Spatial receptive-field structure of cat retinal W cells

We have used frequency-domain methods to characterize the spatial receptive-field structure of cat retinal W cells. For most ON- and OFF-center tonic and phasic W cells, measurements of responsivity to drifting gratings at various spatial frequencies could be adequately described by a difference-of-Gaussians (DOG) function, consistent with the presence of center and surround mechanisms that are approximately Gaussian in shape and whose signals are combined additively. Estimates of the responsivity of the center mechanisms of tonic and phasic W cells were similar, but both were significantly lower than the corresponding values for X or Y cells. The width of the center mechanisms of tonic W cells, phasic W cells, and Y cells did not differ significantly from each other, but all were significantly larger than the width of X-cell centers. Surround parameters did not vary significantly among the four groups of ganglion cells. Measurements of contrast gain in both tonic and phasic W cells gave values that were significantly lower than in X or Y cells. Virtually all of the phasic W cells in our sample displayed evidence of spatial non-linearities in their receptive fields, in the form of either d.c. responses to drifting sine-wave gratings or second harmonic responses to counterphased gratings. The spatial resolution of the mechanism underlying these nonlinearities was typically higher than that of the center mechanism of these cells. Most tonic W cells exhibited linear spatial summation, although a subset gave strong second harmonic responses to counterphased gratings. Spatial-responsivity measurements for most ON-OFF and directionally selective W cells were not adequately described by DOG functions. These cells did, however, show evidence of spatial nonlinearities similar to those seen in phasic W cells. Suppressed-by-contrast cells gave both modulated and unmodulated responses to drifting gratings which both appeared to involved rectification, but which differed from each other in both spatial resolution and contrast gain. These data confirm earlier reports that the receptive fields of tonic and most ON- or OFF-center phasic W cells appear to include classical center and surround mechanisms. However, the receptive fields of some phasic cells, as well as ON-OFF and directionally selective W cells may have quite different structures. Our results also suggest that phasic, ON-OFF, directionally selective, suppressed-by-contrast, and a subset of tonic W cells may all receive nonlinear inputs with characteristics similar to those described in the receptive fields of retinal Y cells.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  A J Sefton,et al.  Properties of neurons in cat's dorsal lateral geniculate nucleus: A comparison between medial interlaminar and laminated parts of the nucleus , 1979, The Journal of comparative neurology.

[2]  J. Nathans,et al.  Molecular genetics of human color vision: the genes encoding blue, green, and red pigments. , 1986, Science.

[3]  P. Lennie,et al.  The influence of temporal frequency and adaptation level on receptive field organization of retinal ganglion cells in cat , 1982, The Journal of physiology.

[4]  A. Leventhal,et al.  The afferent ganglion cells and cortical projections of the retinal recipient zone (RRZ) of the cat's ‘pulvinar complex’ , 1980, The Journal of comparative neurology.

[5]  J. Stone,et al.  Properties of ganglion cells in the visual streak of the cat's retina , 1976, The Journal of comparative neurology.

[6]  W. Levick,et al.  Lateral geniculate relay of slowly conducting retinal afferents to cat visual cortex. , 1976, The Journal of physiology.

[7]  M Sur,et al.  Linear and nonlinear W-cells in C-laminae of the cat's lateral geniculate nucleus. , 1982, Journal of neurophysiology.

[8]  W. Levick,et al.  Bimodal receptive fields of cat retinal ganglion cells , 1983, Vision Research.

[9]  C. Mason,et al.  Morphology of retino-geniculate axons in the cat , 1979, Neuroscience.

[10]  J. Stone,et al.  Naming of neurones. Classification and naming of cat retinal ganglion cells. , 1977, Brain, behavior and evolution.

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

[12]  Y. Fukuda,et al.  Electron microscopic analysis of amacrine and bipolar cell inputs on Y-, X- and W-cells in the cat retina , 1985, Brain Research.

[13]  J. Victor.  The dynamics of the cat retinal X cell centre. , 1987, The Journal of physiology.

[14]  R. Shapley,et al.  Fine structure of receptive-field centers of X and Y cells of the cat , 1991, Visual Neuroscience.

[15]  R. Shapley,et al.  The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[16]  R. Shapley,et al.  The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry , 1984, Vision Research.

[17]  C. Enroth-Cugell,et al.  Spatiotemporal frequency responses of cat retinal ganglion cells , 1987, The Journal of general physiology.

[18]  L. R. Stanford,et al.  W-cells in the cat retina: correlated morphological and physiological evidence for two distinct classes. , 1987, Journal of neurophysiology.

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

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

[21]  R W Rodieck,et al.  Receptive Fields in the Cat Retina: A New Type , 1967, Science.

[22]  S. Sherman.  Functional organization of the W-, X-, and Y- cell pathways in the cat: A review and hypothesis , 1985 .

[23]  J. Stone,et al.  Specialized Receptive Fields of the Cat's Retina , 1966, Science.

[24]  Roger B. H. Tootell,et al.  Segregation of global and local motion processing in primate middle temporal visual area , 1992, Nature.

[25]  J. Mollon.  "Tho' she kneel'd in that place where they grew..." The uses and origins of primate colour vision. , 1989, The Journal of experimental biology.

[26]  R. W. Rodieck.  Quantitative analysis of cat retinal ganglion cell response to visual stimuli. , 1965, Vision research.

[27]  E. Polley,et al.  An analysis of the retinal afferents to the cat's medial interlaminar nucleus and to its rostral thalamic extension, the “geniculate wing” , 1980, The Journal of comparative neurology.

[28]  S. W. Kuffler.  Discharge patterns and functional organization of mammalian retina. , 1953, Journal of neurophysiology.

[29]  R. W. Rodieck,et al.  Identification, classification and anatomical segregation of cells with X‐like and Y‐like properties in the lateral geniculate nucleus of old‐world primates. , 1976, The Journal of physiology.

[30]  C. Enroth-Cugell,et al.  Responses to sinusoidal gratings of two types of very nonlinear retinal ganglion cells of cat , 1989, Visual Neuroscience.

[31]  R. Shapley,et al.  Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. , 1976, The Journal of physiology.

[32]  R. Shapley,et al.  Nonlinear spatial summation and the contrast gain control of cat retinal ganglion cells. , 1979, The Journal of physiology.

[33]  H. Saito,et al.  Morphology of physiologically identified X‐, Y‐, and W‐type retinal ganglion cells of the cat , 1983, The Journal of comparative neurology.

[34]  P. Lennie,et al.  Spatial frequency analysis in the visual system. , 1985, Annual review of neuroscience.

[35]  C. Enroth-Cugell,et al.  Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements , 1982, Vision Research.

[36]  H. Barlow.  Summation and inhibition in the frog's retina , 1953, The Journal of physiology.

[37]  P. Lennie.  Parallel visual pathways: A review , 1980, Vision Research.

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

[39]  J. Stone,et al.  Properties of relay cells in cat's lateral geniculate nucleus: a comparison of W-cells with X- and Y-cells. , 1976, Journal of neurophysiology.

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

[41]  B. Dreher,et al.  Lack of binocularity in cells of area 19 of cat visual cortex following monocular deprivation , 1982, Brain Research.

[42]  D. Mastronarde.  Two types of cat retinal ganglion cells that are suppressed by contrast , 1985, Vision Research.

[43]  C. Enroth-Cugell,et al.  Spatio‐temporal interactions in cat retinal ganglion cells showing linear spatial summation. , 1983, The Journal of physiology.

[44]  B. Knight,et al.  Contrast gain control in the primate retina: P cells are not X-like, some M cells are , 1992, Visual Neuroscience.

[45]  B. Dreher,et al.  Retinal W‐cell projections to the medial interlaminar nucleus in the cat: Implications for ganglion cell classification , 1982, The Journal of comparative neurology.

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

[47]  W. Levick,et al.  Properties of rarely encountered types of ganglion cells in the cat's retina and on overall classification , 1974, The Journal of physiology.

[48]  R. Shapley,et al.  The effect of contrast on the transfer properties of cat retinal ganglion cells. , 1978, The Journal of physiology.

[49]  L Weiskrantz,et al.  The Ferrier Lecture, 1989 - Outlooks for blindsight: explicit methodologies for implicit processes , 1990, Proceedings of the Royal Society of London. B. Biological Sciences.