Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T16:51:32.379Z Has data issue: false hasContentIssue false

Two signals in the human rod visual system: A model based on electrophysiological data

Published online by Cambridge University Press:  02 June 2009

Andrew Stockman
Affiliation:
Department of Psychology, University of California San Diego, La Jolla
Lindsay T. Sharpe
Affiliation:
Forschungsstelle für Experimentelle Ophthalmologie, University of Tübingen, D-72076 Tübingen, Germany
Klaus Rüther
Affiliation:
Pathophysiologie des Sehens und Neuro-Ophthalmologie, Universitäts-Augenklinik, University of Tübingen, D-72076 Tübingen, Germany
Knut Nordby
Affiliation:
Norwegian Telecommunications Administration, Research Department, N-2007 Kjeller, Norway

Abstract

In the human rod visual system, self-cancellation of flicker signals is observed at high rod intensity levels near 15 Hz, both perceptually and in the electroretinogram (ERG). This and other evidence suggests that two rod signals are transmitted through the human retina with different speeds of transmission. Here we report a series of flicker ERG recordings from a normal observer and an observer who lacks cone vision. From these results, we propose a quantitative model of the two rod signals, which assumes (1) that the amplitude of the slow signal grows linearly with log intensity but then saturates at ~1 scot, td; (2) that the amplitude of the fast signal grows linearly with intensity; (3) that there is a difference in time delay of ~33 ms between two rod signals of the same polarity (or of ~67 ms if the signals are of inverted polarity); and (4) that the time delay of both signals declines linearly with log intensity (by ~10 ms per log scot. td). These simple assumptions provide a remarkably good account of the experimental data. Our results and model are relevant to current anatomical theories of the mammalian rod visual system. We speculate that the slower signal in the human ERG may reflect the transmission of the rod response via the rod bipolars and the An amacrine cells, while the faster signal may reflect its transmission via the rod-cone gap junctions and the cone bipolars. There are, however, several objections to this simple correspondence.

Type
Research Articles
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

Alexander, K.R. & Fishman, G.A. (1984). Rod-cone interaction in flicker perimetry. British Journal of Ophthalmology 68, 303309.CrossRefGoogle ScholarPubMed
Alexander, K.R. & Fishman, G.A. (1985). Rod-cone interaction in flicker perimetry: Evidence for a distal retinal locus. Documenta Ophthalmologica 60, 336.CrossRefGoogle ScholarPubMed
Alpern, M., Falls, H.F. & Lee, G.B. (1960). The enigma of typical total monochromacy. American Journal of Ophthalmology 50, 9961012.Google Scholar
Arden, G.B. & Brown, K.T. (1965). Some properties of components of the cat electroretinogram revealed by local recordings under oil. Journal of Physiology (London) 176, 429461.Google Scholar
Arden, G.B., Carter, R.M., Hogg, C.R., Powell, D.J., Ernst, W.J.K., Clover, G.M., Lyness, A.L. & Quinlan, M.P. (1983). A modified ERG technique and the results obtained in X-linked retinitis pigmentosa. British Journal of Ophthalmology 67, 419430.CrossRefGoogle ScholarPubMed
Arden, G.B. & Hogg, C.R. (1985). Rod-cone interaction and analysis of retinal disease. British Journal of Ophthalmology 69, 404415.CrossRefGoogle ScholarPubMed
Arden, G.B. & Weale, R.A. (1954). Variations of the latent period of vision. Proceedings of the Royal Society (London) B142, 258269.Google Scholar
Baylor, D.A., Nunn, B.J. & Schnapf, J.L. (1984). The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. Journal of Physiology (London) 357, 575607.CrossRefGoogle ScholarPubMed
Blakemore, C.B. & Rushton, W.A.H. (1965). Dark adaptation and increment threshold in a rod monochromat. Journal of Physiology (London) 181, 612628.CrossRefGoogle Scholar
Brown, K.T. & Wiesel, T.N. (1961a). Analysis of the intraretinal electroretinogram in the intact cat eye. Journal of Physiology (London) 158, 229256.CrossRefGoogle ScholarPubMed
Brown, K.T. & Wiesel, T.N. (1961b). Localization of origins of electroretinogram components by intraretinal recording in the intact cat eye. Journal of Physiology (London) 158, 257280.Google Scholar
Chun, M.-H., Han, S.-H., Chung, J.-W. & Wässle, H. (1993). Electron microscopic analysis of the rod pathway of the rat retina. Journal of Comparative Neurology 332, 421432.CrossRefGoogle ScholarPubMed
Coletta, N.J. & Adams, A.J. (1984). Rod-cone interaction in flicker detection. Vision Research 24, 13331340.Google Scholar
Conner, J.D. (1982). The temporal properties of rod vision. Journal of Physiology (London) 332, 139155.CrossRefGoogle ScholarPubMed
Conner, J.D. & MacLeod, D.I.A. (1977). Rod photoreceptors detect rapid flicker. Science 195, 689699.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, 331345.CrossRefGoogle ScholarPubMed
Daw, N.W., Jensen, R.J. & Brunken, W.J. (1990). Rod pathways in mammalian retinae. Trends in Neurosciences 13, 110115.CrossRefGoogle ScholarPubMed
De Lange, H. (1958). Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light. I. Attenuation characteristics with white and colored light. Journal of the Optical Society of America 48, 777784.CrossRefGoogle Scholar
Detwiler, P.B., Hodgkin, A.L. & McNaughton, P.A. (1978). A surprising property of electrical spread in the network of rods in the turtle retina. Nature 274, 562565.CrossRefGoogle Scholar
Dodt, E. & Walther, J.B. (1958). Der photopische Dominator im Flimmer-ERG der Katze. Pflügers Archiv für die gesamte Physiologie des Menschen und Tiere 266, 175186.Google Scholar
Falls, H.F., Wolter, J.R. & Alpern, M. (1965). Typical total monochromacy. Archives of Ophthalmology 74, 610616.Google Scholar
Famiglietti, E.V. & Kolb, H. (1975). A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84, 293300.CrossRefGoogle Scholar
Finkelstein, D., Gouras, P. & Hoff, M. (1968). Human electroretinogram near the absolute threshold of vision. Investigative Ophthalmology and Visual Science 7, 214218.Google ScholarPubMed
Frumkes, T.E., Naarendorp, F. & Goldberg, S.H. (1986). The influence of cone adaptation upon rod mediated flicker. Vision Research 26, 11671176.Google Scholar
Fulton, A.B. & Rushton, W.A.H. (1978). The human rod ERG: correlation with psychophysical response in light and dark adaptation. Vision Research 18, 793800.Google Scholar
Glickstein, M. & Heath, G.G. (1975). Receptors in the monochromat eye. Vision Research 15, 633636.Google Scholar
Goldberg, S.H., Frumkes, T.E. & Nygaard, R.W. (1983). Inhibitory influence of unstimulated rods in the human retina: Evidence provided by examining cone flicker. Science 221, 180182.Google Scholar
Granit, R. (1947). Sensory Mechanisms of the Retina. London: Oxford University Press.Google Scholar
Harrison, D., Hoefnagel, D. & Hayward, J.N. (1960). Congenital total colour blindness, a clinicopathological report. Archives of Ophthalmology 64, 685692.CrossRefGoogle Scholar
Hecht, S., Shlaer, S., Smith, E.L., Haig, C. & Peskin, J.C. (1938). The visual functions of a completely color blind person. American Journal of Physiology 123, 9495.Google Scholar
Hecht, S., Shlaer, S., Smith, E.L., Haig, C. & Peskin, J.C. (1948). The visual functions of the complete color-blind. Journal of General Physiology 31, 459472.Google Scholar
Hess, R.F. & Nordby, K. (1986). Spatial and temporal limits of vision in the achromat. Journal of Physiology (London) 371, 365385.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, 107126.CrossRefGoogle ScholarPubMed
Hood, D.C. & Birch, D.G. (1993). Light adaptation of the human rod receptors: the leading edge of the human a-wave and models of rod receptor activity. Vision Research 33, 16051618.CrossRefGoogle Scholar
Jacobs, G.H. (1990). Duplicity theory and ground squirrels: linkages between photoreceptors and visual function. Visual Neuroscience 5, 311318.CrossRefGoogle ScholarPubMed
Knave, B., Moller, A. & Persson, H.E. (1972). A component analysis of the electroretinogram. Vision Research 12, 16691684.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, 131153.CrossRefGoogle ScholarPubMed
Kolb, H. (1979). The inner plexiform layer in the retina of the cat: Electron microscopic observations. Journal of Neurocytology 8, 295329.CrossRefGoogle ScholarPubMed
Kolb, H. & Famiglietti, E.V. (1974). Rod and cone pathways in the inner plexiform layer of the cat retina. Science 186, 4749.Google Scholar
Kolb, H. & Nelson, R. (1983). Rod pathways in the retina of the cat. Vision Research 23, 301302.CrossRefGoogle ScholarPubMed
Kolb, H. & Nelson, R. (1984). Neural architecture of the cat retina. In Progress in retinal research, ed. Osborne, N. & Chader, G., pp. 2160. New York: Pergamon Press.Google Scholar
Kraft, T.W., Schneeweis, D.M. & Schnapf, J.L. (1993). Visual transduction in human rod photoreceptors. Journal of Physiology (London) 464, 747765.Google Scholar
Larsen, H. (1921). Präparate von einem monochromatischen Auge. Klinische Monatsblätter für Augenheilkunde 67, 301302.Google Scholar
MacLeod, D.I.A. (1972). Rods cancel cones in flicker. Nature 235, 173174.CrossRefGoogle ScholarPubMed
Marmor, M.F., Arden, G.B., Nilsson, S.E.G. & Zrenner, E. (1989). Standard for clinical electroretinography. Archives of Ophthalmology 107, 816819.Google Scholar
Miller, R.F. & Dowling, J.E. (1970). Intracellular responses of the Müller (glial) cells of mudpuppy retina: Their relation to the b-wave of the electroretinogram. Journal of Neurophysiology 33, 323341.CrossRefGoogle Scholar
Müller, F., Wässle, H. & Voight, T. (1988). Pharmacological modulation of the rod pathway in cat retina. Journal of Neurophysiology 59, 16571672.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
Nelson, R. (1982). Aii amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47, 928947.CrossRefGoogle ScholarPubMed
Nelson, R. & Kolb, H. (1983). Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23, 11831195.Google Scholar
Nelson, R., Kolb, H. & Freed, M.A. (1993). OFF-alpha and OFF-beta ganglion cells in the cat retina. 1: Intracellular electrophysiology and HRP stains. Journal of Comparative Neurology 329, 6884.CrossRefGoogle ScholarPubMed
Nordby, K.N. & Sharpe, L.T. (1988). The directional sensitivity of the photoreceptors in the human achromat. Journal of Physiology (London) 399, 267281.CrossRefGoogle ScholarPubMed
Peachey, N.S., Alexander, K.R., Derlacki, D.J. & Fishman, G.A. (1992). Light adaptation, rods, and the human cone flicker ERG. Visual Neuroscience 8, 145150.CrossRefGoogle ScholarPubMed
Peachey, N.S., Alexander, K.R. & Fishman, G.A. (1989). The luminance-response function of the dark-adapted human electroretinogram. Vision Research 29, 263270.Google Scholar
Raviola, E. & Gilula, N.B. (1973). Gap junctions between photoreceptor cells in the vertebrate retina. Proceedings of the National Academy of Sciences of the U.S.A. 70, 16771681.CrossRefGoogle ScholarPubMed
Raviola, E. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. Journal of Cell Biology 65, 192222.CrossRefGoogle ScholarPubMed
Schneeweis, D.M. & Schnapf, J.L. (1995). Photovoltage of rods and cones in the macaque retina. Science 268, 10531056.Google Scholar
Schweitzer, N.M.J. & Padmos, P. (1966). The microstructure of the human scotopic ERG. In The clinical value of electroretinography, ISCERG Symposium, ed. Ghent, , Institute for Perception pp. 198204. Basel: Karger.Google Scholar
Schweitzer, N.M.J. & Troelsta, A. (1965). A negative component in the b-wave of the human ERG. Ophthalmologica 149, 230235.CrossRefGoogle ScholarPubMed
Sharpe, L.T., Collewijn, H. & Nordby, K. (1986). Fixation, pursuit and nystagmus in a complete achromat. Clinical Vision Sciences 1, 3949.Google Scholar
Sharpe, L.T., Fach, C.C. & Stockman, A. (1993). The spectral properties of the two rod pathways. Vision Research 33, 27052720.Google Scholar
Sharpe, L.T., Hofmeister, J., Fach, C.C. & Stockman, A. (1994). Spatial relations of flicker signals in the two rod pathways. Journal of Physiology (London) 474, 421431.Google Scholar
Sharpe, L.T. & Nordby, K. (1990). The photoreceptors in the achromat. In Night Vision: basic, clinical and applied aspects, ed. Hess, R., Sharpe, L.T. & Nordby, K., pp. 335389. Cambridge: Cambridge University Press.Google Scholar
Sharpe, L.T. & Stockman, A. (submitted). Two rod pathways: The importance of seeing nothing.Google Scholar
Sharpe, L.T., Stockman, A., Fach, C.C. & Markstahler, U. (1993). Temporal and spatial summation in the human rod visual system. Journal of Physiology (London) 463, 325348.CrossRefGoogle ScholarPubMed
Sharpe, L.T., Stockman, A. & MacLeod, D.I.A. (1989). Rod flicker perception: Scotopic duality, phase lags and destructive interference. Vision Research 29, 15391559.Google Scholar
Sieving, P.A., Frishman, L.J. & Steinberg, R.H. (1986). Scotopic threshold response of proximal retina of cat. Journal of Neurophysiology 56, 10491061.Google Scholar
Sieving, P.A. & Nino, C. (1988). Scotopic threshold response (STR) of the human electroretinogram. Investigative Ophthalmology and Visual Science 29, 16081614.Google 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, 35053517.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, 317331.CrossRefGoogle Scholar
Sterling, P., Freed, M. & Smith, R.G. (1986). Microcircuitry and functional architecture of the cat retina. Trends in Neurosciences 9, 186192.Google Scholar
Sterling, P., Freed, M. & Smith, R.G. (1988). Architecture of rod and cone circuits to the on-beta ganglion cells. Journal of Neuroscience 8, 623642.Google Scholar
Stockman, A., Sharpe, L.T., Zrenner, E. & Nordby, K. (1991). Slow and fast pathways in the human rod visual system: ERG and psychophysics. Journal of the Optical Society of America A 8, 16571665.Google Scholar
Tamura, T., Nakatani, K. & Yau, K.-W. (1991). Calcium feedback and sensitivity in primate rods. Journal of General Physiology 98, 95130.Google Scholar
Tomita, T. (1950). Studies on intraretinal action potential Part I. Relation between the localization of micro-pipette in the retina and the shape of the intraretinal action potential. Journal of Neurophysiology 1, 110117.Google Scholar
Veringa, F. & Roelofs, J. (1966). Electro-optical stimulation in the human retina. Nature 211, 321322.Google Scholar
Wässle, H. & Boycott, B.B. (1991). Functional architecture of the mammalian retina. Physiological Reviews 71, 447480.Google Scholar
Williams, T.P. & Gale, J.G. (1977). A critique of an incremental threshold function. Vision Research 17, 881882.CrossRefGoogle ScholarPubMed
Wyszecki, G. & Stiles, W.S. (1982). Color Science (2nd ed.). New York:–Wiley.Google Scholar