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Retinotopic and nonretinotopic field potentials in cat visual cortex

Published online by Cambridge University Press:  02 June 2009

M. Kitano
Affiliation:
The Smith-KettlewellEye Research Institute, San Francisco
K. Niiyama
Affiliation:
The Smith-KettlewellEye Research Institute, San Francisco
T. Kasamatsu
Affiliation:
The Smith-KettlewellEye Research Institute, San Francisco
E. E. Sutter
Affiliation:
The Smith-KettlewellEye Research Institute, San Francisco
A. M. Norcia
Affiliation:
The Smith-KettlewellEye Research Institute, San Francisco

Abstract

Two types of field potentials were identified in cat visual cortex using contrast reversal of oriented bar gratings: a short-latency fast-local component with a retinotopic organization similar to that seen with single-unit discharges at the same cortical site, and a slow, nonretinotopic component with a longer peak latency. The slow-distributed component had an extensive receptive field mapped by measuring the amplitude of binary kernels and showed strong inhibitory interactions within the receptive field. The peak latency of the slow-local component increased with distance from the retinotopic center, suggesting a possible conduction delay. Both components showed some orientation bias depending on the laminar location, but the bias could be independent of the orientation preferred by single units in the immediate vicinity. The present findings indicate that locally generated field potentials reflect cortical mechanisms for nonlinear integration over wide areas of the visual field.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1994

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References

Albus, K. & Sieber, B. (1984). On the spatial arrangement of iso-orientation bands in the cat's visual areas 17 and 18 –a C14 deoxy-glucose study. Experimental Brain Research 56, 384388.CrossRefGoogle Scholar
Allman, J., Miezen, F. & McGuinness, E. (1985). Stimulus specific responses from beyond the classical receptive field: Neurophysiological mechanisms for local-global comparisons in visual neurons. Annual Review of Neuroscience 8, 407430.CrossRefGoogle ScholarPubMed
Amitai, Y., Friedman, A., Connors, B.W. & Gutnick, M.J. (1993). Regenerative activity in apical dendrites of pyramidal cells in neo-cortex. Cerebral Cortex 3, 2638.CrossRefGoogle Scholar
Andersen, P., Storm, J. & Wheal, H.V. (1987). Threshold of action potentials evoked by synapses on the dendrites of pyramidal cells of the rat hippocampus in vitro. Journal of Physiology (London) 383, 509526.CrossRefGoogle Scholar
Anderson, P.A., Olavarria, J. & Van Sluyters, R.C. (1988). The overall pattern of ocular dominance bands in cat visual cortex. Journal of Neuroscience 8, 21832200.CrossRefGoogle ScholarPubMed
Barlow, H.P., Derrington, A.M., Harris, L.R. & Lennie, P. (1977). The effects of remote retinal stimulation on the responses of cat retinal ganglion cells. Journal of Physiology 269, 177194.CrossRefGoogle ScholarPubMed
Bishop, P.O., Coombs, J.S. & Henry, G.H. (1973). Receptive fields of simple cells in the cat striate cortex. Journal of Physiology 231, 3160.CrossRefGoogle ScholarPubMed
Blakemore, C. & Tobin, E.A. (1972). Lateral inhibition between orientation detectors in the cat's visual cortex. Experimental Brain Research 15, 439440.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
Cannon, M.W. & Fullenkamp, S.C. (1991). Spatial interactions in apparent contrast: Inhibitory effects among grating patterns of different spatial frequencies, spatial patterns and orientations. Vision Research 31, 19851998.CrossRefGoogle ScholarPubMed
Connors, B.M., Cauller, L.J., Kim, H.G. & Büthoff, I. (1994). Layer I and the excitable apical dendrite: Substrates for intracortical communication. In Structural and Functional Organization of the Neocortex, eds. Albowitz, B., Albus, K., Kuhnt, U., Nothdurft, H.C., & Wahle, P., Heidelberg: Springer-Verlag (in press).Google Scholar
Cowey, A. (1964). Projection of the retina on to striate and prestriate cortex in the squirrel monkey, Saimiri sciureus. Journal of Neurophysiology 27, 366393.CrossRefGoogle Scholar
Creutzfeldt, O.D., Garey, L.J., Kuroda, R. & Wolff, J.R. (1977). The distribution of degenerating axons after small lesions in the intact and isolated visual cortex of the cat. Experimental Brain Research 27, 419440.Google ScholarPubMed
Creutzfeldt, O.D., Kuhnt, U. & Benevento, L.A. (1974). An intra-cellular analysis of visual cortical neurones to moving stimuli: Responses in a cooperative neuronal network. Experimental Brain Research 21, 251274.CrossRefGoogle Scholar
Creutzfeldt, O.D., Rosina, A., Ito, M. & Probst, W. (1969). Visual evoked response of single cells and of EEG in primary visual area of the cat. Journal of Neurophysiology 32, 127139.CrossRefGoogle ScholarPubMed
Derrington, A.M., Lennie, P. & Wright, M.J. (1979). The mechanisms of peripherally evoked responses in retinal ganglion cells. Journal of Physiology (London) 289, 299310.CrossRefGoogle ScholarPubMed
Deschénes, M. (1981). Dendritic spikes induced in fast pyramidal tract neurons by thalamic stimulation. Experimental Brain Research 43, 304308.Google ScholarPubMed
Doty, R.W. (1958). Potentials evoked in cat cerebral cortex by diffuse and by punctiform photic stimuli. Journal of Neurophysiology 21, 437464.CrossRefGoogle ScholarPubMed
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society B (London) 166, 80111.Google ScholarPubMed
Ebersole, J.S. & Kaplan, B.J. (1981). Intracortical evoked potentials of cats elicited by punctate visual stimuli in receptive field peripheries. Brain Research 224, 160164.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
Fetz, E., Toyama, K. & Smith, W. (1991). Synaptic interactions between cortical neurons. In Cerebral Cortex: Vol. 9, ed. Peters, A., pp. 147. New York: Plenum.Google Scholar
Fiorani, M. Jr., Rosa, M.G.P., Gattass, R. & Rocha-Miranda, C.E. (1992). Dynamic surrounds of receptive fields in primate striate cortex: A physiological basis for perceptual completion? Proceedings of the National Academy of Sciences of the U.S.A. 89, 85478551.CrossRefGoogle Scholar
Fischer, B. (1973). Overlap of receptive field centers and representation of the visual field in the cat's optic tract. Vision Research 13, 21132120.CrossRefGoogle ScholarPubMed
Fischer, B. & Krüger, J. (1974). The shift effect in the cat's lateral geniculate neurones. Experimental Brain Research 21, 225227.CrossRefGoogle Scholar
Fisken, R.A., Garey, L.J. & Powell, T.P.S. (1975). The intrinsic association and commisural connections of area 17 of the visual cortex. Philosophical Transactions of the Royal Society B (London) 272, 487536.Google Scholar
Fries, W., Albus, K. & Creutzfeldt, O.D. (1977). Effects of interacting visual patterns on single cell responses in cat's striate cortex. Vision Research 17, 10011008.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
Gilbert, C.D. & Wiesel, T.N. (1983). Clustered intrinsic connections in cat visual cortex. Journal of Neuroscience 3, 11161133.CrossRefGoogle ScholarPubMed
Gilbert, C.D. & Wiesel, T.N. (1989). Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex. Journal of Neuroscience 9, 24322442.CrossRefGoogle ScholarPubMed
Gilbert, C.D., Hirsch, J.A. & Wiesel, T.N. (1990). Lateral interactions in visual cortex. In Cold Spring Harbor Symposia on Quantitative Biology, Vol. LV, pp. 663677. New York: Cold Spring Harbor Laboratory Press.Google Scholar
Grinvald, A., Ts'o, D.Y., Frostig, R.D., Lieke, E., Arieli, A. & Hildesheim, R. (1989). Optical imaging of neuronal activity in the visual cortex. In Neural Mechanisms of Visual Perception, ed. Lam, D.M.K. & Gilbert, C.D. pp. 117136. The Woodlands, Texas: Portfolio Publishing.Google Scholar
Hammond, P. & Mackay, D.M. (1981). Modularity influences of moving textured backgrounds on responsiveness of simple cells in feline striate cortex. Journal of Physiology (London) 319, 431442.CrossRefGoogle Scholar
Hata, Y., Tsumoto, T., Sato, H. & Tamura, H. (1991). Horizontal interactions between visual cortical neurones studied by cross-correlation analysis in the cat. Journal of Physiology (London) 441, 593614.CrossRefGoogle ScholarPubMed
Heeger, D.J. (1992 a). Normalization of cell responses in cat striate cortex. Visual Neuroscience 9, 181197.CrossRefGoogle ScholarPubMed
Heeger, D.J. (1992 b). Half-squaring in responses of cat striate cells. Visual Neuroscience 9, 427443.CrossRefGoogle ScholarPubMed
Heeger, D.J. & Adelson, E.H. (1989). Mechanisms for extracting local orientation. Association for Research in Vision and Ophthalmology Abstracts 30, 110.Google Scholar
Heeley, D.W. (1979). A perceived spatial frequency shift at orientations orthogonal to adapting gratings. Vision Research 19, 12291236.CrossRefGoogle ScholarPubMed
Herreras, O. (1990). Propagating dendritic action potential mediates synaptic transmission in CA1 pyramidal cells in situ. Journal of Neurophysiology 64, 14291441.CrossRefGoogle ScholarPubMed
Hill, D.R. & Bowery, N.G. (1981). 3H-Baclofen and 3H-GABA bind to bicuculline-insensitive GABAb sites in rat brain. Nature 290, 149152.CrossRefGoogle Scholar
Hirsch, J. & Gilbert, C.D. (1991). Synaptic physiology of horizontal connections in the cat's visual cortex. Journal of Neuroscience 11, 18001809.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976). Linear and non-linear spatial subunits in Y cat retinal ganglion cells. Brain Research 83, 391403.Google 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
Hubel, D.H. & Wiesel, T.N. (1974). Uniformity of monkey striate cortex: A parallel relationship between size, scatter, and magnification factor. Journal of Comparative Neurology 158, 295306.CrossRefGoogle ScholarPubMed
Huguenard, J.R., Hamill, O.P. & Prince, D.A. (1989). Sodium channels in dendrites of rat cortical pyramidal neurons. Proceedings of the National Academy of Sciences of the U.S.A. 86, 24732477.CrossRefGoogle ScholarPubMed
Ikeda, H. & Wright, M.J. (1972). Functional organization of the periphery effect in retinal ganglion cells. Vision Research 12, 18571879.CrossRefGoogle ScholarPubMed
Innocenti, G.M. (1986). General organization of callosal connections in the cerebral cortex. In Cerebral Cortex: Vol. 5 Sensory-Motor Areas and Aspects of Cortical Connectivity, ed. Jones, E.G. & Peters, A., pp. 291353. New York: Plenum.Google Scholar
Jones, B.H. (1970). Responses of single neurons in cat visual cortex to a simple and more complex stimulus. American Journal of Physiology 218, 11021107.CrossRefGoogle ScholarPubMed
Kasamatsu, T., Kitano, M., Sutter, E.E. & Norcia, A.M. (1991). Intracortical interactions in cat visual cortex: Evidence from post-synaptic field potentials. Society for Neuroscience Abstracts 17, 1089.Google Scholar
Kitano, M., Kasamatsu, T. & Norcia, A.M. (1990). Intracortical connectivity revealed by evoked potentials in cat visual cortex. Society for Neuroscience Abstracts 16, 569.Google Scholar
Kitano, M., Kasamatsu, T., Norcia, A.M. & Sutter, E.E. (1991). Experience-dependent intracortical interactions in cat visual cortex: Evidence from postsynaptic field potentials. Society for Neuroscience Abstracts 17, 1089.Google Scholar
Kitano, M., Kasamatsu, T., Norcia, A.M. & Sutter, E.E. (1994). Long-range propagation of field potentials in cat visual cortex (submitted).Google Scholar
Knierim, J.J. & Van Essen, D.C. (1992). Neuronal responses to static texture patterns in area V1 of the alert macaque monkey. Journal of Neurophysiology 67, 961980.CrossRefGoogle ScholarPubMed
Koch, C., Zador, A. & Brown, T.H. (1992). Dendritic spines: convergence of theory and experiment. Science 256, 973974.CrossRefGoogle ScholarPubMed
Krüger, J. & Fischer, B. (1973). Strong periphery effect in cat retinal ganglion cells. Excitatory responses in ON- and OFF-center neurones to single grid displacements. Experimental Brain Research 18, 316318.CrossRefGoogle ScholarPubMed
Kumar, T. & Glaser, D.A. (1991). Influence of remote objects on local depth perception. Vision Research 31, 16871699.CrossRefGoogle ScholarPubMed
Land, E.H. (1983). Recent advances in retinex theory and some implications for cortical computation: Color vision and the natural image. Proceedings of the National Academy of Sciences of the U.S.A. 80, 51635169.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medicine and Biological Engineering 10, 510515.CrossRefGoogle ScholarPubMed
Levick, W.R., Oyster, C. & Davis, D. (1965). Evidence that McIlwain's periphery effect is not a stray light artifact. Journal of Neurophysiology 28, 555559.CrossRefGoogle Scholar
Llinas, R. & Sugimori, M. (1980). Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. Journal of Physiology (London) 305, 197213.CrossRefGoogle ScholarPubMed
Löwel, S., Bischof, H.-J., Leutenecker, B. & Singer, W. (1988). Topographic relations between ocular dominance and orientation columns in the cat striate cortex. Experimental Brain Research 71, 3346.CrossRefGoogle ScholarPubMed
Luhmann, H.J., Singer, W. & Martinez-Millán, L. (1990 a). Horizontal interactions in cat striate cortex: I. Anatomical substrate and postnatal development. European Journal of Neuroscience 2, 344357.CrossRefGoogle ScholarPubMed
Luhmann, H.J., Greuel, J.M. & Singer, W. (1990 b). Horizontal interactions in cat striate cortex: II. A current source-density analysis. European Journal of Neuroscience 2, 358368.CrossRefGoogle ScholarPubMed
Maffei, L. & Fiorentini, A. (1976). The unresponsive regions of visual cortical receptive fields. Vision Research 16, 11311139.CrossRefGoogle ScholarPubMed
Martin, K.A.C. & Whitteridge, D. (1984). Form, function and intracortical projections of spiny neurones in striate visual cortex of the cat. Journal of Physiology (London) 353, 463504.CrossRefGoogle ScholarPubMed
Mason, A., Nicoll, A. & Stratford, K. (1991). Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. Journal of Neuroscience 11, 7284.CrossRefGoogle ScholarPubMed
Matsubara, J., Cynader, M., Swindale, N.V. & Stryker, M.P. (1985). Intrinsic projections within visual cortex: Evidence for orientation specific local connections. Proceedings of the National Academy of Sciences of the U.S.A. 82, 935939.CrossRefGoogle ScholarPubMed
Matsubara, J., Cynader, M. & Swindale, N.V. (1987). Anatomical properties and physiological correlates of the intrinsic connections in cat area 18. Journal of Neuroscience 7, 14281446.CrossRefGoogle ScholarPubMed
Masukawa, L.M. & Prince, D.A. (1984). Synaptic control of excitability in isolated dendrites of hippocampal neurons. Journal of Neuroscience 4, 217227.CrossRefGoogle ScholarPubMed
McGuire, B.A., Gilbert, C.D., Rivlin, P.K. & Wiesel, T.N. (1991). Targets of horizontal connections in macaque primary visual cortex. Journal of Comparative Neurology 305, 370392.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1964). Receptive fields of optic tract axons and lateral geniculate cells: Peripheral extent and barbiturate sensitivity. Journal of Neurophysiology 27, 11541173.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1966). Some evidence concerning the physiological basis of the periphery effect in the cat's retina. Experimental Brain Research 1, 265271.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1975). Visual receptive fields and their images in superior colliculus of the cat. Journal of Neurophysiology 38, 219230.CrossRefGoogle ScholarPubMed
Michalski, A., Gerstein, G.L., Czarkowska, J. & Tarnecki, R. (1983). Interactions between cat striate cortex neurons. Experimental Brain Research 51, 97107.CrossRefGoogle ScholarPubMed
Mitzdorf, U. (1985). Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiological Reviews 65, 37100.CrossRefGoogle ScholarPubMed
Mitzdorf, U. (1986). The physiological causes of VEP: Current source density analysis of electrically and visually evoked potentials. In Evoked Potentials, ed. Cracco, R.Q. & Bodis-Wollner, I., pp. 141154. New York: Alan R. Liss.Google Scholar
Morrone, M.C. & Burr, D.C. (1986). Evidence for the existence and development of visual inhibition in humans. Nature 321, 235237.CrossRefGoogle ScholarPubMed
Nelson, J.I. & Frost, B. (1978). Orientation selective inhibition from beyond the classic visual receptive field. Brain Research 139, 359365.CrossRefGoogle ScholarPubMed
Niiyama, K., Kasamatsu, T., Sutter, E.E. & Norcia, A.M. (1993). Response properties of geniculate cells revealed by M-sequence-modulated contrast reversal of bar gratings. Association for Research in Vision and Ophthalmology Abstracts 34, 792.Google Scholar
Ohashi, T., Norcia, A.M., Kasamatsu, T. & Jampolsky, A. (1991). Cortical recovery from effects of monocular deprivation caused by diffusion and occlusion. Brain Research 548, 6373.CrossRefGoogle ScholarPubMed
Rockland, K.S. & Lund, J.S. (1983). Intrinsic laminar lattice connections in primate visual cortex. Journal of Comparative Neurology 216, 303318.CrossRefGoogle ScholarPubMed
Rockland, K.S., Lund, J.S. & Humphrey, A.L. (1982). Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis). Journal of Comparative Neurology 209, 4158.CrossRefGoogle Scholar
Rodieck, R.W., Pettiorew, J.D., Bishop, P.O. & Nikara, T. (1967). Residual eye movements in receptive-field studies of paralyzed cats. Vision Research 7, 107110.CrossRefGoogle ScholarPubMed
Schwarz, C. & Bolz, J. (1991). Functional specificity of a long-range horizontal connection in cat visual cortex: A cross-correlation study. Journal of Neuroscience 11, 29953007.CrossRefGoogle ScholarPubMed
Shatz, C.J., Lindstrom, S. & Wiesel, T.N. (1977). The distribution of afferents representing the right and left eyes in the cat's visual cortex. Brain Research 131, 103116.CrossRefGoogle ScholarPubMed
Snowden, R. J. & Hammett, S.T. (1992). Subtractive and divisive adaptation in the human visual system. Nature 355, 248250.CrossRefGoogle ScholarPubMed
Sutter, E.E. (1985). Multi-input VER and ERG analysis for objective perimetry. Proceedings of the 7th Annual Conference of IEEE Engineering in Medicine and Biology Society 1, 414419.Google Scholar
Sutter, E.E. (1991). The fast m-transform: A fast computation of cross-correlations with binary m-sequences. SIAM Journal on Computing 20, 686694.CrossRefGoogle Scholar
Sutter, E.E. (1992). A deterministic approach to nonlinear systems analysis. In Nonlinear Vision: Determination of Neural Receptive Fields, Function and Networks, ed. Pinter, R.B. & Nabet, B., pp. 171220. Boca Raton, Florida: CRC Press.Google Scholar
Sutter, E.E. & Tran, D. (1992). The field topography of ERG components in man: I. The photopic luminance response. Vision Research 32, 433446.CrossRefGoogle ScholarPubMed
Toyama, K., Kimura, M. & Tanaka, K. (1981 a). Cross-correlational analysis of interneuronal connectivity in cat visual cortex. Journal of Neurophysiology 46, 191201.CrossRefGoogle Scholar
Toyama, K., Kimura, M. & Tanaka, K. (1981 b). Organization of cat visual cortex as investigated by cross-correlational technique. Journal of Neurophysiology 46, 202213.CrossRefGoogle Scholar
Treisman, A. & Gelade, G. (1980). A feature-integration theory of attention. Cognitive Psychology 12, 97136.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
Turner, R.W., Meyers, D.E.R. & Barker, J.L. (1989). Localization of tetrodotoxin-sensitive field potentials of CA1 pyramidal cells in the rat hippocampus. Journal of Neurophysiology 62, 13751387.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, 213236.CrossRefGoogle ScholarPubMed
Van Essen, D.C., Anderson, C.H. & Felleman, D.J. (1992). Information processing in the primate visual system: An integrated systems perspective. Science 255, 419423.CrossRefGoogle ScholarPubMed
Van Essen, D.C. & Maunsell, J.H.R. (1983). Hierarchical organization and functional streams in the visual cortex. Trends in Neuroscience 6, 370375.CrossRefGoogle Scholar
Von Der Heydt, R. & Peterhans, E. (1989). Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity. Journal of Neuroscience 9, 17311748.CrossRefGoogle ScholarPubMed
Wilson, H.R. (1990). Psychophysics of contrast gain control. Association for Research in Vision and Ophthalmology Abstracts 31, 430.Google Scholar
Wong, R.K., Prince, D.A. & Basbaum, A.I. (1979). Intradendritic recordings from hippocampal neurons. Proceedings of the National Academy of Sciences of the U.S.A. 76, 986990.CrossRefGoogle ScholarPubMed
Wong-Riley, M. (1979). Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Research 171, 1128.CrossRefGoogle ScholarPubMed