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Spatio-temporal receptive-field structure of phasic W cells in the cat retina

Published online by Cambridge University Press:  02 June 2009

M.H. Rowe  and
L.A. Palmer
M.H. Rowe
Affiliation:
Department of Biological Sciences, Neurobiology Program, Ohio University, Athens
L.A. Palmer
Affiliation:
Department of Neuroscience, University of Pennsylvania, Philadelphia
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Abstract

The spatio-temporal receptive-field structure of 54 phasic W cells in cat retinas has been examined using the reverse-correlation method of Jones and Palmer (1987). Within this sample, 12 cells had on-center, 16 off-center, and 26 on-off receptive fields. Three of the on-center and seven of the on-off cells were directionally selective. Forty percent of the cells in this sample had local receptive fields consisting of two or more distinct subregions. However, no correlation was observed between the number of subregions in the local receptive field and other response properties such as center sign or direction selectivity. In all cases, individual subregions, including those in on-off cells, appear to be produced by a half-wave rectification of the input signal. For 76% of the cells, these local receptive fields were contained within large suppressive fields which could be seen to extend for at least 10 deg in all directions with no apparent spatial structure. The mechanism producing the suppressive field also appears to involve a rectification of the input signal, and has a relatively high spatial resolution. Furthermore, the suppressive field itself is only responsive to moving or flickering stimuli; large, stationary gratings have no effect on the output of the local receptive-field mechanism. Thus, the overall receptive-field organization of these cells is particularly well suited for detecting local motion. The remaining 24% of cells in the sample lacked suppressive fields, and consequently responded well to large moving stimuli, but these cells were otherwise similar in their receptive-field properties to cells with suppressive fields. The significance of these properties is discussed in the context of the projections of phasic W cells to the superior colliculus and accessory optic system.

Keywords

W cellsLocal motionSuperior colliculusAccessory optic system
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 1 , January 1995 , pp. 117 - 139
Copyright
Copyright © Cambridge University Press 1995

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References

Ballas, I., Hoffmann, K.P. & Wagner, H.J. (1981). Retinal projection to the nucleus of the optic tract in the cat as revealed by retrograde transport of horseradish peroxidase. Neuroscience Letters 26, 197–202.Google Scholar
Barbur, J.L., Harlow, A.J. & Weiskrantz, L. (1994). Spatial and temporal response properties of residual vision in a case of hemianopia. Philosophical Transactions of the Royal Society B (London) 343, 157–166.Google Scholar
Barlow, H.B., Hill, R.M. & Levick, W.R. (1964). Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. Journal of Physiology 173, 377–407.CrossRefGoogle ScholarPubMed
Berman, N. & Cynader, M. (1972). Comparison of receptive-field organization of the superior colliculus in Siamese and normal cats. Journal of Physiology 224, 363–389.CrossRefGoogle ScholarPubMed
Berson, D.M. (1987). Retinal W-cell input to the upper superficial gray layer of the cat's superior colliculus: A conduction velocity analysis. Journal of Neurophysiology 58, 1035–1051.Google Scholar
Berson, D.M. (1988 a). Convergence of retinal W-cell and corticotectal input to cells of the cat superior colliculus. Journal of Neurophysiology 60, 1861–1873.Google Scholar
Berson, D.M. (1988 b). Retinal and cortical inputs to cat superior colliculus: Composition, convergence and laminar specificity. In Progress in Brain Research Vol. 75, ed. Hicks, T.P. & Benedek, G., pp. 17–26. New York: Elsevier.Google Scholar
Berson, D.M. & McLwain, J.T. (1982). Retinal Y-cell activation of deep-layer cells in superior colliculus of the cat. Journal of Neurophysiology 47, 700–714.Google Scholar
Boycott, B.B. & Wassle, H. (1974). The morphological types of ganglion cells of the domestic cat's retina. Journal of Physiology 240, 397–419.Google Scholar
Boyd, J.D. & Matsubara, J.A. (1993). The C-laminae of the cat lateral geniculate selectively target cytochrome oxidase blobs in area 17. Society for Neuroscience Abstracts 19, 140.5.Google Scholar
Casagrande, V.A. (1994). A third parallel visual pathway to primate area VI. Trends in Neurosciences 17, 305–309.Google Scholar
Cleland, B.C. & Levick, W.R. (1974 a). Brisk and sluggish concentrically organized ganglion cells in the cat's retina. Journal of Physiology 240, 421–456.Google Scholar
Cleland, B.G. & Levick, W.R. (1974 b). Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. Journal of Physiology 240, 457–492.Google Scholar
Cleland, B.C., Levick, W.R., Morstyn, R. & Wagner, H.G. (1976). Lateral geniculate relay of slowly conducting retinal afferents to cat visual cortex. Journal of Physiology 255, 299–320.Google Scholar
Crabtree, J.W., Spear, P.D., McCall, M.A., Jones, K.R. & Korn-Guth, S.E. (1986). Contributions of Y- and W-cell pathways to response properties of cat superior colliculus neurons: Comparison of anti-body and deprivation-induced alterations. Journal of Neurophysiology 56, 1157–1173.Google Scholar
Demonasterio, P.M. (1978). Properties of ganglion cells with atypical receptive-field organization in retina of macaques. Journal of Neurophysiology 41, 1435–1449.Google Scholar
Dreher, B. & Hoffmann, K.P. (1973). Properties of excitatory and inhibitory regions in the receptive fields of single units in the cat's superior colliculus. Experimental Brain Research 16, 333–353.Google Scholar
Dreher, B. & Sefton, A.J. (1979). Properties of neurons in the cat's lateral geniculate nucleus: A comparison between medial interlaminar and laminated parts of the nucleus. Journal of Comparative Neurology 183, 47–64.Google Scholar
Eckert, M.P. & Buchsbaum, G. (1993). Efficient coding of natural time varying images in the early visual system. Philosophical Transactions of the Royal Society B (London) 339, 385–395.Google Scholar
Farmer, S.G. & Rodieck, R.W. (1982). Ganglion cells of the cat accessory optic system: Morphology and retinal topography. Journal of Comparative Neurology 205, 190–198.Google Scholar
Fukuda, Y. & Stone, J. (1974). Retinal distribution and central projections of Y-, X-, and W-cells of the cat's retina. Journal of Neurophysiology 37, 749–772.Google Scholar
Garey, L.J., Dreher, B. & Robinson, S.R. (1991). The organization of the visual thalamus. In Vision and Visual Dysfunction, Vol. Ill, Neuroanatomy of the Visual Pathways and Their Retinotopic Organization, ed. Dreher, B. & Robinson, S.R., pp 176–234. Hampshire: Macmillan Press.Google Scholar
Grasse, K.L. & Cynader, M.S. (1982). Electrophysiology of medial terminal nucleus of accessory optic system in the cat. Journal of Neurophysiology 48, 490–504.Google Scholar
Grasse, K.L. & Cynader, M.S. (1984). Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system. Journal of Neurophysiology 51, 276–293.Google Scholar
Guillery, R.W., Geisert, E.E., Polley, E.H. & Mason, C.A. (1980). An analysis of the retinal afferents to the cat's medial interlaminar nucleus and to its rostral thalamic extension, the ‘geniculate wing’. Journal of Comparative Neurology 194, 117–142.CrossRefGoogle Scholar
Hendry, S.H.C. & Yoshioka, T. (1994). A neurochemically distinct third channel in the macaque dorsal lateral geniculate nucleus. Science 264, 575–577.Google Scholar
Hoffmann, K.P. (1973). Conduction velocity in pathways from retina to superior colliculus in the cat: A correlation with receptive-field properties. Journal of Neurophysiology 36, 409–424.Google Scholar
Hoffmann, K.P. & Distler, C. (1989). Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. Journal of Neurophysiology 62, 416–428.CrossRefGoogle ScholarPubMed
Hoffmann, K.P. & Dreher, B. (1973). The spatial organization of the excitatory region of receptive fields in the cat's superior colliculus. Experimental Brain Research 16, 354–370.Google Scholar
Hoffmann, K.P. & Schoppmann, A. (1975). Retinal input to direction selective cells in the nucleus tractus opticus of the cat. Brain Research 99, 359–366.CrossRefGoogle ScholarPubMed
Hoffmann, K.P. & Schoppmann, A. (1981). A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract. Experimental Brain Research 42, 146–157.Google Scholar
Hoffmann, K.P. & Stone, J. (1985). Retinal input to the nucleus of the optic tract of the cat assessed by antidromic activation of ganglion cells. Experimental Brain Research 59, 395–403.Google Scholar
Hughes, A.H. (1976). A supplement to the cat schematic eye. Vision Research 16, 149–154.Google Scholar
Hughes, A.H. (1977). The topography of vision in mammals of contrasting life style: Comparative optics and retinal organization. In Handbook of Sensory Physiology. The Visual System in Vertebrates, ed. Crescitelli, F., pp. 613–756. Berlin: Springer-Verlag.Google Scholar
Itoh, K., Conley, M. & Diamond, I.T. (1981). Different distributions of large and small retinal ganglion cells in the cat after HRP injections of single layers of the lateral geniculate body and the superior colliculus. Brain Research 207, 147–152.CrossRefGoogle ScholarPubMed
Jones, J.D. & Palmer, L.A. (1987). The two-dimensional spatial structure of simple receptive fields in cat striate cortex. Journal of Neurophysiology 58, 1187–1211.CrossRefGoogle ScholarPubMed
Kawamura, S., Fukushfma, N. & Hattori, S. (1979). Topographical origin and ganglion cell type of the retino-pulvinar projection in the cat. Brain Research 173, 419–429.Google Scholar
Kolb, H., Nelson, R. & Mariani, A. (1981). Amacrine cells, bipolar cells and ganglion cells of the cat retina: A golgi study. Vision Research 21, 1081–1114.Google Scholar
Lachica, E.A. & Casagrande, V.A. (1993). The morphology of col-licular and retinal axons ending on small relay (W-like). cells of the primate lateral geniculate nucleus. Visual Neuroscience 10, 403–418.Google Scholar
Lettvin, J.Y., Maturana, H.R., McCulloch, W.S. & Pitts, W.H. (1959). What the frog's eye tells the frog's brain. Proceedings of the Institute of Radio Engineers 47, 1940–1951.Google Scholar
Lettvin, J.Y., Maturana, H.R., Pitts, W.H. & McCulloch, W.S. (1961). Two remarks on the visual system of the frog. In Sensory Communication, ed. Rosenblith, W., pp. 757–776. New York: M.I.T. Press.Google Scholar
Leventhal, A.G., Keens, J. & Tork, I. (1980). The afferent ganglion cells and cortical projections of the retinal recipient zone (RRZ) of the cat's ‘Pulvinar complex’. Journal of Comparative Neurology 194, 535–554.Google Scholar
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1981). Retinal ganglion cell classes in the old world monkey: Morphology and central projections. Science 213, 1139–1142.Google Scholar
Leventhal, A.G., Rodieck, R.W. & Dreher, B. (1985). Central projections of cat retinal ganglion cells. Journal of Comparative Neurology 237, 216–226.Google Scholar
Mason, C.A. & Robson, J.A. (1979). Morphology of retino-geniculate axons in the cat. Neuroscience 4, 79–97.Google Scholar
Mason, R. (1979). Responsiveness of cells in the cat's superior colliculus to textured visual stimuli. Experimental Brain Research 37, 231–240.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1976). Large receptive fields and spatial transformations in the visual system. International Review of Physiology, Neurophysiology, II 10, 223–248.Google Scholar
McIlwain, J.T. (1978). Cat superior colliculus: Extracellular potentials related to W-cell synaptic actions. Journal of Neurophysiology 41, 1343–1358.Google Scholar
McIlwain, J.T. & Buser, P. (1968). Receptive fields of single cells in the cat's superior colliculus. Experimental Brain Research 5, 314–325.Google Scholar
McLean, J. & Palmer, L.A. (1989). Contribution of linear spatiotem-poral receptive-field structure to velocity selectivity of simple cells in area 17 of cat. Vision Research 29, 675–679.Google Scholar
McLean, J., Raab, S. & Palmer, L.A. (1994). Contribution of linear mechanisms to the specification of local motion by simple cells in areas 17 and 18 of the cat. Visual Neuroscience 11, 271–306.Google Scholar
Nakayama, K. (1985). Biological image motion processing: A review. Vision Research 25, 625–660.CrossRefGoogle ScholarPubMed
Ogasawara, K., McHaffie, J.G. & Stein, B.E. (1984). Two visual corticotectal systems in cat. Journal of Neurophysiology 52, 1226–1245.Google Scholar
Olavarria, J.F. & Lia, B. (1993). The distribution of cortico-collicular projection neurons correlates with cytochrome oxidase architecture in striate cortex of macaque monkey. Society for Neuroscience Abstracts 19, 140.6.Google Scholar
Perry, V.H. & Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 1125–1137.CrossRefGoogle Scholar
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.G. (1979). Improved use of tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490–495.Google Scholar
Reid, R.C., Soodak, R.E. & Shapley, R.M. (1991). Direction selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. Journal of Neurophysiology 66, 505–529.Google Scholar
Rizzolatti, G., Tradardi, V. & Camarda, R. (1970). Unit responses to visual stimuli in the cat's superior colliculus after removal of the visual cortex. Brain Research 24, 336–339.Google Scholar
Rizzolatti, G., Camarda, R., Grupp, L.A. & Pisa, M. (1974). Inhibitory effect of remote visual stimuli on the visual responses of the cat superior colliculus: Spatial and temporal factors. Journal of Neurophysiology 37, 1262–1275.Google Scholar
Rosenquist, A.C. & Palmer, L.A. (1971). Visual receptive field properties of cells of the superior colliculus after cortical lesions in the cat. Experimental Neurology 33, 629–652.Google Scholar
Rowe, M.H. (1990). Evidence for degeneration of retinal W-cells following early visual cortical removal in cats. Brain, Behavior, and Evolution 35, 253–267.Google Scholar
Rowe, M.H. (1991). The functional organization of the retina. In Vision and Visual Dysfunction, Vol. III, Neuroanatomy of the Visual Pathways and Their Retinotopic Organization, ed. Dreher, B. & Robinson, S.R., pp. 1–68. Hampshire: Macmillan Press.Google Scholar
Rowe, M.H. & Cox, J.F. (1990). The role of ganglion cell dendritic architecture in increasing the spatial bandwidth of cat retinal W-cells. Society for Neuroscience Abstracts 16, 1217.Google Scholar
Rowe, M.H. & Cox, J.F. (1992). Spatio-temporal response profiles of cat retinal W-cells. Society for Neuroscience Abstracts 18, 1028.Google Scholar
Rowe, M.H. & Cox, J.F. (1993 a). Local and non-local rectified responses of phasic retinal W-cells in the cat. Society for Neuroscience Abstracts 19, 1417.Google Scholar
Rowe, M.H. & Cox, J.F. (1993 b). Spatial receptive-field structure of cat retinal W-cells. Visual Neuroscience 10, 765–779.Google Scholar
Rowe, M.H. & Dreher, B. (1982). Retinal W-cell projections to the medial interlaminar nucleus in the cat: Implications for ganglion cell classification. Brain, Behavior, and Evolution 204, 117–133.Google Scholar
Rowe, M.H. & Stone, J. (1976 a). Properties of ganglion cells in the visual streak of the cat's retina. Journal of Comparative Neurology 169, 99–125.Google Scholar
Rowe, M.H. & Stone, J. (1976 b). Conduction velocity groupings among axons of cat retinal ganglion cells, and their relationship to retinal topography. Experimental Brain Research 25, 339–357.CrossRefGoogle Scholar
Rowe, M.H. & Stone, J. (1977). Naming of neurons: Classification and naming of cat retinal ganglion cells. Brain, Behavior, and Evolution 14, 185–216.Google ScholarPubMed
Rowe, M.H. & Stone, J. (1980 a). Parametric and feature extraction analyses of the receptive fields of visual neurones: Two streams of thought in the study of a sensory pathway. Brain, Behavior, and Evolution 17, 152–163.Google Scholar
Rowe, M.H. & Stone, J. (1980 b). The interpretation of variation in the classification of nerve cells. Brain, Behavior, and Evolution 17, 123–151.Google Scholar
Schiller, P.H. & Malpeli, J.G. (1977). Properties and tectal projections of monkey retinal ganglion cells. Journal of Neurophysiology 40, 428–445.Google Scholar
Shapley, R. & Lennie, P. (1985). Spatial frequency analysis in the visual system. Annual Review of Neuroscience 8, 547–583.Google Scholar
Simpson, J.I. (1984). The accessory optic system. Annual Review of Neuroscience 7, 13–41.Google Scholar
Soodak, R.E., Shapley, R.M. & Kaplan, E. (1991). Fine structure of receptive-field centers of X and Y cells of the cat. Visual Neuroscience 6, 621–628.CrossRefGoogle ScholarPubMed
Spear, P.D. (1991). Functions of extrastriate visual cortex in non-primate species. In Vision and Visual Dysfunction, Vol. IV, The Neural Basis of Visual Function, ed. Leventhal, A.G., pp. 339–370. Hampshire: Macmillan Press.Google Scholar
Spear, P.D., Smith, D.C. & Williams, L.L. (1977). Visual receptive-field properties of single neurons in the cat's ventral lateral geniculate nucleus. Journal of Neurophysiology 40, 390–409.Google Scholar
Stanford, L.R. (1987 a). W-cells in the cat retina: Correlated morphological and physiological evidence for two distinct classes. Journal of Neurophysiology 57, 218–244.Google Scholar
Stanford, L.R. (1987 b). X-cells in the cat retina: Relationships between the morphology and physiology of a class of cat retinal ganglion cells. Journal of Neurophysiology 58, 940–964.Google Scholar
Stein, A., Mullikin, W. & Stevens, J. (1983). The spatiotemporal building blocks of X-, Y- and W-ganglion cell receptive fields of the cat's retina. Experimental Brain Research 49, 341–352.Google Scholar
Sterling, P. (1973). Quantitative mapping with the electron microscope: Retinal terminals in the superior colliculus. Brain Research 54, 347–354.Google Scholar
Sterling, P. & Wickelgren, E.G. (1969). Visual receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 1–15.Google Scholar
Stone, J. (1973). Sampling properties of microelectrodes assessed in the cat's retina. Journal of Neurophysiology 36, 1071–1079.Google Scholar
Stone, J. & Clarke, R. (1980). The morphology of cat retinal ganglion cells: Evidence of further variation in the gamma-cell class. Journal of Comparative Neurology 192, 211–217.Google Scholar
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells: A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 37, 722–748.Google Scholar
Sur, M. & Sherman, S.M. (1982). Linear and nonlinear W-cells in C-laminae of the cat's lateral geniculate nucleus. Journal of Neurophysiology 47, 869–884.Google Scholar
Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. Journal of Physiology 386, 219–246.CrossRefGoogle ScholarPubMed
Victor, J.D. (1988). The dynamics of the cat retinal Y cell subunit. Journal of Physiology 405, 289–320.Google Scholar
Wassle, H. & Illing, R.B. (1980). The retinal projection to the superior colliculus in the cat: A quantitative study with HRP. Journal of Comparative Neurology 190, 333–356.Google Scholar
Wickelgren, B.G. & Sterling, P. (1969). Influence of visual cortex on receptive fields in the superior colliculus of the cat. Journal of Neurophysiology 32, 16–23.Google Scholar
Wilson, P.D., Rowe, M.H. & Stone, J. (1976). Properties of relay cells in cat's lateral geniculate nucleus: A comparison of W-cells with X- and Y-cells. Journal of Neurophysiology 39, 1193–1209.Google Scholar