle Scholar
Mayer, M.L., Westbrook, G.L. & Guthrie, P.B. (1984). Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309, 261–263.CrossRefGoogle ScholarPubMed
McIlwain, J.T. & Fields, H.L. (1971). Interaction of cortical and retinal projections on single neurones of cat superior colliculus. Journal of Neurophysiology 34, 763–772.CrossRefGoogle Scholar
McIlwain, J.T. & Buser, P. (1968). Receptive fields of single cells in cat superior colliculus. Experimental Brain Research 5, 314.CrossRefGoogle Scholar
Mendola, J.D. & Payne, B.R. (1993). Directional selectivity and physiological compensation in the superior colliculus following removal of areas 17 and 18. Visual Neuroscience 10, 1019–1026.CrossRefGoogle Scholar
Michael, C.R. (1972). Visual receptive fields of single neurons in superior colliculus of the ground squirrel. Journal of Neurophysiology 35, 815–832.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Mize, R.R. & Murphy, E.H. (1976). Alterations of receptive field properties of superior colliculus cells produced by visual cortex ablations in infant and adult cats. Journal of Comparative Neurology 168, 393–424.CrossRefGoogle ScholarPubMed
Mize, R.R., Spencer, R.F. & Sterling, P. (1982). Two types of GABA-accumulating neurons in the superficial grey layer of the cat superior colliculus. Journal of Comparative Neurology 206, 180–192.CrossRefGoogle ScholarPubMed
Nelson, J.I., Kato, H. & Bishop, P.O. (1977). Discrimination of orientation and position disparities by binocular activated neurones in the cat striate cortex. Journal of Neurophysiology 40, 260–283.CrossRefGoogle Scholar
Nowak, L., Bregestoviski, P., Ascher, P., Herbert, A. & Prochi-Antz, A. (1984). Magnesium gates glutamate activated channels in mouse central neurones. Nature 307, 462–465.CrossRefGoogle ScholarPubMed
Ogasawara, K., McHaffie, J.G. & Stein, B.E. (1984). Two visual corticotectal systems in the cat. Journal of Neurophysiology 52, 1226–1245.CrossRefGoogle Scholar
Rizzolatti, G., Tradardi, V. & Camarda, R. (1970). Unit responses to visual stimuli in the cat's superior colliculus after removal of the visual cortex. Brain Research 24, 336–339.CrossRefGoogle ScholarPubMed
Rosenquist, A.C. & Palmer, L.A. (1971). Visual receptive field properties of cells of the superior colliculus after cortical lesions in the cat. Experimental Neurology 33, 629–652.CrossRefGoogle ScholarPubMed
Rowe, M.H. & Cox, J.F. (1993). Spatial receptive-field structure of cat retinal W cells. Visual Neuroscience 10, 765–779.CrossRefGoogle ScholarPubMed
Sakuria, T., Miyamoto, T. & Okada, Y. (1990). Reduction of glutamate content in rat superior colliculus after retinotectal denervation. Neuroscience Letters 190, 299–303.CrossRefGoogle Scholar
Shou, T. & Leventhal, A.G. (1899). Organized arrangement of orientation-sensitive relay cells in the cats dorsal lateral geniculate nucleus. Journal of Neuroscience 9, 4287–4302.CrossRefGoogle Scholar
Sprague, J.M. (1991). The role of superior colliculus in facilitating visual attention and form perception. Proceedings of the National Academy of Sciences of the U.S.A. 88, 1286–1290.CrossRefGoogle ScholarPubMed
Sterling, P. & Wickelgren, E.G. (1969). Visual receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 1.CrossRefGoogle ScholarPubMed
Thibos, L.N. & Levick, W.R. (1985). Orientation bias of brisk-transient Y-cells of the cat retina for drifting and alternating gratings. Experimental Brain Research 58, 1–10.CrossRefGoogle ScholarPubMed
Thompson, K.G., Leventhal, A.G., Zhou, Y. & Liu, D. (1994). Stimulus dependence of orientation and direction sensitivity of cat LGNd relay cells without cortical inputs: A comparison with area 17 cells. Visual Neuroscience 11, 939–951.CrossRefGoogle ScholarPubMed
Updyke, B.V. (1977). Topographic organization of the projections from cortical areas 17, 18 and 19 onto thalamus, pretectum and superior colliculus in the cat. Journal of Comparative Neurology 183, 81.CrossRefGoogle Scholar
Vidyasagar, T.R. & Urbas, J.V. (1982). Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18. Brain Research 46, 157–169.CrossRefGoogle Scholar
Weyand, T.G., Malpeli, J.G., Lee, C. & Schwark, H.D. (1986). Cat area 17. III. Response properties and orientation anisotropies of corticotectal cells. Journal of Neurophysiology 56, 1088–1101.CrossRefGoogle ScholarPubMed
Wickelgren, B.G. & Sterling, P. (1969). Influence of visual cortex on receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 16–23.CrossRefGoogle ScholarPubMed
Xue, J.T., Kim, C.B.Y., Moore, R.J. & Spear, P.D. (1994). Influence of the superior colliculus on responses of lateral geniculate neurons in the cat. Visual Neuroscience 11, 1059–1076.CrossRefGoogle ScholarPubMed