Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-24T20:33:43.328Z Has data issue: false hasContentIssue false
  • English
  • Français

Response linearity and kinetics of the cat retina: The bipolar cell component of the dark-adapted electroretinogram

Published online by Cambridge University Press:  02 June 2009

J. G. Robson  and
L. J. Frishman
J. G. Robson
Affiliation:
Physiological Laboratory, Cambridge CB2 3EG, UK
L. J. Frishman
Affiliation:
College of OptometryUniversity of Houston,, Houston
Get access Rights & Permissions [Opens in a new window]

Abstract

The electroretinogram (ERG) of the dark-adapted cat eye in response to brief ganzfeld flashes of a wide range of intensities was recorded after intravitreal injection of n-methyl dl aspartate (NMdlA, cumulative intravitreal concentration of 1.3–3.9 mM) to suppress inner-retinal components, and after intravitreal dl or L-2-amino-4-phosphonobutyric acid (dl-APB, 1–3 mM; l-APB, 1.2 mM) and 6-cyano-7-nitroquinoxaline-2, 3 dione (CNQX, 40–60 µM), to suppress all post-receptoral neuronal responses. Rod PII, the ERG component arising from rod bipolar cells, was derived by subtracting records obtained after APB and CNQX from post-NMDLA records. When we measured the derived response at fixed times after the stimulus, we found that PII initially increased in proportion to stimulus intensity without any sign of a threshold. The leading edge of PII at early times after the stimulus, when the response was still small, was well described by V(t) = kI(t −td)5 where k is a constant, I is the intensity of the stimulus, and td is a brief delay of about 3 ms. Correspondingly, the time for the response to rise to an arbitrary small criterion voltage Vcrit was adequately fitted by tcrit = td + (Vcrit/kI)1/5. The time course of the leading edge of the PII response can be interpreted to indicate that the mechanism generating PII introduces three stages of temporal integration in addition to the three stages that are provided by the mechanism of the rod photoreceptors. This finding is consistent with the operation within the rod bipolar cell of a G-protein cascade similar to that in the rods.

Keywords

ElectroretinogramBipolar cellPIIG-proteinb-wave
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 5 , September 1995 , pp. 837 - 850
Copyright
Copyright © Cambridge University Press 1995

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

REFERENCES

Arden, G.B., Carter, R.M., Hogg, C.R., Powell, D.J., Ernst, W.J.K., Clover, G.M., Lynes, A.L. & Quinlan, M.P. (1983). A modified ERG technique and the results obtained in X-linked retinitis pigmentosa. British Journal of Ophthalmology 67, 419–430.CrossRefGoogle ScholarPubMed
Ashmore, J.F. & Falk, G. (1979). Transmission of visual signals to bipolar cells near absolute threshold. Vision Research 19, 419–423.CrossRefGoogle ScholarPubMed
Ashmore, J.F. & Falk, G. (1980). Responses of rod bipolar cells in the dark-adapted retina of the dogfish, Scyliorhinus canicula. Journal of Physiology 300 115–150.CrossRefGoogle ScholarPubMed
Ashmore, J.F. & Falk, G. (1982). An analysis of voltage noise in rod bipolar cells of the dogfish retina. Journal of Physiology 332, 273–297.CrossRefGoogle ScholarPubMed
Barlow, H.B. & Levick, W.R. (1969). Three factors limiting the reliable detection of light by retinal ganglion cells of the cat. Journal of Physiology 200, 1–24.CrossRefGoogle ScholarPubMed
Barlow, H.B., Levick, W.R. & Yoon, M. (1971). Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research (Suppl.) 3, 87–101.CrossRefGoogle Scholar
Baylor, D.A. & Fuortes, M.G.F. (1970). Electrical responses of single cones in the retina of the turtle. Journal of Physiology 207, 77–92.CrossRefGoogle ScholarPubMed
Baylor, D.A., Lamb, T.D. & Yau, K.W. (1979). The membrane current of single rod outer segments. Journal of Physiology 288, 589–611.CrossRefGoogle ScholarPubMed
Baylor, D.A., Hodgkin, A.K. & Lamb, T.D. (1974). The electrical response of turtle cones to flashes and steps of light. Journal of Physiology 242, 685–727.CrossRefGoogle ScholarPubMed
Boos, R., Schneider, H. & Wässle, H. (1993). Voltage- and transmitter-gated currents of Aii-amacrine cells in a slice preparation of the rat retina. Journal of Neuroscience 13, 2874–2888.CrossRefGoogle Scholar
Boycott, B.B. & Kolb, H. (1973). The connections between bipolar cells and photoreceptors in the retina of the domestic cat. Journal of Comparative Neurology 148, 91–114.CrossRefGoogle ScholarPubMed
Breton, M.A., Schueller, A.W., Lamb, T.D. & Pugh, E.N. (1994). Analysis of ERG a-wave amplification and kinetics in terms of the G-protein cascade of phototransduction. Investigative Ophthalmology and Visual Science 35, 295–309.Google ScholarPubMed
Brown, K.T. & Wiesel, T.N. (1961). Localization of origins of electroretinogram components by intraretinal recording in the intact cat eye. Journal of Physiology 158, 257–280.CrossRefGoogle ScholarPubMed
Bush, R. & Remé, C.E. (1992). Chronic lithium treatment induces reversible and irreversible changes in the rat ERG in vivo. Clinical Vision Sciences 5, 393–401.Google Scholar
Bush, R.A. & Sieving, P.A. (1994). Possible mechanisms for supranormal dark-adapted ERG b-waves in humam cone dystrophy: PDA/KYN enhance dark-adapted b-wave in monkey. Investigative Ophthalmology and Visual Science 35, 1957.Google Scholar
Cohen, E.D. & Miller, R.F. (1994). The role of NMDA and non-NMDA excitatory amino-acid receptors in the functional organization of primate retinal ganglion cells. Visual Neuroscience 11, 317–332.CrossRefGoogle ScholarPubMed
Cohen, E.D. & Fain, G.L. (1994). Pharmacology of ligand-gated currents of cat ganglion cell types in a retinal slice preparation. Society for Neuroscience Abstracts 19, 1418.Google Scholar
Cone, R.A. (1963). Quantum relations of the rat electroretinogram. Journal of General Physiology 46, 1267–1286.CrossRefGoogle ScholarPubMed
Dacheux, R.F. & Raviola, E. (1986). The rod pathway in the rabbit retina: A depolarizing bipolar and amacrine cell. Journal of Neuroscience 6, 331–345.CrossRefGoogle ScholarPubMed
Freed, M.A., Smith, R.G. & Sterling, P. (1987). Rod bipolar array in the cat retina: Pattern of input from rods and GABA-accumulating amacrine cells. Journal of Comparative Neurology 266, 445–455.CrossRefGoogle ScholarPubMed
Frishman, L.J. & Sieving, P.A. (1995). Evidence for two sites of adaptation affecting the dark-adapted ERG of cats and primates. Vision Research 35, 435–442.CrossRefGoogle ScholarPubMed
Frishman, L.J. & Steinberg, R.H. (1989a). Intraretinal analysis of the threshold dark-adapted ERG of cat retina. Journal of Neurophysiology 61, 1221–1232.CrossRefGoogle ScholarPubMed
Frishman, L.J. & Steinberg, R.H. (1989b). Light-evoked changes in [K+]0 in proximal portion of the dark-adapted cat retina. Journal of Neurophysiology 61, 1233–1243.CrossRefGoogle Scholar
Fulton, A.B. & Rushton, W.A.H. (1978a). Rod ERG of the mudpuppy: Effect of dim red backgrounds. Vision Research 18, 785–792.CrossRefGoogle ScholarPubMed
Fulton, A.B. & Rushton, W.A.H. (1978b). The human rod ERG: Correlation with psychophysical responses in light and dark adaptation. Vision Research 18, 793–800.CrossRefGoogle ScholarPubMed
Granit, R. (1933). The components of the retinal action potential in mammals and their relation to the discharge in the optic nerve. Journal of Physiology 77, 207–239.CrossRefGoogle Scholar
Gurevich, L. & Slaughter, M.M. (1993). Comparison of the waveforms of the ON bipolar neuron and the b-wave of the electroretinogram. Vision Research 33, 2431–2435.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1990a). The a-wave of the human ERG and rod receptor function. Investigative Ophthalmology and Visual Science 31, 2070–2081.Google ScholarPubMed
Hood, D.C. & Birch, D.G. (1990b). A quantitative measure of the electrical activity of human rod photoreceptors using electroretinography. Visual Neuroscience 5, 379–387.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1992). A computational model of the amplitude and implicit time of the b-wave of the human ERG. Visual Neuroscience 8, 107–126.CrossRefGoogle ScholarPubMed
Hubbard, N.P. & Naarendorp, F. (1994). Effects of dim background lights on the scotopic threshold response of the rat ERG. Investigative Ophthalmology and Visual Science 35, 2047.Google Scholar
Kaneko, A. (1994). Glutamate-induced responses in identified cat bipolar cells. Investigative Ophthalmology and Visual Science 35, 1382.Google Scholar
Katz, B.J., Wen, R., Zheng, J., Xu, Z. & Oakley, B. II (1991). M-wave of the toad electroretinogram. Journal of Neurophysiology 66, 1927–1940.CrossRefGoogle ScholarPubMed
Lamb, T.D. & Pugh, E.N. (1992). A quantitative account of the activation steps involved in phototransduction in amphibian photoreceptors. Journal of Physiology 449, 717–757.CrossRefGoogle ScholarPubMed
Massey, S.C. (1990). Cell types using glutamate as a neurotransmitter in the vertebrate retina. In Progress in Retinal Research, Vol. 9, ed. Osborne, N.N. & Chader, G.J., pp. 399–425. Oxford, UK: Pergamon Press.Google Scholar
Mastronarde, D.N. (1983). 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
Naarendorp, F. & Sieving, P.A. (1991). The scotopic threshold response of the cat ERG is suppressed selectively by GABA and glycine. Vision Research 31, 1–15.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1990). Suppression by glutamate of cGMP- activated conductance in retinal bipolar cells. Nature 346, 269–271.CrossRefGoogle ScholarPubMed
Nawy, S. & Jahr, C.E. (1991). cGMP-gated conductances in retinal bipolar cells is suppressed by photoreceptor transmitter. Neuron 7, 677–683.CrossRefGoogle ScholarPubMed
Newman, E.A. (1980). Current-source density analysis of the b-wave of frog retina. Journal of Neurophysiology 43, 1355–1366.CrossRefGoogle ScholarPubMed
Newman, E.A. & Odette, L.L. (1984). Model of electroretinogram b-wave generation: A test of the K+ hypothesis. Journal of Neurophysiology 51, 164–182.CrossRefGoogle ScholarPubMed
Peachey, N.A., Alexander, K.R. & Fishman, G.A. (1989). The luminance-response function of the dark-adapted human electroretinogram. Vision Research 29, 263–270.CrossRefGoogle ScholarPubMed
Robson, J.G., Frishman, L.J. & Du, L. (1993). Component potentials of the dark-adapted cat ERG. Society for Neuroscience Abstracts 19, 1413.Google Scholar
Schneider, T. & Zrenner, E. (1987). The variable interdependence of amplitude and implicit-time in PII, b-wave and optic-nerve responses of the cat. Experimental Eye Research 45, 655–664.CrossRefGoogle Scholar
Shapley, R.M. & Enroth-Cugell, Ch. (1984). Visual adaptation and retinal gain controls. In Progress in Retinal Research, Vol. 3, ed. Osborne, N.N. & Chader, G.J., pp. 263–346. Oxford: Pergamon Press.Google Scholar
Shiells, R.A. & Falk, G. (1990). Glutamate receptors of rod bipolar cells are linked to a cyclic GMP cascade via a G-protein. Proceedings of the Royal Society B (London) 242, 91–94.Google ScholarPubMed
Shiells, R.A. & Falk, G. (1992). The glutamate-receptor linked cGMP cascade of retinal on-bipolar cells is pertussis and cholera toxin-sensitive. Proceedings of the Royal Society B (London) 247, 17–21.Google ScholarPubMed
Sieving, P.A. (1991). Retinal ganglion cell loss does not abolish the STR of the cat and human ERG. Clinical Vision Sciences 6, 149–158.Google Scholar
Sieving, P.A., Frishman, L.J. & Steinberg, R.H. (1986). Scotopic threshold response of proximal retina in cat. Journal Neurophysiology 56, 1049–1061.CrossRefGoogle ScholarPubMed
Sieving, P.A., Murayama, K. & Naarendorp, F. (1994). Push-pull model of the primate electroretinogram: A role for hyperpolarizing neurons in shaping the b-wave. Visual Neuroscience 11, 519–532.CrossRefGoogle ScholarPubMed
Slaughter, M.M. & Miller, R.F. (1981). 2-amino-4-phosphonobutyric acid —a new pharmacological tool for retina research. Science 211, 182–185.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Steinberg, R.H. (1969). Comparison of the intraretinal b-wave and d.c. component in the area centralis of cat retina. Vision Research 9, 317–331.CrossRefGoogle Scholar
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, 229–248.CrossRefGoogle ScholarPubMed
Sterling, P. (1983). Microcircuitry of the cat retina. Annual Review of Neuroscience 6, 149–185.CrossRefGoogle ScholarPubMed
Stockton, R.A. & Slaughter, M.M. (1989). B-Wave of the electroretinogram: A reflection of ON bipolar cell activity. Journal of General Physiology 93, 101–122.CrossRefGoogle ScholarPubMed
Vaegan, & Millar, T.J. (1994). Effect of kainic acid and NMdA on the pattern electroretinogram, the scotopic threshold response, the oscillatory potentials and the electroretinogram in the urethane anaesthetized cat. Vision Research 34, 1111–1125.CrossRefGoogle ScholarPubMed
Wakabayashi, K., Gieser, J. & Sieving, P.A. (1988). Aspartate separation of the scotopic threshold response (STR). from the photoreceptor a-wave of the cat and monkey ERG. Investigative Ophthalmology and Visual Science 29, 1615–1622.Google Scholar
Xu, X.J. & Karwoski, C.J. (1994). Current-source density analysis of retinal field potentials. 2. Pharmacological analysis of the b-wave and m-wave. Journal of Neurophysiology 72, 96–105.CrossRefGoogle ScholarPubMed
Yamashita, M. & Wässle, H. (1991). Responses of rod bipolar cells isolated from the rat retina to the glutamate agonist 2-amino-4-phos-phonobutyric acid (APB). Journal of Neuroscience 11, 2372–2382.CrossRefGoogle Scholar
Zhou, Z.J., Marshak, D.W. & Fain, G.L. (1994). Amino-acid receptors of midget and parasol ganglion cells in primate retina Proceedings of the National Academy of Sciences of the U.S.A. 91, 4907–4911.CrossRefGoogle ScholarPubMed