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

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.

[1]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[2]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[3]  G. F. Cooper,et al.  The spatial selectivity of the visual cells of the cat , 1969, The Journal of physiology.

[4]  O. Creutzfeldt,et al.  Significance of intracortical inhibition in the visual cortex. , 1972, Nature: New biology.

[5]  P. O. Bishop,et al.  Receptive fields of simple cells in the cat striate cortex , 1973, The Journal of physiology.

[6]  P. O. Bishop,et al.  Orientation specificity of cells in cat striate cortex. , 1974, Journal of neurophysiology.

[7]  A. Sillito.  The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. , 1975, The Journal of physiology.

[8]  H. Hirsch,et al.  Receptive-field properties of neurons in different laminae of visual cortex of the cat. , 1978, Journal of neurophysiology.

[9]  Y. Frégnac,et al.  Early development of visual cortical cells in normal and dark‐reared kittens: relationship between orientation selectivity and ocular dominance. , 1978, The Journal of physiology.

[10]  D. G. Albrecht,et al.  Cortical cells ; Bar and edge detectors, or spatial frequency filters , 1978 .

[11]  L. Maffei,et al.  Spatial Frequency Channels: Neural Mechanisms , 1978 .

[12]  P. O. Bishop,et al.  Hypercomplex and simple/complex cell classifications in cat striate cortex. , 1978, Journal of neurophysiology.

[13]  Earl L. Smith,et al.  Frontiers in Visual Science , 1978 .

[14]  J. Movshon,et al.  Spatial summation in the receptive fields of simple cells in the cat's striate cortex. , 1978, The Journal of physiology.

[15]  K. Albus,et al.  The detection of movement direction and effects of contrast reversal in the cat's striate cortex , 1980, Vision Research.

[16]  D. G. Albrecht,et al.  Visual cortical neurons: are bars or gratings the optimal stimuli? , 1980, Science.

[17]  A. Sillito,et al.  A re-evaluation of the mechanisms underlying simple cell orientation selectivity , 1980, Brain Research.

[18]  P. Heggelund,et al.  Receptive field organization of simple cells in cat striate cortex , 1981, Experimental brain research.

[19]  D. Tolhurst,et al.  On the variety of spatial frequency selectivities shown by neurons in area 17 of the cat , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[20]  W. Levick,et al.  Analysis of orientation bias in cat retina , 1982, The Journal of physiology.

[21]  D. Burr,et al.  Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence , 1982, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[22]  D. G. Albrecht,et al.  Spatial frequency selectivity of cells in macaque visual cortex , 1982, Vision Research.

[23]  A. Leventhal,et al.  Relationship between preferred orientation and receptive field position of neurons in cat striate cortex , 1983, The Journal of comparative neurology.

[24]  J. Movshon,et al.  The statistical reliability of signals in single neurons in cat and monkey visual cortex , 1983, Vision Research.

[25]  A. Leventhal,et al.  Structural basis of orientation sensitivity of cat retinal ganglion cells , 1983, The Journal of comparative neurology.

[26]  B R Payne,et al.  Functional organization of neurons in cat striate cortex: variations in preferred orientation and orientation selectivity with receptive-field type, ocular dominance, and location in visual-field map. , 1983, Journal of neurophysiology.

[27]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[28]  T. Wiesel,et al.  Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  J D Schall,et al.  Retinal constraints on orientation specificity in cat visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  D. Ferster.  Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  P Heggelund,et al.  Quantitative studies of the discharge fields of single cells in cat striate cortex. , 1986, The Journal of physiology.

[32]  C. Koch,et al.  Neuronal connections underlying orientation selectivity in cat visual cortex , 1987, Trends in Neurosciences.

[33]  R. Shapley,et al.  Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat. , 1987, Journal of neurophysiology.

[34]  F. Wörgötter,et al.  Lateral interactions at direction‐selective striate neurones in the cat demonstrated by local cortical inactivation. , 1988, The Journal of physiology.

[35]  M. Hawken,et al.  Laminar organization and contrast sensitivity of direction-selective cells in the striate cortex of the Old World monkey , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  H. Tamura,et al.  Inhibition contributes to orientation selectivity in visual cortex of cat , 1988, Nature.

[37]  A. Leventhal,et al.  Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  D. Godwin,et al.  Effects of bicuculline on receptive field center sensitivity of relay cells in the lateral geniculate nucleus , 1989, Brain Research.

[39]  T. Wiesel,et al.  Columnar specificity of intrinsic horizontal and corticocortical connections in cat visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[40]  T R Vidyasagar,et al.  Relationship between preferred orientation and ordinal position in neurones of cat striate cortex , 1990, Visual Neuroscience.

[41]  P. Hammond,et al.  Influence of spatial frequency on tuning and bias for orientation and direction in the cat's striate cortex , 1990, Vision Research.

[42]  D. Tolhurst,et al.  Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex , 1991, Visual Neuroscience.

[43]  M. Stryker,et al.  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 , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  G A Orban,et al.  Subtraction inhibition combined with a spiking threshold accounts for cortical direction selectivity. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[45]  C. Koch,et al.  Isotropic connections generate functional asymmetrical behavior in visual cortical cells. , 1991, Journal of neurophysiology.

[46]  A. Leventhal.  The neural basis of visual function , 1991 .

[47]  C. Koch,et al.  A detailed model of the primary visual pathway in the cat: comparison of afferent excitatory and intracortical inhibitory connection schemes for orientation selectivity , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  F. Wörgötter,et al.  Topographical Aspects of Intracortical Excitation and Inhibition Contributing to Orientation Specificity in Area 17 of the Cat Visual Cortex , 1991, The European journal of neuroscience.

[49]  I. Ohzawa,et al.  Direction selectivity of cells in the cat's striate cortex: Differences between bar and grating stimuli , 1992, Visual Neuroscience.

[50]  A. L. Humphrey,et al.  Temporal-frequency tuning of direction selectivity in cat visual cortex , 1992, Visual Neuroscience.

[51]  A. Leventhal,et al.  Direction-sensitive X and Y cells within the A laminae of the cat's LGNd , 1994, Visual Neuroscience.