Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-24T02:47:51.843Z Has data issue: false hasContentIssue false

Visual responsiveness and direction selectivity of cells in area 18 during local reversible inactivation of area 17 in cats

Published online by Cambridge University Press:  02 June 2009

C. Casanova
Affiliation:
School of Physical and Occupational Therapy, McGill University, Montreal, Canada
Y. Michaud
Affiliation:
Departement de Sciences Biologiques et Centre de Recherche en Sciences Neurologiques, Universite de Montreal, Canada
C. Morin
Affiliation:
Departement de Sciences Biologiques et Centre de Recherche en Sciences Neurologiques, Universite de Montreal, Canada
P.A. McKinley
Affiliation:
School of Physical and Occupational Therapy, McGill University, Montreal, Canada
S. Molotchnikoff
Affiliation:
Departement de Sciences Biologiques et Centre de Recherche en Sciences Neurologiques, Universite de Montreal, Canada

Abstract

We have investigated the effects of inactivation of localized sites in area 17 on the visual responses of cells in visuotopically corresponding regions of area 18. Experiments were performed on adult normal cats. The striate cortex was inactivated by the injection of nanoliters of lidocaine hydrochloride or of γ-aminobutyric acid (GABA) dissolved in a staining solution. Responses of the simple and complex cells of area 18 to optimally oriented light and dark bars moving in the two directions of motion were recorded before, during, and after the drug injection. Two main effects are described.

First, for a substantial number of cells, the drug injection provoked an overall reduction of the cell's visual responses. This nonspecific effect largely predominated in the complex cell family (76% of the units affected). This effect is consistent with the presence of long-range excitatory connections in the visual cortex.

Second, the inactivation of area 17 could affect specific receptive-field properties of cells in area 18. The main specific effect was a loss of direction selectivity of a number of cells in area 18, mainly in the simple family (more than 53% of the units affected). The change in direction selectivity comes either from a disinhibitory effect in the nonpreferred direction or from a reduction of response in the preferred direction. It is proposed that the disinhibitory effects were mediated by inhibitory interneurones within area 18. In a very few cases, the change of directional preference was associated with a modification of the cell's response profile.

These results showed that the signals from area 17 are necessary to drive a number of units in area 18, and that area 17 can contribute to, or at least modulate, the receptive-field properties of a large number of cells in the parastriate area.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1992

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

Abramson, B.P. & Chalupa, L.M. (1985). The laminar distribution of cortical connections with the tecto- and cortico-recipient zones in the cat's lateral posterior nucleus. Neuroscience 15, 8195.CrossRefGoogle ScholarPubMed
Albus, K. (1975). A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat. Experimental Brain Research 24, 159179.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Rezak, M. (1976). The cortical projections of the inferior pulvinar and adjacent lateral pulvinar in the rhesus monkey (Macaca mulatto): An autoradiographic study. Brain Research 108, 124.CrossRefGoogle Scholar
Benevento, L.A. & Yoshida, K. (1981). The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. Journal of Comparative Neurology 203, 455474.CrossRefGoogle ScholarPubMed
Bullier, J. & Kennedy, H. (1983). Projection of the lateral geniculate nucleus onto cortical area V2 in the macaque monkey. Experimental Brain Research 53, 168172.CrossRefGoogle ScholarPubMed
Bullier, J., Kennedy, H. & Salinger, W. (1984). Branching and laminar origin of projections between visual cortical areas in the cat. Journal of Comparative Neurology 228, 329341.CrossRefGoogle ScholarPubMed
Camarda, R.M., Peterhans, E. & Bishop, P.O. (1985). Spatial organization of subregions in receptive fields of simple cells in cat striate cortex as revealed by stationary flashing bars and moving edges. Experimental Brain Research 60, 136150.Google ScholarPubMed
Casanova, C. & Molotchnikoff, S. (1990). Influence of the superior colliculus on visual responses of cells in the rabbit's lateral posterior nucleus. Experimental Brain Research 80, 387396.CrossRefGoogle ScholarPubMed
Casanova, C., Michaud, Y., Lachapelle, P. & Molotchnikoff, S. (1991a). Changes of direction selectivity and response profiles of cells in area 18 after inactivation of the cat's striate cortex. Investigative Ophthalmology and Visual Science (Suppl.) 32, 908.Google Scholar
Casanova, C., McKinley, P.A. & Molotchnikoff, S. (1991b). Responsiveness of reorganized primary somatosensory cortex (SI) after local inactivation of normal SI cortex in chronic spinal cats. Somatosensory Motor Research 8, 6576.CrossRefGoogle ScholarPubMed
Crook, J.M., Eysel, U.T. & Machemer, H.F. (1991). Influence of GABA-induced remote inactivation on the orientation tuning of cells in area 18 of feline visual cortex: A comparison with area 17. Neuroscience 40, 112.CrossRefGoogle ScholarPubMed
Curcio, C.A. & Harting, J.K. (1978). Organization of pulvinar afferents to area 18 in the squirrel monkey: Evidence for stripes. Brain Research 143, 155161.CrossRefGoogle ScholarPubMed
Donaldson, I.M.L. & Nash, J.R.G. (1975). The effect of a chronic lesion in cortical area 17 on the visual responses of units in area 18 of the cat. Journal of Physiology (London) 245, 325332.CrossRefGoogle ScholarPubMed
Dreher, B. (1986). Thalamocortical and corticocortical interconnections in the cat visual system: Relation to the mechanisms of information processing. In Visual Neuroscience, ed. Pettigrew, J.D., Sanderson, K.J. & Levick, W.R., pp. 290314. Cambridge: Cambridge University Press.Google Scholar
Dreher, B. & Cottee, L.J. (1975). Visual receptive-field properties of cells in area 18 of cat's cerebral cortex before and after lesions in area 17. Journal of Neurophysiology 38, 735750.CrossRefGoogle ScholarPubMed
Dreher, B., Leventhal, A.G. & Hale, P.T. (1980). Geniculate input to cat visual cortex: A comparison of area 19 with areas 17 and 18. Journal of Neurophysiology 44, 804826.CrossRefGoogle Scholar
Duysens, J., Maes, H. & Orban, G.A. (1987). The velocity dependence of direction selectivity of visual cortical neurones in the cat. Journal of Physiology (London) 387, 95113.CrossRefGoogle ScholarPubMed
Eysel, U.T., Muche, T. & Wörgötter, F. (1988). Lateral interactions at direction-selective striate neurones in the cat demonstrated by local cortical inactivation. Journal of Physiology (London) 399, 657675.CrossRefGoogle ScholarPubMed
Ferrer, J.M.R., Price, D.J. & Blakemore, C. (1988). The organization of corticocortical projections from area 17 to area 18 of the cat's visual cortex. Proceedings of the Royal Society B (London) 233, 7798.Google ScholarPubMed
Gilbert, C.D. (1983). Microcircuitry of the visual cortex. Annual Review in Neuroscience 6, 217247.CrossRefGoogle ScholarPubMed
Gilbert, C.D. (1985). Horizontal integration in the neocortex. Trends in Neuroscience 8, 160165.CrossRefGoogle Scholar
Gilbert, C.D. & Wiesel, T.N. (1979). Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature 280, 120125.CrossRefGoogle ScholarPubMed
Girard, P. & Bullier, J. (1989). Visual activity in area V2 during reversible inactivation of area 17 in the macaque monkey. Journal of Neurophysiology 62, 12871302.CrossRefGoogle ScholarPubMed
Harvey, A.R. (1980). The afferent connexions and laminar distribution of cells in area 18 of the cat. Journal of Physiology (London) 302, 483505.CrossRefGoogle ScholarPubMed
Hess, R., Negishi, K. & Creutfeldt, O. (1975). The horizontal spread of intracortical inhibition in the visual cortex. Experimental Brain Research 22, 415419.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology (London) 160, 106154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1965). Receptive fields and functional architecture in two nonstriate visual areas (18 and 19) of the cat. Journal of Neurophysiology 28, 229289.CrossRefGoogle Scholar
Johnson, R.R. & Burkhalter, A. (1991). Feedback connections in visual cortex contact inhibitory neurons. Society for Neuroscience Abstracts 17, 844.Google Scholar
Kennedy, H., Meissirel, C. & Dehay, C. (1991). Callosal pathways and their compliancy to general rules governing the organization of corticocortical connectivity. In Vision and Visual Dysfunction, Vol. 3, ed. Dreher, B. & Robinson, S.R., pp. 324359. Boca Raton: CRC Press.Google Scholar
Kulikowski, J.J., Bishop, P.O. & Kato, H. (1981). Spatial arrangements of responses by cells in the cat visual cortex to light and dark • bars and edges. Experimental Brain Research 44, 371385.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medical Biological Engineering 10, 510515.CrossRefGoogle ScholarPubMed
Malpeli, J.G. (1983). Activity of cells in area 17 of the cat in absence of input from layer A of the lateral geniculate nucleus. Journal of Neurophysiology 49, 595610.CrossRefGoogle Scholar
Michaud, Y., Casanova, C., McKinley, P.A. & Molotchnikoff, S. (1989). Responsiveness of cells in area 18 after local inactivation of area 17 in cats. Society for Neuroscience Abstracts 15, 1056.Google Scholar
Mignard, M. & Malpeli, J.G. (1991). Paths of information flow through visual cortex. Science 251, 12491251.CrossRefGoogle ScholarPubMed
Molotchnikoff, S. & Hubert, F. (1990). Susceptibility of neurons in area 18a to blockade of area 17 in rats. Brain Research 510, 223228.CrossRefGoogle ScholarPubMed
Montero, V.M. (1981). Topography of the cortico-cortical connections from the striate cortex in the cat. Brain, Behavior, and Evolution 18, 194218.CrossRefGoogle ScholarPubMed
Ooren, M.P. & Hendrickson, A.E. (1977). The distribution of pulvinar terminals in visual areas 17 and 18 of the monkey. Brain Research 137, 343350.Google Scholar
Orban, G.A. (1984). Neuronal operations in the visual cortex. In Studies of the Brain, Vol. 11, ed. Barlow, H.B., Bullock, T.H., Florey, E., Grüsser, O.J. & Peters, A., pp. 186. Berlin: Springer-Verlag.Google Scholar
Orban, G.A., Kennedy, H. & Maes, H. (1981). Response To Movement Of Neurons In Areas 17 And 18 Of The Cat: Direction Selectivity. Journal of Neurophysiology 45, 10591073.CrossRefGoogle ScholarPubMed
Price, D.J. & Blakemore, C. (1985). The postnatal development of the association projection from visual cortical area 17 to area 18 in the cat. Journal of Neuroscience 5, 24432452.CrossRefGoogle ScholarPubMed
Raczkowski, D. & Rosenquist, A. C (1983). Connections Of The Multiple Visual Cortical Areas With The Lateral Posterior-Pulvinar Complex And Adjacent Nuclei In The Cat. Journal of Neuroscience 3, 19121942.CrossRefGoogle ScholarPubMed
Rockland, K.S. & Virga, A. (1990). Organization of individual cortical axons projecting from area VI (area 17) to V2 (area 18) in the macaque monkey. Visual Neuroscience 4, 1128.CrossRefGoogle Scholar
Schiller, P.H. & Malpeli, J.G. (1977). The effect of striate cortex cooling on area 18 cells in the monkey. Brain Research 126, 366369.CrossRefGoogle ScholarPubMed
Sherk, H. (1978). Area 18 cell responses in cat during reversible inactivation of area 17. Journal of Neurophysiology 41, 204215.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1977). Inhibitory processes underlying the directional specificity of simple, complex, and hypercomplex cells in the cat's striate cortex. Journal of Physiology (London) 271, 699720.CrossRefGoogle Scholar
Somogyi, P., Kisvarday, Z.F., Martin, K.A.C. & Whitteridge, D. (1983). Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10, 261294.CrossRefGoogle ScholarPubMed
Stone, J. & Dreher, B. (1973). Projection Of X And Y Cells Of The Cat's Lateral Geniculate Nucleus To Areas 17 And 18 Of The Visual Cortex. Journal of Neurophysiology 36, 551567.CrossRefGoogle ScholarPubMed
Stone, J., Dreher, B. & Leventhal, A. (1979). Hierarchical and parallel mechanisms in the organization of visual cortex. Brain Research Reviews 1, 345394.CrossRefGoogle Scholar
Swadlow, H.A. (1983). Efferent systems of primary visual cortex: A review of structure and function. Brain Research Reviews 6, 124.CrossRefGoogle Scholar
Symonds, L.L. & Rosenquist, A.C. (1984a). Corticocortical connections among visual areas in the cat. Journal of Comparative Neurology 229, 138.CrossRefGoogle ScholarPubMed
Symonds, L.L. & Rosenquist, A.C. (1984b). Laminar origins of visual corticocortical connections in the cat. Journal of Comparative Neurology 229, 3947.CrossRefGoogle ScholarPubMed
Tretter, F., Cynader, M. & Singer, W. (1975). Cat parastriate cortex: A primary or secondary visual area? Journal of Neurophysiology 38, 10991113.CrossRefGoogle ScholarPubMed
Ts'o, D.Y., Gilbert, C.D. & Wiesel, T.N. (1986). Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. Journal of Neuroscience 6, 11601170.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) of the cat. Journal of Comparative Neurology 177, 213236.CrossRefGoogle ScholarPubMed
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of area 18 and 19 in the cat. Journal of Comparative Neurology 185, 657678.CrossRefGoogle Scholar
Weller, R.E. & Kaas, J.H. (1983). Retinotopic patterns of connections of area 17 with visual areas V-Il and MT in macaque monkeys. Journal of Comparative Neurology 220, 253279.CrossRefGoogle Scholar
Wilson, M.E. (1968). Cortico-cortical connexions of the cat visual areas. Journal of Anatomy 102, 375386.Google ScholarPubMed