Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-23T19:35:23.679Z Has data issue: false hasContentIssue false
  • English
  • Français

Steady discharges of X and Y retinal ganglion cells of cat under photopic illuminance

Published online by Cambridge University Press:  02 June 2009

J.B. Troy  and
J.G. Robson
J.B. Troy
Affiliation:
Departments of Biomedical Engineering and Neurobiology, and Physiology, Northwestern University, Evanston
J.G. Robson
Affiliation:
The Physiological Laboratory, University of Cambridge, Cambridge, CB2 3EC, U.K.
Get access Rights & Permissions [Opens in a new window]

Abstract

The discharges of ON- and OFF-center X and Y retinal ganglion cells in the presence of stationary patterns or of a uniform field of photopic luminance were recorded from urethane-anesthetized adult cats. The interval statistics and power spectra of these discharges were determined from these discharge records. The patterned stimuli were selected and positioned with respect to a cell's receptive field so as to generate steady discharges that were different in mean discharge rate from that cell's discharge for the diffuse field. The interval statistics of discharges recorded for diffuse or patterned illumination for all cell types can be modeled, approximately, as coming from renewal processes with gamma-distributed intervals. The gamma order of the interval distributions was found to be nearly proportional to the mean discharge rate for X cells, but not for Y cells. Typical values for the gamma orders and their dependence on mean rate for different cell types are given. The same model of a renewal process with gamma-distributed intervals is used to model the measured power spectra and performs well. When the gamma order is proportional to mean rate, the power spectral density at low temporal frequencies is independent of discharge rate. Gamma order was proportional to mean rate for X cells but not for Y cells. Nonetheless, the power spectral densities of both cell types at low frequencies were approximately independent of discharge rate. Hence, noise in this band of frequencies can be considered additive. The consequences of departures from the renewal process and of the gamma order not being proportional to mean rate are considered. The significance of different rates of discharge for signaling is discussed.

Keywords

CatMaintained dischargeNoisePower spectrumRetinal ganglion cell
Type
Research Article
Information
Visual Neuroscience , Volume 9 , Issue 6 , December 1992 , pp. 535 - 553
Copyright
Copyright © Cambridge University Press 1992

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barlow, H.B. & Levick, W.R. (1969). Changes in the maintained discharge with adaptation level in the cat retina. Journal of Physiology 202, 669–718.CrossRefGoogle ScholarPubMed
Bendat, J.S. & Piersol, A.C. (1986). Random Data: Analysis and Measurement Procedures. 2nd edition, pp. 94–99 and pp. 342–345. New York: John Wiley and Sons.Google Scholar
Bisti, S., Carmignoto, C., Galli, L. & Maffei, L. (1985). Spatial-frequency characteristics of neurones of area 18 in the cat: Dependence on the velocity of the visual stimulus. Journal of Physiology 359, 259–268.CrossRefGoogle ScholarPubMed
Bricham, E.O. (1974). The Fast Fourier Transform. Englewood Cliffs, New Jersey: Prentice-Hall.Google Scholar
Cleland, B.G. & Levick, W.R. (1974). Brisk and sluggish concentrically organized ganglion cells in the cat's retina. Journal of Physiology 240, 421–456.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, 649–680.CrossRefGoogle ScholarPubMed
Cox, D.R. & Lewis, P.A.W. (1966). The Statistical Analysis of Series of Events. London, U.K.: Chapman and Hall.CrossRefGoogle Scholar
De Kwaadsteniet, J.W. (1982). Statistical analysis and stochastic modeling of neuronal spike-train activity. Mathematical Biosciences 60, 17–71.CrossRefGoogle Scholar
Derrinoton, 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, 343–366.CrossRefGoogle Scholar
Eadih, W.T., Druard, D., James, F.E., Roos, M. & Sadoulet, B. (1971). Statistical Methods in Experimental Physics. New York: American Elsevier.Google Scholar
Enroth-Cugell, CH. & Robson, J.G. (1966). The contrast sensitivity of retinal ganglion cells of the cat. Journal of Physiology 187, 517–552.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, 279–307.CrossRefGoogle ScholarPubMed
Field, K.J. & Lang, C.M. (1988). Hazards of urethane (ethyl carbamate): A review of the literature. Laboratory Animals 22, 255–262.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, 559–628.Google ScholarPubMed
Frishman, L.J. & Levine, M.W. (1983). Statistics of the maintained discharge of cat retinal ganglion cells. Journal of Physiology 339, 475–494.CrossRefGoogle ScholarPubMed
Fuster, J.M., Herz, A. & Creutzfeldt, O.D. (1965). Interval analysis of cell discharge in spontaneous and optically modulated activity in the visual system. Arch. Hal. Biol. 103, 159–177.Google ScholarPubMed
Gestri, G., Maffei, L. & Petracchi, D. (1966). Spatial and temporal organization in retinal units. Kybernetik 3, 196–202.CrossRefGoogle ScholarPubMed
Goldberg, J.M., Adrian, H.O. & Smith, F.D. (1964). Response of neurons of the superior olivary complex of the cat to acoustic stimuli of long duration. Journal of Neurophysiology 27, 706–749.CrossRefGoogle ScholarPubMed
Hochstein, S. & Shapley, R.M. (1976). Quantitative analysis of retinal ganglion cell classifications. Journal of Physiology 262, 237–264.CrossRefGoogle ScholarPubMed
Koles, Z.J. (1970). A Study of the Sensory Dynamics of a Muscle Spindle, p. 47. Ph.D. Thesis, University of Alberta, Edmonton, Alberta, Canada.Google Scholar
Kuffler, S.W., Fitzhugh, R. & Barlow, H.B. (1957). Maintained activity in the cat's retina in light and darkness. Journal of General Physiology 40, 683–702.CrossRefGoogle ScholarPubMed
Lederer, W.J., Soindler, A.J. & Eisner, D.A. (1979). Thick slurry bevelling: A new technique for bevelling extremely fine microelectrodes and micropipettes. Pflügers Archives European Journal of Physiology 381, 287–288.CrossRefGoogle ScholarPubMed
Levick, W.R. (1972). Another tungsten microelectrode. Medical and Biological Engineering 10, 510–515.CrossRefGoogle ScholarPubMed
Levine, M.W. (1991). The distribution of the intervals between neural impulses in the maintained discharges of retinal ganglion cells. Biological Cybernetics 65, 459–467.CrossRefGoogle ScholarPubMed
Levine, M.W. & Shefner, J.M. (1977). A model for the variability of interspike intervals during sustained firing of a retinal neuron. Biophysical Journal 19, 241–252.CrossRefGoogle Scholar
Marmarelis, P.Z. & Marmarelis, V.Z. (1978). Analysis of Physiological Systems. The White-Noise Approach. New York: Plenum Press.CrossRefGoogle Scholar
Mastronarde, D.N. (1983a). Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X and Y cells. Journal of Neurophysiology 49, 303–324.CrossRefGoogle Scholar
Mastronarde, D.N. (1983b). Correlated firing of cat retinal ganglion cells. II. Responses of X and Y cells to single quantal events. Journal of Neurophysiology 49, 325–349.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1983c). Interactions between ganglion cells in cat retina. Journal of Neurophysiology 49, 350–365.CrossRefGoogle ScholarPubMed
Movshon, J.A., Thompson, I.D. & Tolhurst, D.J. (1978). Spatial and temporal contrast sensitivity of neurones in areas 17 and 18 of the cat's visual cortex. Journal of Physiology 283, 101–120.CrossRefGoogle ScholarPubMed
Nelsen, D.E. (1964). Calculation of power spectra for a class of randomly jittered waveforms. In Quarterly Progress Report No. 76 (MIT Research Laboratory of Electronics, Cambridge, Massachusetts), pp. 168–179.Google Scholar
Perkel, D.H., Gerstein, G.L. & Moore, G.P. (1967). Neuronal spike trains and stochastic point processes. I. The single spike train. Biophysical Journal 7, 391–418.CrossRefGoogle ScholarPubMed
Pettigrew, J.D., Cooper, M.L. & Blasdel, G.C. (1979). Improved use of tapetal reflection for eye-position monitoring. Investigative Ophthalmology and Visual Science 18, 490–495.Google ScholarPubMed
Purpura, K., Kaplan, E. & Shapley, R.M. (1989). Fluctuations in spontaneous discharge and visual responses in M and P pathways of macaque monkey. Investigative Ophthalmology and Visual Science (ARVO Abstracts) 30(3), 297.Google Scholar
Robson, J.G. & Troy, J.B. (1987). Nature of the maintained discharge of Q, X, and Y retinal ganglion cells of the cat. Journal of the Optical Society of America A 4, 2301–2307.CrossRefGoogle Scholar
Rodieck, R.W. (1967). Maintained activity of cat retinal ganglion cells. Journal of Neurophysiology 30, 1043–1071.CrossRefGoogle ScholarPubMed
Rodieck, R.W. & Smith, P.S. (1966). Slow dark discharge rhythms of cat retinal ganglion cells. Journal of Neurophysiology 29, 942–953.CrossRefGoogle ScholarPubMed
Sato, Y., Yamamoto, M. & Nakahama, H. (1976). Variability of interspike intervals of cat's on-center optic tract fibres activated by steady light spot: A comparative study on Xand Y-fibres. Experimental Brain Research 24, 285–293.CrossRefGoogle Scholar
Schmidt, R. & Creutzfeldt, O.D. (1968). Veränderungen von spontanaktivitaät und reizantwort retinaler und geniculärer neurone der katze bei fraktionierter injektion von pentobarbitol-Na (Nembutal). Pflügers Archives European Journal of Physiology 300, 129–147.CrossRefGoogle ScholarPubMed
Smith, C.E. (1979). A comment on a retinal neuron model. Biophysical Journal 25, 385–386.CrossRefGoogle ScholarPubMed
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells: A comparison of W-cells with Xand Y-cells. Journal of Neurophysiology 37, 722–748.CrossRefGoogle Scholar
Thorson, J. (1966). Small-signal analysis of a visual reflex in the locust. II. Frequency dependence. Kybernetik 3, 53–66.CrossRefGoogle ScholarPubMed
Troy, J.B. & Enroth-Cugell, CH. (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.CrossRefGoogle ScholarPubMed
Troy, J.B., Enroth-Cugell, CH. & Robson, J.G. (1987). Do X and Y retinal ganglion cells signal contrast? Proceedings of the 1987 IEEE International Conference on Systems, Man, and Cybernetics, pp. 1070–1074. New York: IEEE.Google Scholar
Troy, J.B., Robson, J.G. & Enroth-Cugell, CH. (1986). Retinal ganglion cell processing of spatial information in cats. Proceedings of the 1986 IEEE International Conference on Systems, Man, and Cybernetics, pp. 498–503.Google Scholar
Yang, G.L. & Chen, T.C. (1978). On statistical methods in neuronal spike-train analysis. Mathematical Biosciences 38, 1–34.CrossRefGoogle Scholar