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GABA-induced inactivation of functionally characterized sites in cat striate cortex: Effects on orientation tuning and direction selectivity

Published online by Cambridge University Press:  02 June 2009

John M. Crook ,
Zoltan F. Kisvárday  and
Ulf T. Eysel
John M. Crook
Affiliation:
Department of Neurophysiology, Faculty of Medicine, Ruhr-University of Bochum, FOB 102148, D-44801 Bochum, Germany
Zoltan F. Kisvárday
Affiliation:
Department of Neurophysiology, Faculty of Medicine, Ruhr-University of Bochum, FOB 102148, D-44801 Bochum, Germany
Ulf T. Eysel
Affiliation:
Department of Neurophysiology, Faculty of Medicine, Ruhr-University of Bochum, FOB 102148, D-44801 Bochum, Germany
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Abstract

Microiontophoresis of γ-aminobutyric acid (GABA) was used to reversibly inactivate small sites of defined orientation/direction specificity in layers II-IV of cat area 17 while single cells were recorded in the same area at a horizontal distance of ~350–700 jam. We compared the effect of inactivating iso-orientation sites (where orientation preference was within 22.5 deg) and cross-orientation sites (where it differed by 45–90 deg) on orientation tuning and directionality. The influence of iso-orientation inactivation was tested in 33 cells, seven of which were subjected to alternate inactivation of two iso-orientation sites with opposite direction preference. Of the resulting 40 inactivations, only two (5%) caused significant changes in orientation tuning, whereas 26 (65%) elicited effects on directionality: namely, an increase or a decrease in response to a cell's preferred direction when its direction preference was the same as that at an inactivation site, and an increase in response to a cell's nonpreferred direction when its direction preference was opposite that at an inactivation site. It is argued that the decreases in response to the preferred direction reflected a reduction in the strength of intracortical iso-orientation excitatory connections, while the increases in response were due to the loss of iso-orientation inhibition. Of 35 cells subjected to cross-orientation inactivation, only six (17%) showed an effect on directionality, whereas 21 (60%) showed significant broadening of orientation tuning, with an increase in mean tuning width at half-height of 126%. The effects on orientation tuning were due to increases in response to nonoptimal orientations. Changes in directionality also resulted from increased responses (to preferred or nonpreferred directions) and were always accompanied by broadening of tuning. Thus, the effects of cross-orientation inactivation were presumably due to the loss of a cross-orientation inhibitory input that contributes mainly to orientation tuning by suppressing responses to nonoptimal orientations. Differential effects of iso-orientation and cross-orientation inactivation could be elicited in the same cell or in different cells from the same inactivation site. The results suggest the involvement of three different intracortical processes in the generation of orientation tuning and direction selectivity in area 17: (1) suppression of responses to nonoptimal orientations and directions as a result of cross-orientation inhibition and iso-orientation inhibition between cells with opposite direction preferences; (2) amplification of responses to optimal stimuli via iso-orientation excitatory connections; and (3) regulation of cortical amplification via iso-orientation inhibition.

Keywords

Cat area 17Orientation/direction selectivityIso-orientation inactivationCross-orientation inactivationIntracortical inhibitionRecurrent excitation
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 1 , January 1997 , pp. 141 - 158
Copyright
Copyright © Cambridge University Press 1997

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References

Ahmed, B., Anderson, J.C., Douglas, R.J., Martin, K.A.C. & Nelson, J.C. (1994). Polyneuronal innervation of spiny stellate neurons in cat visual cortex. Journal of Comparative Neurology 341, 39–49.Google Scholar
Anderson, J.C., Douglas, R.J., Martin, K.A.C. & Nelson, J.C. (1994). Synaptic output of physiologically identified spiny stellate neurons in cat visual cortex. Journal of Comparative Neurology 341, 16–24.Google Scholar
Beaulieu, C. & Colonnier, M. (1985). A laminar analysis of the number of round asymmetrical and flat symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat. Journal of Comparative Neurology 231, 180–189.Google Scholar
Berman, N.E.J., Wilkes, N.E. & Payne, B.R. (1987). Organisation of orientation and direction selectivity in areas 17 and 18 of cat cerebral cortex. Journal of Neurophysiology 58, 676–699.Google Scholar
Berman, N.J., Douglas, R.J. & Martin, K.A.C. (1992). GABA-mediated inhibition in the neural networks of visual cortex. In Progress in Brain Research, Vol. 90, ed. Mize, R.R., Marc, R.E. & Sillito, A.M., pp. 443–476. Amsterdam: Elsevier.Google Scholar
Blakemore, C., Fiorentini, A. & Maffei, L. (1972). A second neural mechanism of binocular depth discrimination. Journal of Physiology (London) 226, 725–740.CrossRefGoogle ScholarPubMed
Bonhoeffer, T., Kim, D.-S., Malonek, D., Shoham, D. & Grinvald, A. (1995) Optical imaging of the layout of functional domains in area 17 and across the area 17/18 border in cat visual cortex. European Journal of Neuroscience 7, 1973–1988.CrossRefGoogle ScholarPubMed
Boyd, J. & Matsubara, J. (1991). Intrinsic connections in cat visual cortex: A combined anterograde and retrograde tracing study. Brain Research 560, 207–215.CrossRefGoogle ScholarPubMed
Chapman, B., Zahs, K.R. & Stryker, M.P. (1991). Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. Journal of Neuroscience 11, 1347–1358.Google Scholar
Creutzfeldt, O.D., Kuhnt, U. & Benevento, L.A. (1974). An intracellular analysis of visual cortical neurones to moving stimuli: Responses in a co-operative neuronal network. Experimental Brain Research 21, 251–274.Google Scholar
Crook, J.M. (1990). Directional tuning of cells in area 18 of the feline visual cortex for visual noise, bar and spot stimuli: A comparison with area 17. Experimental Brain Research 80, 545–561.Google Scholar
Crook, J.M. & Eysel, U.T. (1992). GABA-induced inactivation of functionally characterized sites in cat visual cortex (area 18): Effects on orientation tuning. Journal of Neuroscience 12, 1816–1825.Google Scholar
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, 1–12.CrossRefGoogle ScholarPubMed
Crook, J.M., Kisvárday, Z.F. & Eysel, U.T. (1992 a). Contribution of lateral inhibition to orientation and direction selectivity in cat visual cortex (area 18): GABA-inactivation combined with injections of [3H]-nipecotic acid. In Rhythmogenesis in Neurons and Networks, ed. Elsner, N. & Richter, D., p. 355. New York: Georg Thieme.Google Scholar
Crook, J.M., Kisvárday, Z.F. & Eysel, U.T. (1992 b). Local mechanisms of cortical direction selectivity: GABA-inactivation combined with injections of [3H]-nipecotic acid. Society for Neuroscience Abstracts 18, 1033.Google Scholar
Crook, J.M., Kisvárday, Z.F. & Eysel, U.T. (1996). GABA-induced inactivation of functionally characterized sites in cat visual cortex (area 18): Effects on direction selectivity. Journal of Neurophysiology 75, 2071–2088.Google Scholar
Curtis, D.R. & Crawford, J.M. (1969). Central synaptic transmission: Microelectrophoretic studies. Annual Review of Pharmacology 9, 209–240.Google Scholar
Curtis, D.R. & Johnston, G.A.R. (1974). Amino acid transmitters in the mammalian central nervous system. Reviews of Physiology 69, 98–188.Google Scholar
DeAngelis, G.C., Robson, J.G., Ohzawa, I. &Freeman, R.D. (1992). Organization of suppression in receptive fields of neurons in cat visual cortex. Journal of Neurophysiology 68, 144–163.Google Scholar
Douglas, R.J., Koch, C., Mahowald, M., Martin, K.A.C. & Suarez, H.H. (1995). Recurrent excitation in neocortical circuits. Science 269, 981–985.CrossRefGoogle ScholarPubMed
Douglas, R.J. & Martin, K.A.C. (1991). A functional microcircuit for cat visual cortex. Journal of Physiology (London) 440, 735–769.CrossRefGoogle ScholarPubMed
Douglas, R.J., Martin, K.A.C. & Whitteridge, D. (1988). Selective responses of visual cortical cells do not depend on shunting inhibition. Nature 332, 642–644.Google Scholar
Douglas, R.J., Martin, K.A.C. & Whitteridge, D. (1991). An intracellular analysis of the visual responses of neurones in cat visual cortex. Journal of Physiology (London) 440, 659–696.Google Scholar
Emerson, R.C., Citron, M.C., Vaughn, W.J. & Klein, S.A. (1987). Nonlinear directionally selective subunits in complex cells of cat striate cortex. Journal of Neurophysiology 58, 33–65.Google Scholar
Emerson, R.C. & Gerstein, G.L. (1977). Simple striate neurons in the cat. II. Mechanisms underlying directional asymmetry and directional selectivity. Journal of Neurophysiology 40, 136–155.Google Scholar
Engel, A.K., König, P., Gray, C.M. & Singer, W. (1990). Stimulus-dependent neuronal oscillations in cat visual cortex: Inter-columnar interaction as determined by cross-correlation analysis. European Journal of Neuroscience 2, 588–606.Google Scholar
Eysel, U.T., Crook, J.M. & Machemer, H.F. (1990). GABA-induced remote inactivation reveals cross-orientation inhibition in cat striate cortex. Experimental Brain Research 80, 626–630.Google Scholar
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, 657–675.CrossRefGoogle ScholarPubMed
Ferster, D. (1986). Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. Journal of Neuroscience 6, 1284–1301.Google Scholar
Ferster, D. (1987). Origin of orientation selective EPSPs in simple cells of cat visual cortex. Journal of Neuroscience 7, 1780–1791.Google Scholar
Ferster, D., Chung, S. & Wheat, H. (1996). Orientation selectivity of lhalamic input to simple cells of cat visual cortex. Nature 380, 249–252.CrossRefGoogle ScholarPubMed
Ferster, D. & Koch, C. (1987). Neuronal connections underlying orientation selectivity in cat visual cortex. Trends in Neuroscience 10, 487–492.CrossRefGoogle Scholar
Ferster, D. & Lindström, S. (1983). An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. Journal of Physiology 342, 181–215.Google Scholar
Ganz, L. & Felder, R. (1984). Mechanism of directional selectivity in simple neurons of the cat's visual cortex analyzed with stationary flash sequences. Journal of Neurophysiology 51, 294–323.Google Scholar
Carey, L.J. & Powell, T.P.S. (1971). An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proceedings of the Royal Society B (London) 179, 41–63.Google Scholar
Gilbert, C.D. & Wiesel, T.N. (1983). Clustered intrinsic connections in cat visual cortex. Journal of Neuroscience 3, 1116–1133.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, 2432–2442.CrossRefGoogle ScholarPubMed
Goodwin, A.W., Henry, G.H. & Bishop, P.O. (1975). Direction selectivity of simple striate cells: properties and mechanism. Journal of Neurophysiology 38, 1500–1523.Google Scholar
Hammond, P. & Pomfrett, C.J.D. (1991). Interocular mismatch in spatial frequency and directionality characteristics of striate cortical neurones. Experimental Brain Research 85, 631–640.CrossRefGoogle ScholarPubMed
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, 593–614.Google Scholar
Heggelund, P. (1984). Direction asymmetry by moving stimuli and static receptive field plots for simple cells in cat striate cortex. Vision Research 24, 13–16.Google Scholar
Hess, R. & Murata, K. (1974). Effects of glutamate and GABA on specific response properties of neurones in the visual cortex. Experimental Brain Research 21, 285–297.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, 106–154.CrossRefGoogle ScholarPubMed
Innocenti, G.M. & Fiore, L. (1974). Post-synaptic inhibitory components of the responses to moving stimuli in area 17. Brain Research 80, 122–126.Google 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, 475–486.Google Scholar
Kisvárday, Z.F. & Eysel, U.T. (1992). Cellular organization of reciprocal patchy networks in layer Ill of cat visual cortex (area 17). Neuroscience 46, 275–286.CrossRefGoogle Scholar
Kisvárday, Z.F. & Eysel, U.T. (1993). Functional and structural topography of horizontal inhibitory connections in cat visual cortex. European Journal of Neuroscience 5, 1558–1572.Google Scholar
Kisvárday, Z.F., Martin, K.A.C., Freund, T.F., Maglocsky, Z.S., Whitteridge, D. & Somogyi, P. (1986). Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex. Experimental Brain Research 64, 541–552.Google Scholar
Kisvárday, Z.F., Toth, E., Rausch, M. & Eysel, U.T. (1995). Comparison of lateral excitatory and inhibitory connections in cortical orientation maps of the cat. Society for Neuroscience Abstracts 21, 907.Google Scholar
LeVay, S. (1986). Synaptic organisation of claustral and geniculate afferents to the visual cortex of the cat. Journal of Neuroscience 6, 3564–3575.CrossRefGoogle Scholar
LeVay, S. & Gilbert, C.D. (1976). Laminar patterns of geniculocortical projection in the cat. Brain Research 113, 1–19.Google Scholar
Lund, J.S., Henry, G.H., Macqueen, G.L. & Harvey, A.R. (1979). Anatomical organisation of the primary visual cortex (area 17) of the cat. A comparison with area 17 of the monkey. Journal of Comparative Neurology 184, 599–618.Google Scholar
Maex, R. & Orban, G.A. (1996). Model circuit of spiking neurons generating directional selectivity in simple cells. Journal of Neurophysiology 75, 1515–1545.Google Scholar
Martin, K.A.C., Somogyi, P. & Whitteridge, D. (1983). Physiological and morphological properties of identified basket cells in the cat's visual cortex. Experimental Brain Research 50, 193–200.Google Scholar
Martin, K.A.C. & Whitteridge, D. (1984). Form, function and intra-cortical projections of spiny neurones in the striate visual cortex of the cat. Journal of Physiology (London) 353, 463–504.Google Scholar
Morrone, M.C., Burr, D.C. & Maffei, L. (1982). Functional implications of cross-orientation inhibition of cortical visual cells. I. Neuro-physiological evidence. Proceedings of the Royal Society B (London) 216, 335–354.Google Scholar
Nelson, J.I., Kato, H. & Bishop, P.O. (1977). Discrimination of orientation and position disparities by binocularly activated neurons in cat striate cortex. Journal of Neurophysiology 40, 260–283.Google Scholar
Nelson, S., Toth, L., Sheth, B. & Sur, M. (1994). Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science 265, 774–777.Google Scholar
Orban, G.A. (1984). Neunmal Operations in the Visual Cortex. Studies in Brain Function, Vol. 11, Berlin: Springer.Google Scholar
Orban, O.A., Kennedy, H. & Maes, H. (1981). Response to movement of neurons in areas 17 and 18 of the cat: Directional selectivity. Journal of Neurophysiology 45, 1059–1073.Google Scholar
Pei, X., Vidyasagar, T.R., Volgushev, M. & Creutzfeldt, O.D. (1994). Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. Journal of Neuroscience 14, 7130–7140.CrossRefGoogle ScholarPubMed
Peterhans, E., Bishop, P.O. & Camarda, R.M. (1985). Direction selectivity of simple cells in cat striate cortex to moving light bars. I. Relation to stationary flashing bar and moving edge responses. Experimental Brain Research 57, 512–522.Google Scholar
Peters, A. & Payne, B.R. (1993). Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cerebral Cortex 3, 69–78.Google Scholar
Ramoa, A.S., Shadlen, M., Skottun, B.C. & Freeman, R.D. (1986). A comparison of inhibition in orientation and spatial frequency selectivity of cat visual cortex. Nature 321, 237–239.Google Scholar
Sato, H., Daw, N.W. & Fox, K. (1991). An intracellular recording study of stimulus-specific response properties in cat area 17. Brain Research 544, 156–161.Google Scholar
Shmuel, A. & Grinvald, A. (1996). Functional organization for direction of motion and its relationship to orientation maps in cat area 18. Journal of Neuroscience 16, 6945–6964.Google Scholar
Sillito, A.M. (1977). Inhibitory processes underlying the directional specificity of simple, complex and hypercomplex cells in the cat's visual cortex. Journal of Physiology (London) 271, 699–720.Google Scholar
Sillito, A.M. (1979). Inhibitory mechanisms influencing complex cell orientation selectivity and their modification at high resting discharge levels. Journal of Physiology (London) 289, 33–53.Google Scholar
Sillito, A.M. (1992). GABA mediated inhibitory processes in the function of the geniculostriate system. In Progress in Brain Research, Vol. 90, ed. Mize, R.R., Marc, R.E. & Sillito, A.M., pp. 349–384. Amsterdam: Elsevier.Google Scholar
Sillito, A.M., Kemp, J.A., Milson, J.A. & Beradi, N. (1980). A reevaluation of the mechanisms underlying simple cell orientation selectivity. Brain Research 194, 517–520.Google Scholar
Skottun, B.C. & Freeman, R.D. (1984). Stimulus specificity of binocular cells in the cat's visual cortex: Ocular dominance and the matching of left and right eyes. Experimental Brain Research 56, 206–216.Google Scholar
Somers, D.C., Nelson, S.B. & Sur, M. (1995). An emergent model of orientation selectivity in cat visual cortical simple cells. Journal of Neuroscience 15, 5448–5465.Google Scholar
Somogyi, P., Kisvárday, 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, 261–294.Google Scholar
Soodak, R.E., Shapley, R.M. & Kaplan, E. (1987). Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat. Journal of Neurophysiology 58, 267–275.Google Scholar
Suarez, H., Koch, C. & Douglas, R. (1995). Modeling direction selectivity of simple cells in striate visual cortex within the framework of the canonical microcircuit. Journal of Neuroscience 15, 6700–6719.CrossRefGoogle ScholarPubMed
Thompson, K.G., Leventhal, A.G., Zhou, Y. & Liu, D. (1994 a). 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
Thompson, K.G., Zhou, Y. & Leventhal, A.C. (1994 b). Direction-sensitive X and Y cells within the A laminae of the cat's LGNd. Visual Neuroscience 11, 927–938.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, 1160–1170.Google Scholar
Tsumoto, T., Eckart, W. & Creutzfeldt, O.D. (1979). Modification of orientation sensitivity of cat visual cortex neurones by removal of GABA-mediated inhibition. Experimental Brain Research 34, 351–363.Google Scholar
Vidyasagar, T.R. (1987). A model of striate response properties based on geniculate anisotropies. Biological Cybernetics 57, 11–23.Google Scholar
Vidyasagar, T.R. & Heide, W. (1984). Geniculate biases seen with moving sine-wave gratings: Implications for a model of simple cell afferent connectivity. Experimental Brain Research 57, 196–200.Google 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. Experimental Brain Research 46, 157–169.Google Scholar
Volgushev, M., Pei, X., Vidyasagar, T.R. & Creutzfeldt, O.D. (1993). Excitation and inhibition in orientation selectivity of cat visual cortex neurons revealed by whole-cell recordings in vivo. Visual Neuroscience 10, 1151–1155.Google Scholar
Wörgötter, F. & Koch, C. (1991). A detailed model of the primary visual pathway in the cat: Comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity. Journal of Neuroscience 11, 1959–1979.Google Scholar