Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus

We studied the physiological orientation biases of over 700 relay cells in the cat's dorsal lateral geniculate nucleus (LGNd). Relay cells were sampled at regular intervals along horizontally as well as vertically oriented electrode penetrations in a fashion analogous to that used previously in studies of visual cortex (Hubel and Wiesel, 1962). The strengths of the orientation biases and the distributions of the preferred orientations were determined for different classes of relay cells, relay cells in different layers of the LGNd, and relay cells subserving different parts of the visual field. We find that, at the population level, LGNd cells exhibit about the same degree of orientation bias as do the retinal ganglion cells providing their inputs (see also Soodak et al., 1987). Also, as in the retina (Levick and Thibos, 1982; Leventhal and Schall, 1983), most LGNd cells tend to prefer stimuli oriented radially, i.e., parallel to the line connecting their receptive fields to the area centralis projection. However, the radial bias in the LGNd is weaker than in the retina. Moreover, there is a relative overrepresentation of cells preferring tangentially oriented stimuli in the LGNd but not in the retina. As a result of the overrepresentation of cells preferring radial and tangential stimuli, the overall distribution of preferred orientations varies in regions of the LGNd subserving different parts of the visual field. Reconstructions of our electrode penetrations provide evidence that, unlike in the retina, cells having similar preferred orientations are clustered in the LGNd. This clustering is apparent for all cell types and in all parts of laminae A and A1. The tendency to cluster according to preferred orientation is evident for cells preferring radially, intermediately, and tangentially oriented stimuli and thus is not simply a reflection of the radial bias evident among retinal ganglion cells at the population level. It is already known that cells having inputs from different eyes, on-center, off-center, X-, Y-, W-type, and color-sensitive ganglion cells are distributed nonrandomly in the LGNd of cats and monkeys (for review, see Rodieck, 1979; Stone et al., 1979; Lennie, 1981; Stone, 1983). The finding that relay cells having similar preferred orientations are also distributed nonrandomly suggests that the initial sorting of virtually all properties segregated in visual cortex may begin in the LGNd.

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

[2]  W. Burke,et al.  The identification of single units in central visual pathways , 1962, The Journal of physiology.

[3]  D. Hubel,et al.  Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey. , 1966, Journal of neurophysiology.

[4]  C. Enroth-Cugell,et al.  The contrast sensitivity of retinal ganglion cells of the cat , 1966, The Journal of physiology.

[5]  K. Sanderson,et al.  The projection of the visual field to the lateral geniculate and medial interlaminar nuclei in the cat , 1971, The Journal of comparative neurology.

[6]  R Fernald,et al.  An improved method for plotting retinal landmarks and focusing the eyes. , 1971, Vision research.

[7]  K. Mardia Statistics of Directional Data , 1972 .

[8]  D. Hubel,et al.  Sequence regularity and geometry of orientation columns in the monkey striate cortex , 1974, The Journal of comparative neurology.

[9]  J. Stone,et al.  Properties of cat retinal ganglion cells: a comparison of W-cells with X- and Y-cells. , 1974, Journal of neurophysiology.

[10]  W. Levick,et al.  Brisk and sluggish concentrically organized ganglion cells in the cat's retina , 1974, The Journal of physiology.

[11]  C. Gilbert,et al.  The projections of cells in different layers of the cat's visual cortex , 1975, The Journal of comparative neurology.

[12]  K. Albus A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat , 1975, Experimental brain research.

[13]  R. Shapley,et al.  Quantitative analysis of retinal ganglion cell classifications. , 1976, The Journal of physiology.

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

[15]  Jonathan Stone,et al.  Hierarchical and parallel mechanisms in the organization of visual cortex , 1979, Brain Research Reviews.

[16]  J. Pettigrew,et al.  Improved use of tapetal reflection for eye-position monitoring. , 1979, Investigative ophthalmology & visual science.

[17]  H. Spekreijse,et al.  Visual Pathways , 1981, Documenta Ophthalmologica Proceedings Series.

[18]  B. Boycott,et al.  Morphology and topography of on- and off-alpha cells in the cat retina , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  B. Boycott,et al.  Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations , 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]  A. Leventhal Morphology and distribution of retinal ganglion cells projecting to different layers of the dorsal lateral geniculate nucleus in normal and Siamese cats , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  B. Heller Circular Statistics in Biology, Edward Batschelet. Academic Press, London & New York (1981), 371, Price $69.50 , 1983 .

[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]  W. Levick,et al.  Bimodal receptive fields of cat retinal ganglion cells , 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]  K. Albus,et al.  Orientation bias in the response of kitten LGNd neurons to moving light bars. , 1983, Brain research.

[27]  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.

[28]  Jonathan Stone,et al.  Parallel Processing in the Visual System: The Classification of Retinal Ganglion Cells and its Impact on the Neurobiology of Vision , 1983 .

[29]  A. Leventhal,et al.  Relationship between preferred orientation and receptive field position of neurons in extrastriate cortex (area 19) in the cat , 1984, The Journal of comparative neurology.

[30]  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.

[31]  A. Leventhal,et al.  Retinal ganglion cell dendritic fields in old-world monkeys are oriented radially , 1986, Brain Research.

[32]  R E Soodak,et al.  Two-dimensional modeling of visual receptive fields using Gaussian subunits. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[33]  D. B. Bowling,et al.  The distribution of on‐ and off‐centre X‐ and Y‐like cells in the A layers of the cat's lateral geniculate nucleus. , 1986, The Journal of physiology.

[34]  J D Schall,et al.  Relationships between ganglion cell dendritic structure and retinal topography in the cat , 1987, The Journal of comparative neurology.

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

[36]  K. Albus A quantitative study of the projection area of the central and the paracentral visual field in area 17 of the cat , 1975, Experimental Brain Research.