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Spatiotemporal integration of light by the cat X-cell center under photopic and scotopic conditions

Published online by Cambridge University Press:  06 October 2005

J.B. TROY ,
D.L. BOHNSACK ,
J. CHEN ,
X. GUO  and
C.L. PASSAGLIA
J.B. TROY
Affiliation:
Department of Biomedical Engineering and the Neuroscience Institute, Northwestern University, Evanston
D.L. BOHNSACK
Affiliation:
Department of Biomedical Engineering and the Neuroscience Institute, Northwestern University, Evanston
J. CHEN
Affiliation:
Department of Biomedical Engineering and the Neuroscience Institute, Northwestern University, Evanston
X. GUO
Affiliation:
Department of Biomedical Engineering and the Neuroscience Institute, Northwestern University, Evanston
C.L. PASSAGLIA
Affiliation:
Department of Biomedical Engineering and the Neuroscience Institute, Northwestern University, Evanston Department of Biomedical Engineering, Boston University, Boston
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Abstract

Visual responses to stimulation at high temporal frequency are generally considered to result from signals that avoid light adaptive gain adjustment, simply reflecting linear summation of luminance. Under conditions of high photopic illuminance, the center of the receptive field of the cat X-cell has been shown to expand in size when stimulated at high temporal frequency, raising the possibility that there is spatiotemporal interaction in luminance summation. Here we show that this expansion maintains constant the product of the center's luminance summing area and the temporal period of luminance modulation, implying that spatial and temporal integration of luminance can be traded for one another by the X-cell center. As such the X-cell has a spatiotemporal window for luminance integration that fuses the classical concepts of a spatial window of luminance integration (Ricco's Law) with a temporal window of luminance integration (Bloch's Law). We were interested to determine whether this tradeoff between spatial and temporal summation of luminance occurs also at lower light levels, where the temporal-frequency bandwidth of the X-cell is narrower. We found that it does not. Center radius does not expand with temporal frequency under either low photopic or scotopic conditions. These results are discussed within the context of the known retinal circuitry that underlies the X-cell center for photopic and scotopic conditions.

Keywords

Contrast sensitivityRetinal ganglion cellRod and cone inputsVisual adaptationTemporal frequency
Type
Research Article
Information
Visual Neuroscience , Volume 22 , Issue 4 , July 2005 , pp. 493 - 500
Copyright
2005 Cambridge University Press

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References

REFERENCES

Attwell, D., Werblin, F.S., & Wilson, M. (1982). The properties of single cones isolated from the tiger salamander retina. Journal of Physiology 328, 259–283.Google Scholar
Attwell, D., Wilson, M., & Wu, S.M. (1984). A quantitative analysis of interactions between photoreceptors in the salamander (Ambystoma) retina. Journal of Physiology 352, 703–737.Google Scholar
Bader, C.R., Bertrand, D., & Schwartz, E.A. (1982). Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. Journal of Physiology 331, 253–284.Google Scholar
Bader, C.R., MacLeish, P.R., & Schwartz, E.A. (1979). A voltage-clamp study of the light response in solitary rods of the tiger salamander. Journal of Physiology 296, 1–26.Google Scholar
Barnes, S. & Hille, B. (1989). Ionic channels of the inner segment of tiger salamander cone photoreceptors. Journal of General Physiology 94, 719–743.Google Scholar
Brown, J.E. & Pinto, L.H. (1974). Ionic mechanism for the photoreceptor potential of the retina of Bufo Marinus. Journal of Physiology 236, 575–591.Google Scholar
Chan, L.-H., Freeman, A.W., & Cleland, B.G. (1992). The rod-cone shift and its effect on ganglion cells in the cat retina. Vision Research 32, 2209–2219.Google Scholar
Cleland, B.G. & Freeman, A.W. (1988). Visual adaptation is highly localized in the cat's retina. Journal of Physiology 404, 591–611.Google Scholar
Cleland, B.G., Harding, T.H., & Tulunay-Keesey, U. (1979). Visual resolution and receptive-field size: Examination of two kinds of cat retinal ganglion cell. Science 205, 1015–1017.Google Scholar
Cleland, B.G. & Levick, W.R. (1974a). 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. (1974b). 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
Corey, D.P., Dubinsky, J.M., & Schwartz, E.A. (1984). The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. Journal of Physiology 354, 557–575.Google Scholar
Dawis, S., Shapley, R., Kaplan, E., & Tranchina, D. (1984). The receptive field organization of X-cells in the cat: Spatiotemporal coupling and asymmetry. Vision Research 24, 549–564.Google Scholar
De Monasterio, F.M. & Gouras, P. (1975). Functional properties of ganglion cells of the rhesus monkey retina. Journal of Physiology 251, 167–195.Google Scholar
Demontis, G.C., Longoni, B., Barcaro, U., & Cervetto, L. (1999). Properties and functional roles of hyperpolarization-gated currents in guinea-pig retinal rods. Journal of Physiology 515.3, 813–828.Google Scholar
Dennis, J.E.Jr. & Schnabel, R.B. (1983). Numerical Methods for Unconstrained Optimization and Nonlinear Equations. Englewood Cliffs, New Jersey: Prentice Hall.
Detwiler, P.B., Hodgkin, A.L., & McNaughton, P.A. (1978). A surprising property of electrical spread in the network of rods in the turtle's retina. Nature 274, 562–565.Google Scholar
Detwiler, P.B., Hodgkin, A.L., & McNaughton, P.A. (1980). Temporal and spatial characteristics of the voltage response of rods in the retina of the snapping turtle. Journal of Physiology 300, 213–250.Google Scholar
Enroth-Cugell, C. & Robson, J.G (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517–552.Google Scholar
Enroth-Cugell, C. & Shapley, R.M. (1973). Flux, not retinal illumination, is what cat retinal ganglion cells really care about. Journal of Physiology 233, 311–326.Google Scholar
Enroth-Cugell, C., 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, 279–307.Google Scholar
Frishman, L.J., Freeman, A.W., Troy, J.B., Schweitzer-Tong, D., & Enroth-Cugell, C. (1987). Spatiotemporal frequency responses of cat retinal ganglion cells. Journal of General Physiology 89, 599–628.Google Scholar
Fuortes, M.G.F. & Hodgkin, A.L. (1964). Changes in time scale and sensitivity in the ommatidia of Limulus. Journal of Physiology 156, 179–192.Google Scholar
Graham, N. & Hood, D.C. (1992). Modeling the dynamics of light adaptation: The merging of two traditions. Vision Research 32, 1373–1393.Google Scholar
Hammond, P. & Mouat, G.S.V. (1985). The relationship between feline pupil size and luminance. Experimental Brain Research 59, 485–490.Google Scholar
Hestrin, S. (1987). The properties and function of inward rectification in rod photoreceptors of the tiger salamander. Journal of Physiology 390, 319–333.Google Scholar
Hochstein, S. & Shapley, R.M. (1976). Quantitative analysis of retinal ganglion cell classifications. Journal of Physiology 262, 237–264.Google Scholar
Kelly, D.H. (1972). Adaptation effects on spatio-temporal sine-wave thresholds. Vision Research 12, 89–101.Google Scholar
Koch, C. (1984). Cable theory in neurons with active, linearized membranes. Biological Cybernetics 50, 15–33.Google Scholar
Kolb, H. (1977). The organization of the outer plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 6, 131–153.Google Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 37–68.Google Scholar
Lennie, P., Hertz, B.G., & Enroth-Cugell, C. (1976). Saturation of rod pools in cat. Vision Research 16, 935–940.Google Scholar
Linsenmeier, R.A., Frishman, L.J., Jakiela, H.G., & Enroth-Cugell, C. (1982). Receptive field properties of X and Y cells in the cat retina derived from contrast sensitivity measurements. Vision Research 22, 1173–1183.Google Scholar
Maricq, A.V. & Korenbrot, J.I. (1988). Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1, 503–515.Google Scholar
Maricq, A.V. & Korenbrot, J.I. (1990). Inward rectification in the inner segment of single retinal cone photoreceptors. Journal of Neurophysiology 64, 1917–1928.Google Scholar
Oh, J.K., Bohnsack, D.L., Troy, J.B., & Enroth-Cugell, Ch. (1995). The cat's pupillary light response under urethane anesthesia. Visual Neuroscience 12, 281–284.Google Scholar
Passaglia, C.L. & Troy, J.B. (2004a). Information transmission rates of cat retinal ganglion cells. Journal of Neurophysiology 91, 1217–1229.Google Scholar
Passaglia, C.L. & Troy, J.B. (2004b). The impact of noise on retinal coding of visual signals. Journal of Neurophysiology 92, 1023–1033.Google Scholar
Peichl, L. & Wässle, H. (1979). Size, scatter, and coverage of ganglion cell receptive field centers in the cat retina. Journal of Physiology 291, 117–141.Google Scholar
Pinter, R.B. (1966). Sinusoidal and delta function responses of visual cells of the Limulus eye. Journal of General Physiology 49, 565–593.Google Scholar
Rodieck, R.W. (1965). Quantitative analysis of cat retinal ganglion cell response to visual stimuli. Vision Research 5, 583–601.Google Scholar
Roufs, J.A.J. (1972a). Dynamic properties of vision—I. Experimental relationships between flicker and flash thresholds. Vision Research 12, 261–278.Google Scholar
Roufs, J.A.J. (1972b). Dynamic properties of vision—II. Theoretical relationships between flicker and flash thresholds. Vision Research 12, 279–292.Google Scholar
Saito, H. & Fukada, Y. (1986). Gain control mechanisms in X- and Y-type retinal ganglion cells of the cat. Vision Research 26, 391–408.Google Scholar
Schneeweis, D.M. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056.Google Scholar
Shapley, R. & Enroth-Cugell, C. (1984). Visual adaptation and retinal gain controls. Progress in Retinal Research 3, 263–343.Google Scholar
Smith, R.G., Freed, M.A., & Sterling, P. (1986). Microcircuitry of the dark-adapted cat retina: Functional architecture of the rod–cone network. Journal of Neuroscience 6, 3505–3517.Google Scholar
Stone, J. & Fukada, 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
Tranchina, D., Gordon, J., & Shapley, R.M. (1984). Retinal light adaptation—evidence for a feedback mechanism. Nature 310, 314–316.Google Scholar
Troy, J.B. & Enroth-Cugell, C. (1989). The dependence of center radius on temporal frequency for the receptive fields of X retinal ganglion cells of cat. Journal of General Physiology 94, 987–995.Google Scholar
Troy, J.B. & Robson, J.G. (1992). Steady discharges of X and Y retinal ganglion cells of cat under photopic illuminance. Visual Neuroscience 9, 535–553.Google Scholar
Troy, J.B. & Enroth-Cugell, C. (1993). X and Y ganglion cells inform the cat's brain about contrast in the retinal image. Experimental Brain Research 93, 383–390.Google Scholar
Troy, J.B. & Shou, T. (2002). The receptive fields of cat retinal ganglion cells in physiological and pathological states: Where we are after half a century of research. Progress in Retinal and Eye Research 21, 263–302.Google Scholar
Troy, J.B., Bohnsack, D.L., & Diller, L.C. (1999). Spatial properties of the cat X-cell receptive field as a function of mean light level. Visual Neuroscience 16, 1089–1104.Google Scholar
Victor, J.D. (1987). The dynamics of the cat retinal X cell centre. Journal of Physiology 386, 219–246.Google Scholar
Yagi, T. & MacLeish, P.R. (1994). Ionic conductances of monkey solitary cone inner segments. Journal of Neurophysiology 71, 656–665.Google Scholar