Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-04T18:01:41.197Z Has data issue: false hasContentIssue false
  • English
  • Français

Stimulus dependence of orientation and direction sensitivity of cat LGNd relay cells without cortical inputs: A comparison with area 17 cells

Published online by Cambridge University Press:  02 June 2009

Kirk G. Thompson ,
Audie G. Leventhal ,
Yifeng Zhou  and
Dan Liu
Kirk G. Thompson
Affiliation:
Department of Anatomy, University of Utah, School of Medicine, Salt Lake City
Audie G. Leventhal
Affiliation:
Department of Anatomy, University of Utah, School of Medicine, Salt Lake City
Yifeng Zhou
Affiliation:
Department of Biology, University of Science and, Technology of China, Hefei, Anhui 230026, People's Republic of China
Dan Liu
Affiliation:
Department of Anatomy, University of Utah, School of Medicine, Salt Lake City
Get access Rights & Permissions [Opens in a new window]

Abstract

The cortical contribution to the orientation and direction sensitivity of LGNd relay cells was investigated by recording the responses of relay cells to drifting sinusoidal gratings of varying spatial frequencies, moving bars, and moving spots in cats in which the visual cortex (areas 17, 18, 19, and LS) was ablated. For comparison, the spatial-frequency dependence of orientation and direction tuning of striate cortical cells was investigated employing the same quantitative techniques used to test LGNd cells. There are no significant differences in the orientation and direction tuning to relay cells in the LGNd of normal and decorticate cats. The orientation and direction sensitivities of cortical cells are dependent on stimulus parameters in a fashion qualitatively similar to that of LGNd cells. The differences in the spatial-frequency bandwidths of LGNd cells and cortical cells may explain many of their differences in orientation and direction tuning. Although factors beyond narrowness of spatial-frequency tuning must exist to account for the much stronger orientation and direction preferences of cells in area 17 when compared to LGNd cells, the evidence suggests that the orientation and direction biases present in the afferents to the visual cortex may contribute to the orientation and direction selectivities found in cortical cells.

Keywords

Visual cortexLateral geniculate nucleusReceptive-field properties
Type
Research Articles
Information
Visual Neuroscience , Volume 11 , Issue 5 , September 1994 , pp. 939 - 951
Copyright
Copyright © Cambridge University Press 1994

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

Albrecht, D.G., DeValois, R.L. & Thorell, L.G. (1980). Visual cortical neurons: Are bars or gratings the optimal stimuli? Science 207, 88–90.CrossRefGoogle ScholarPubMed
Albus, K. (1980). The detection of movement direction and effects of contrast reversal in the cat's striate cortex. Vision Research 20, 289–293.CrossRefGoogle ScholarPubMed
Bauer, R. & Dow, B.M. (1989). Complementary global maps for orientation coding in upper and lower layers of the monkey's foveal striate cortex. Experimental Brain Research 76, 503–509.CrossRefGoogle ScholarPubMed
Benevento, L.A., Creutzfeldt, O.D. & Kuhnt, U. (1972). Significance of intracortical inhibition in the visual cortex. Nature 238, 124–126.Google 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, 31–60.CrossRefGoogle ScholarPubMed
Blakemore, C., Garey, L.J. & Vital-Durand, F. (1981). Orientation preferences in the monkey's visual cortex. Journal of Physiology 319, 78.Google Scholar
Campbell, F.W., Cooper, G.F. & Enroth-Cugell, C. (1969). The spatial selectivity of the visual cells of the cat. Journal of Physiology 203, 223–235.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Norton, T.T. (1991). The lateral geniculate nucleus: A review of its physiology and function. In The Neural Basis of Visual function, ed. Leventhal, A.G., pp. 41–84. London: Macmillan.Google Scholar
Casanova, C., Nordmann, J.P., Ohzawa, I. & Freeman, R.D. (1992). Direction selectivity of cells in the cat's striate cortex: Differences between bar and grating stimuli. Visual Neuroscience 9, 505–513.CrossRefGoogle ScholarPubMed
Chapman, B., Kahs, K.R. & Stryker, M.P. (1991). Relation of cortical 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.CrossRefGoogle ScholarPubMed
DeBusk, B.C., Bonds, A.B. & DeBruyn, E.J. (1992). Spike clustering in cat cortical cells supports independent encoding of spatial and contrast information. Investigative Ophthalmology and Visual Science (Suppl.) 33, 1255.Google Scholar
Derrington, A.M. & Lennie, P. (1984). Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. Journal of Physiology 357, 219–240.CrossRefGoogle ScholarPubMed
DeValois, R.L., Albrecht, D.G. & Thorell, L.G. (1977). Spatial tuning of LGN and cortical cells in monkey visual system. In Spatial Contrast, ed. Spekreijse, H. & Van Der Tweel, L.H., pp. 60–63. Amsterdam: North Holland.Google Scholar
DeValois, R.L., Albrecht, D.G. & Thorell, L.G. (1978). Cortical cells: bar and edge detectors or spatial frequency filters? In Frontiers in Visual Science, ed. Cool, S.J. & Smith, E.L., pp. 544–556. New York: Springer-Verlag.CrossRefGoogle Scholar
DeValois, R.L., Albrecht, D.G. & Thorell, L.G. (1982). Spatial frequency selectivity of cells in macaque visual cortex. Vision Research 22, 545–559.CrossRefGoogle Scholar
Eysel, U.T., Munche, T. & Wörgötter, F. (1988). Lateral interactions at direction-selective striate neurones in the cat demonstrated by local cortical inactivation. Journal of Physiology 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.CrossRefGoogle ScholarPubMed
Ferster, D. & Koch, C. (1987). Neuronal connections underlying orientation selectivity in cat visual cortex. Trends in Neuroscience 10, 487–492.CrossRefGoogle Scholar
Fregnac, Y. & Imbert, M. (1978). Early development of visual cortical cells in normal and dark-reared kittens: Relationship between orientation selectivity and ocular dominance. Journal of Physiology 278, 27–44.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
Hammond, P. & Pomfrett, C.J.D. (1990). Influence of spatial frequency on tuning and bias for orientation and direction in the cat's striate cortex. Vision Research 30, 359–369.CrossRefGoogle ScholarPubMed
Hata, Y., Tsumoto, T., Sato, H., Hagigara, K. & Tamura, H. (1988). Inhibition contributes to orientation selectivity in visual cortex of cat. Nature 335, 815–817.CrossRefGoogle ScholarPubMed
Hawken, M.J., Parker, A.J. & Lund, J.S. (1988). Laminar organization and contrast sensitivity of direction selective cells in the striate cortex of the old world monkey. Journal of Neuroscience 8, 3541–3548.CrossRefGoogle ScholarPubMed
Heggelund, P. (1981). Receptive field organization of simple cells in cat striate cortex. Experimental Brain Research 42, 89–98.Google ScholarPubMed
Heggelund, P. (1986). Quantitative studies of the discharge fields of single cells in cat striate cortex. Journal of Physiology 37, 272–292.Google Scholar
Henry, G.H., Dreher, B. & Bishop, P.O. (1974). Orientation specificity of cells in cat striate cortex. Journal of Neurophysiology 37, 1394–1409.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1962). Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. Journal of Physiology 160, 106–154.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215–243.CrossRefGoogle ScholarPubMed
Kato, H., Bishop, P.O. & Orban, G.A. (1978). Hypercomplex and the simple/complex cell classification in cat striate cortex. Journal of Neurophysiology 41, 1071–1095.CrossRefGoogle ScholarPubMed
Leventhal, A.G. (1983). Relationship between preferred orientation and receptive field position of neurons in cat striate cortex. Journal of Comparative Neurology 220, 476–483.CrossRefGoogle ScholarPubMed
Leventhal, A.G. & Hirsch, H.V.B. (1978). Receptive-field properties of neurons in different laminae of visual cortex of the cat. Journal of Neurophysiology 41, 948–962.CrossRefGoogle ScholarPubMed
Leventhal, A.G. & Schall, J.D. (1983). Structural bases of orientation sensitivity of cat retinal ganglion cells. Journal of Comparative Neurology 220, 465–475.CrossRefGoogle Scholar
Levick, W.R. & Thibos, L.N. (1982). Analysis of orientation bias in cat retina. Journal of Physiology 329, 243–261.CrossRefGoogle ScholarPubMed
Maex, R. & Orban, G.A. (1991). Subtraction inhibition combined with a spiking threshold accounts for cortical direction selectivity. Proceedings of the National Academy of Sciences of the U.S.A. 88, 3549–3553.CrossRefGoogle ScholarPubMed
Maffei, L. (1978). Spatial frequency channels: Neural mechanisms. Handbook of Sensory Physiology 8, 39–66.Google Scholar
Morrone, M.C., Burr, D.C. & Maffel, L. (1982). Functional implications of cross-orientation inhibition of cortical visual cells I. Neurophysiological evidence. Proceedings of the Royal Society B 216, 335–354.Google ScholarPubMed
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978). Spatial summation in the receptive fields of simple cells in the cat's striate cortex. Journal of Physiology 283, 53–77.CrossRefGoogle ScholarPubMed
Norton, T.T., Holdefer, R.N. & Godwin, D.W. (1989). Effects of bicuculline on receptive-field centre sensitivity of relay cells in the lateral geniculate nucleus. Brain Research 488, 348–352.CrossRefGoogle ScholarPubMed
Orban, G.A. (1984). Neuronal operations in the visual cortex. In Studies of Brain Function, Vol. 8., ed. Barlow, H.B., Bullock, T.H., Florey, E., Grusser, O.J. & Peters, A., New York: Springer-Verlag.Google Scholar
Payne, B.R. & Berman, N. (1983). Functional organization of neurons in the cat striate cortex: Variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in visual-field map. Journal of Neurophysiology 49, 1051–1072.CrossRefGoogle ScholarPubMed
Saul, A.B. & Humphrey, A.L. (1992). Temporal-frequency tuning of direction selectivity in cat visual cortex. Visual Neuroscience 8, 365–372.CrossRefGoogle ScholarPubMed
Schall, J.D., Vitek, D.J. & Leventhal, A.G. (1986). Retinal constraints on orientation specificity in cat visual cortex. Journal of Neuroscience 6, 823–836.CrossRefGoogle ScholarPubMed
Shou, T. & Leventhal, A.G. (1989). Organized arrangement of orientation sensitive relay cells in the cat's dorsal lateral geniculate nucleus. Journal of Neuroscience 9, 4287–4302.CrossRefGoogle ScholarPubMed
Shou, T., Ruan, D. & Zhou, Y. (1986). The orientation bias of LGN neurons shows topographic relation to area centralis in the cat retina. Experimental Brain Research 64, 233–236.CrossRefGoogle ScholarPubMed
Sillito, A.M. (1975). The contribution of inhibitory mechanisms to the receptive field properties of neurons in the striate cortex of the cat. Journal of Physiology 250, 305–329.CrossRefGoogle Scholar
Sillito, A.M., Kemp, J.A., Milson, J.A. & Bernardi, N. (1980). A reevaluation of the mechanisms underlying simple cell orientation selectivity. Brain Research 194, 517–520.CrossRefGoogle ScholarPubMed
So, Y.T. & Shapley, R.M. (1981). Spatial properties of X and Y cells in the lateral geniculate nucleus of the cat and conduction velocities of their inputs. Experimental Brain Research 36, 533–550.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.CrossRefGoogle ScholarPubMed
Thompson, K.G., Zhou, Y. & Leventhal, A.G. (1994). Direction sensitive X and Y cells within the A laminae of the cat's LGNd. Visual Neuroscience 11, 927–938.CrossRefGoogle ScholarPubMed
Tolhurst, D.J. & Thompson, I.D. (1981). On the variety of spatial frequency selectivities shown by neurones in area 17 of the cat. Proceedings of the Royal Society B (London) 213, 183–199.Google ScholarPubMed
Tolhurst, D.J., Movshon, J.A. & Dean, A.F. (1983). The statistical reliability of signals in single neurons in cat and monkey visual cortex. Vision Research 23, 775–785.CrossRefGoogle Scholar
Tolhurst, D.J. & Dean, A.F. (1991). Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex. Visual Neuroscience 6, 421–428.CrossRefGoogle ScholarPubMed
Ts'o, D., 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.CrossRefGoogle ScholarPubMed
Vidyasagar, T.R. (1984). Contribution of inhibitory mechanisms to the orientation sensitivity of LGNd neurones. Experimental Brain Research 55, 192–195.CrossRefGoogle Scholar
Vidyasagar, T.R. (1987). A model of striate response properties based on geniculate anisotropies. Biological Cybernetics 57, 196–200.CrossRefGoogle Scholar
Vidyasagar, T.R. & Urbas, J.V. (1982). Orientation sensitivity of cat LGNd neurones with and without inputs from visual cortical areas 17 and 18. Experimental Brain Research 46, 157–169.CrossRefGoogle Scholar
Vidyasagar, T.R. & Heide, W. (1984). Geniculate orientation biases seen with moving sine wave gratings: Implications for a model of simple cell afferent connectivity. Experimental Brain Research 57, 196–200.CrossRefGoogle Scholar
Vidyasagar, T.R. & Siguenza, J.A. (1985). Relationship between orientation tuning and spatial frequency in neurones of cat area 17. Experimental Brain Research 57, 628–631.CrossRefGoogle ScholarPubMed
Vidyasagar, T.R. & Henry, G.H. (1990). Relationship between preferred orientation and ordinal position in neurones of cat striate cortex. Visual Neuroscience 5, 565–569.CrossRefGoogle ScholarPubMed
Wörgötter, F. & Eysel, U.T. (1991). Topographical aspects of intra-cortical excitation and inhibition contributing to orientation specificity in area 17 of the cat visual cortex. European Journal of Neuroscience 3, 1232–1244.CrossRefGoogle Scholar
Wörgötter, F., Niebur, E. & Koch, C. (1991). Isotropic connections generate functional asymmetrical behavior in visual cortical cells. Journal of Neurophysiology 66, 444–459.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed