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Effect of ambient illumination on the spatial properties of the center and surround of Y-cell receptive fields

Published online by Cambridge University Press:  02 June 2009

J. B. Troy
Affiliation:
Departments of Biomedical Engineering & Neurobiology and Physiology, Northwestern University, Evanston
J. K. Oh
Affiliation:
Departments of Biomedical Engineering & Neurobiology and Physiology, Northwestern University, Evanston
CH. Enroth-Cugell
Affiliation:
Departments of Biomedical Engineering & Neurobiology and Physiology, Northwestern University, Evanston

Abstract

The primary goal of this study was to expand the description of the filtering properties of the Y-cell receptive field, byquantitatively characterizing the spatial filtering properties of the receptive field’s center-and-surround components as a function of adapting light level. A range of more than five orders of magnitude in retinal illuminance were covered, including the vast majority of the cat’s functional range of vision.

Recordings were taken from optic tract fibers of Y cells in cats under general anesthesia. Sinusoidal gratings and a stimulus designed to selectively probe the properties of the surround mechanism were used. The cells’ responses to these stimuli were fit to a Gaussian center-surround receptive-field model, in which six parameters define the properties of the center and surround. Fits were made independently to data collected at each light level and changes in the values of the model’s parameters with illuminance are reported. A set of equations that summarize the changes in parameter values is given. From these summary equations, reasonable estimates of the parameters’ values can be determined across a wide range of illuminances. Hence, a quantitative model of the spatial properties of the center and surround of the Y-cell receptive field can now be derived from these equations for most of the levels of retinal illuminance experienced by a Y cell. The consistency between the description provided by our equations and results from earlier work is considered.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1993

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References

Ahmed, B. (1981). The size and shape of rod and cone centres of cat retinal ganglion cells. Experimental Brain Research 43, 422428.Google ScholarPubMed
Andrews, D.P. & Hammond, P. (1970). Suprathreshold spectral properties of single optic tract fibres in cat, under mesopic adaptation: Cone-rod interaction. Journal of Physiology 209, 83103.CrossRefGoogle ScholarPubMed
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957). Change of organization in the receptive fields of the cat’s retina during dark adaptation. Journal of Physiology 137, 338354.CrossRefGoogle ScholarPubMed
Bloomfield, S.A. (1992). Effects of tetrodotoxin on receptive fields of amacrine and ganglion cells in the rabbit retina. Investigative Ophthalmology and Visual Science (ARVO Abstracts) 33, 1173.Google Scholar
Boycott, B.B. & Wässle, H. (1974). The morphological types of ganglion cells of the domestic cat’s retina. Journal of Physiology 240, 397419.CrossRefGoogle ScholarPubMed
Chan, L.-H., Freeman, A.W. & Cleland, B.G. (1993). The rod-cone shift and its effect on ganglion cells in the cat’s retina. Vision Research 32, 22092219.CrossRefGoogle Scholar
Cleland, B.G. & Enroth-Cucell, Ch. (1966). Cat retinal ganglion cell responses to changing light intensities: Sinusoidal modulation in the time domain. Acta Physiologica Scandinavica 68, 365381.CrossRefGoogle Scholar
Cleland, B.G. & Enroth-Cugell, Ch. (1968). Quantitative aspects of sensitivity and summation in the cat retina. Journal of Physiology 198, 1738.CrossRefGoogle ScholarPubMed
Cleland, B.G. & Enroth-Cugell, Ch. (1970). Quantitative aspects of gain and latency in the cat retina. Journal of Physiology 206, 7391.CrossRefGoogle ScholarPubMed
Cleland, B.G., Levick, W.R. & Sanderson, K.J. (1973). Properties of sustained and transient ganglion cells in the cat retina. Journal of Physiology 228, 649680.CrossRefGoogle ScholarPubMed
Cohen, H.I. & Winters, R.W. (1981). Lateral spread of adaptation in the receptive-field surrounds of cat retinal ganglion cells. Brain Research 204, 194199.CrossRefGoogle ScholarPubMed
Crocker, R.A., Ringo, J., Wolbarsht, M.L. & Wagner, H.G. (1980). Cone contributions to cat retinal ganglion cell receptive fields. Journal of General Physiology 76, 763785.CrossRefGoogle ScholarPubMed
Dacey, D.M. (1989). Axon-bearing amacrine cells of the macaque retina. Journal of Comparative Neurology 284, 275293.CrossRefGoogle Scholar
Daw, N.W. & Pearlman, A.L. (1969). Cat color vision: One cone process or several? Journal of Physiology 201, 745764.CrossRefGoogle ScholarPubMed
Dennis, J.E. Jr, & Schnabel, R.B. (1983). Numerical Methods for Unconstrained Optimization and Nonlinear Equations. Englewood Cliffs, New Jersey: Prentice Hall. 378 pp.Google Scholar
Derrington, A.M. & Lennie, P. (1982). The influence of temporal frequency and adaptation level on receptive-field organization of retinal ganglion cells in cat. Journal of Physiology 333, 343366.CrossRefGoogle ScholarPubMed
Enroth-Cugell, Ch. & Freeman, A.W. (1987). The receptive-field spatial structure of cat retinal Y cells. Journal of Physiology 384, 4979.CrossRefGoogle ScholarPubMed
Enroth-Cugell, Ch. & Lennie, P. (1975). The control of retinal ganglion cell discharge by receptive-field surrounds. Journal of Physiology 247, 551578.CrossRefGoogle ScholarPubMed
Enroth-Cugell, Ch. & Pinto, L. (1972). Properties of the surround-response mechanism of cat retinal ganglion cells and center-surround interaction. Journal of Physiology 220, 403439.CrossRefGoogle Scholar
Enroth-Cugell, Ch. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517552.CrossRefGoogle ScholarPubMed
Enroth-Cugell, Ch., Hertz, B.G. & Lennie, P. (1977 a). Cone signals in the cat’s retina. Journal of Physiology 269, 273296.CrossRefGoogle ScholarPubMed
Enroth-Cugell, Ch., Hertz, B.G. & Lenne, P. (1977 b). Convergence of rod and cone signals in the cat’s retina. Journal of Physiology 269, 297318.CrossRefGoogle ScholarPubMed
Enroth-Cugell, Ch., Robson, J.G., Schweitzer-Tong, D.E. & Watson, A.B. (1983). Spatiotemporal interactions in cat retinal ganglion cells showing linear spatial summation. Journal of Physiology 341, 279307.CrossRefGoogle ScholarPubMed
Freed, M.A. & Sterling, P. (1988). The ON-alpha ganglion cell of the cat retina and its presynaptic cell types. Journal of Neuroscience 8, 23032320.CrossRefGoogle ScholarPubMed
Freeman, A.W. (1991). Spatial characteristics of the contrast-gain control in the cat’s retina. Vision Research 31, 775785.CrossRefGoogle ScholarPubMed
Frishman, L.J. & Linsenmeier, R.A. (1982). Effects of picrotoxin and strychnine on nonlinear responses of Y-type cat retinal ganglion cells. Journal of Physiology 324, 347363.CrossRefGoogle ScholarPubMed
Frishman, L.J., Freeman, A.W., Troy, J.B., Schweitzer-Tong, D.E. & Enroth-Cugell, Ch. (1987). Spatiotemporal frequency responses of cat retinal ganglion cells. Journal of General Physiology 89, 599628.CrossRefGoogle ScholarPubMed
Hammond, P. & Mouat, G.S.V. (1985). The relationship between feline pupil size and luminance. Experimental Brain Research 59, 485490.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976 a). Quantitative analysis of retinal ganglion cell classifications. Journal of Physiology 262, 237264.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976 b). Linear and nonlinear spatial subunits in Y cat retinal ganglion cells. Journal of Physiology 262, 265284.CrossRefGoogle ScholarPubMed
Hughes, A. (1976). A supplement to the schematic cat eye. Vision Research 16, 149154.CrossRefGoogle Scholar
Kaplan, E., Marcus, S. & So, Y.T. (1979). Effects of dark adaptation on spatial and temporal properties of receptive fields in cat lateral geniculate nucleus. Journal of Physiology 294, 561580.CrossRefGoogle ScholarPubMed
Kirby, A.W. & Schweitzer-Tong, D.E. (1981). Gaba-antagonists alter spatial summation in receptive-field centres of rod- but not conedriven cat retinal ganglion Y cells. Journal of Physiology 320, 303308.CrossRefGoogle ScholarPubMed
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.CrossRefGoogle ScholarPubMed
Lennie, P. (1979). Scotopic increment thresholds in retinal ganglion cells. Vision Research 19, 425430.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medical Biology and Engineering 10, 510515.CrossRefGoogle ScholarPubMed
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G. & Enroth-Cugell, Ch. (1982). Receptive-field properties of X and Y cells in the cat retina derived from contrast-sensitivity measurements. Vision Research 22, 11731183.CrossRefGoogle ScholarPubMed
Loop, M.S., Millican, C.L. & Thomas, S.R. (1987). Photopic spectral sensitivity of the cat. Journal of Physiology 382, 537553.CrossRefGoogle ScholarPubMed
Maffei, L., Fiorentini, A. & Cervetto, L. (1971). Homeostasis in retinal receptive fields. Journal of Neurophysiology 34, 579587.CrossRefGoogle ScholarPubMed
Nelson, R. (1977). Cat cones have rod input: A comparison of the response properties of cones and horizontal cell bodies in the retina of the cat. Journal of Comparative Neurology 172, 109136.CrossRefGoogle ScholarPubMed
Pasternak, T. & Merigan, W.H. (1981). The luminance dependence of spatial vision in the cat. Vision Research 21, 13331339.CrossRefGoogle ScholarPubMed
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583601.CrossRefGoogle ScholarPubMed
Schnapf, J.L. & Baylor, D.A. (1987). How photoreceptor cells respond to light. Scientific American 256, 4047.CrossRefGoogle ScholarPubMed
Shapley, R.M. & Enroth-Cugell, Ch. (1984). Visual adaptation and retinal gain controls. Progress in Retinal Research 3, 263346.CrossRefGoogle Scholar
Shapley, R.M. & Victor, J.D. (1978). The effect of contrast on the transfer properties of cat retinal ganglion cells. Journal of Physiology 285, 275298.CrossRefGoogle ScholarPubMed
So, Y.T. & Shapley, R.M. (1981). The spatial tuning of cells in and around the lateral geniculate nucleus of the cat: X and Y relay cells and perigeniculate neurons. Journal of Neurophysiology 45, 107120.CrossRefGoogle 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, 621628.CrossRefGoogle ScholarPubMed
Steinberg, R.H., Reid, M. & Lacy, P.L. (1973). The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of Comparative Neurology 148, 229248.CrossRefGoogle ScholarPubMed
Thibos, L.N. & Levick, W.R. (1983). Bimodal receptive fields of cat retinal ganglion cells. Vision Research 23, 15611572.CrossRefGoogle ScholarPubMed
Troy, J.B. (1983). Spatio-temporal interaction in neurones of the cat’s dorsal lateral geniculate nucleus. Journal of Physiology 344, 419432.CrossRefGoogle ScholarPubMed
Troy, J.B. & Robson, J.G. (1992). Steady discharges of X and Y retinal ganglion cells of cat under photopic illuminance. Visual Neuroscience 9, 535553.CrossRefGoogle ScholarPubMed
Victor, J.D. & Shapley, R.M. (1979). The nonlinear pathway of Y ganglion cells in the cat retina. Journal of General Physiology 74, 671689.CrossRefGoogle ScholarPubMed
Virsu, V., Lee, B.B. & Creutzfeldt, O.D. (1977). Dark adaptation and receptive-field organisation of cells in the cat lateral geniculate nucleus. Experimental Brain Research 27, 3550.CrossRefGoogle ScholarPubMed
Wässle, H., Levick, W.R. & Cleland, B.G. (1975). The distribution of the alpha type of ganglion cells in the cat retina. Journal of Comparative Neurology 159, 419438.CrossRefGoogle Scholar
Wyszecki, G. & Stiles, W.S. (1982). Color Science. 2nd edition. New York: John Wiley & Sons. 950 pp.Google Scholar