Abstract
Psychophysical and electroretinographic observations in normal and achromat observers suggest that human rod signals travel through two retinal pathways (Conner, 1982; Sharpe, Stockman & MacLeod, 1989; Stockman et al., 1991). One pathway--slow and sensitive--is accessible in the dark; whereas the other--fast and insensitive--becomes prominent at higher intensities. These two pathways must diverge at or before the outer plexiform layer, since both the slow and the fast signals are evident in the b-wave of the electroretinogram (ERG). But, because the two signals can also be demonstrated to interact and extinguish the b-wave, they probably also reconverge at a very early stage in the retina. These findings accord to some extent with anatomical and electrophysiological observations of the mammalian retina.
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References
Adelson, E.H., 1982, Saturation and adaptation in the rod system. Vision Research 22:1299–1312.
Aguilar, M. and Stiles, W.S., 1954, Saturation of the rod mechanism of the retina at high levels of stimulation. Optica Acta 1:59–65.
Alexander, K.R., and Fishman, G.A. 1984, Rod-cone interaction in flicker perimetry. British Journal of Ophthalmolgy 68:303–309.
Alexander, K.R., and Fishman, G.A. 1985, Rod-cone interaction in flicker perimetry: evidence for a distal retinal locus. Documenta Ophthalmologica 60:3–36.
Alpern, M., Falls, H.F., and Lee, G.B. 1960, The enigma of typical total monochromacy. American Journal of Ophthalamolgy 50:996–1012.
Andrews, D.P. and Hammond, P., 1970, Suprathreshold spectral properties of single optic tract fibres in cat, under mesopic adaptation: Cone-rod interaction. Journal of Physiology,London 209:83–103.
Arden, G.B. and Frumkes, T.E. 1986, Stimulation of rods can increase cone flicker ERGs in man. Vision Research 26:711–721.
Arden, G.B. and Hogg, C.R., 1985, Rod-cone interaction and analysis of retinal disease. British Journal of Ophthalmology 69:404–415.
Barlow, H.B., Fitzhugh, R., and Kuffler, S.W. 1957, Change of organization in the receptive fields of the cat’s retina during dark adaptation. Journal of Physiology, London 137:338–354.
Barlow, H.B. and Levick, W.R., 1969, Three factors limiting the reliable detection of light by retinal ganglion cells of the cat. Journal of Physiology,London 200:1–24.
Barlow, H.B., Levick, W.R., and Yoon, M., 1971, Responses to single quanta of light in retinal ganglion cells of the cat. Vision Research Supplement 3:87–101.
Bauer, G.M., Frumkes, T.E., and Nygaard, R.W., 1983, The signal-to-noise characteristics of rod-cone interaction. Journal of Physiology,London, 337:101–119.
Baylor, D.A., Fuortes, M.G.F., and O’Bryan, P.M., 1971, Receptive fields of cones in the retina of the turtle. Journal of Physiology, London,214:265–294.
Baylor, D.A., Lamb, T.D., and Yau, K.-W., 1979, The membrane current of single rod outer segments. Journal of Physiology,London, 288:589–611.
Baylor, D.A., Nunn, B.J., and Schnapf, J.L., 1984, The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca Fascicularis. Journal of Physiology, London 357:575–607.
van den Berg, T.J.T.P. and Spekreijse, H., 1977, Interaction between rod and cone signals studied with temporal sine wave stimulation. Journal of the Optical Society of America 67:1210–1217.
Blakemore, C.B. and Rushton, W.A.H., 1965, Dark adaptation and increment threshold in a rod monochromat. Journal of Physiology, London 181:612–628.
Bloomfield, S.A. and Miller, R.F., 1982, A physiological and morphological study of the horizontal cell types of the rabbit retina. Journal of comparative Neurology 208:288–303.
Boycott, B.B., Hopkins, J.M., and Sperling, H.G., 1987, Cone connections of the horizontal cells of the rhesus monkey’s retina. Proceedings of the Royal Society B229:345–379.
Buck, S.L., 1985, Cone-rod interaction over time and space. Vision Research 25:907–916.
Cajal, S.R., 1893, The vertebrate retina (translated by Maguire, D. and Rodieck, R.W.). In R.W. Rodieck, The vertebrate retina: Principles of structure and function, Appendix I 1973). San Francisco: W.H. Freeman.
Chase, L. and Dowling, J.E., 1990, A comparison of rod and cone pathways in the primate retina. Investigative Ophthalmology & Visual Science Supplement 31:207.
Coletta, N.J. and Adams, A.J., 1984, Rod-cone interactions in flicker detection. Vision Research 24:1333–1340.
Conner, J.D, 1982, The temporal properties of rod vision. Journal of Physiology, London 332:139–155.
Conner, J.D. and MacLeod, D.I.A., 1977, Rod photoreceptors detect rapid flicker. Science 195:689–699.
Curcio, C.A., Sloan, K.R., Packer, O., Hendrickson, A.E., and Kalina, R.E., 1987), Distribution of cones in human and monkey retina: individual variability and radial asymmetry. Science 236:579–582.
Dacheux, R.F. and Raviola, E., 1982, Horizontal cells in the retina of the rabbit. Journal of Neuroscience 2: 1486–1493.
Dacheux, R.F. and Raviola, E., 1986, The rod pathway in the rabbit retina: a depolarizing bipolar and amacrine cell. Journal of Neuroscience 6:331–345.
Daw, N.W., Jensen, R.J., and Brunken, W.J, 1990, Rod pathways in mammalian retinae. Trends in Neuro Sciences 13:110–115.
Daw, N.W. and Pearlman, A.L., 1969, Cat colour vision: one cone process or several? Journal of Physiology, London 201:745–764.
Denny, N., Frumkes, T.E., and Goldberg, S.H., 1990, Comparison of summatory and suppressive rod-cone interaction. Clinical Vision Sciences 5:27–36.
Dick, E. and Miller, R.F., 1978, Light-evoked potassium activity in mudpuppy retina: its relationship to the b-wave of the electroretinogram. Brain Research 154:388–394.
Dodt, E. and Jessen, K.H., 1961, The duplex nature of the retina of the nocturnal gecko as reflected in the electroretinogram. Journal of General Physiology 44:1143–1158.
Dowling, J.E., 1967, The site of visual adaptation. Science 155:273–279.
Dowling, J.E., 1987, The retina, an approachable part of the brain Belknap Press of Harvard University Press, Cambridge, Mass.
Dowling, J.E. and Ehinger, B., 1975, Synaptic organization of the amine-containing interplexiform cells of the goldfish and cebus monkey retina. Science 188:270–273.
Dowling, J.E., Ehinger, B., and Floren, I., 1980, Fluorescence and electron microscopical observations of the amine-accumulating neurons of the cebus monkey retina. Journal of comparative Neurology 192:655–685.
Enroth-Cugell, C., Hertz, B.G., and Lennie, P., 1977, Cone signals in the cat’s retina. Journal of Physiology, London 269:273–296.
Eysteinsson, T. and Frumkes, T.E., 1989, Physiological and pharmacological analysis of suppressive rod-cone interaction. Journal of Neurophysiology 61:866–877.
Fach, C.C., Sharpe, L.T., and Stockman, A., 1991, The field adaptation of the human rod visual system (submitted).
Famiglietti, E.V. and Kolb, H., 1975, A bistratified amacrine cell and synaptic circuitry in the inner plexiform layer of the retina. Brain Research 84:293–300.
Frumkes, T.E. and Eysteinsson, T., 1987, Suppressive rod-cone interaction in distal vertebrate retina: Intracellular records from xenopus and necturus. Journal of Neurophysiology 57:1361–1382.
Frumkes, T.E., Naarendorp, F., and Goldberg, S.H., 1986, The influence of cone adaptation upon rod mediated flicker. Vision Research 26:1167–1176.
Frumkes, T.E., Sekuler, M.D., Barris, M.C., Reiss, E.H., and Chalupa, L.M., 1973, Rod-cone interaction in human scotopic vision. I: temporal analysis. Vision Research 13:269–1282.
Frumkes, T.E. and Temme, L.A., 1977, Rod-cone interaction in human scotopic vision--II. Cones influence rod increment thresholds. Vision Research 17:673–679.
Glickstein, M. and Heath, G.G., 1975, Receptors in the monochromat eye. Vision Research 15:633–636.
Goldberg, S.H., Frumkes, T.E., and Nygaard, R.W., 1983, Inhibitory influence of unstimulated rods in the human retina: evidence provided by examining cone flicker. Science 221:180–182.
Gouras, P. and Link, K., 1966, Rod and cone interaction in dark-adapted monkey ganglion cells. Journal of Physiology, London,184:499–510.
Green, D.G. and Siegel, I.M., 1975, Double branched flicker fusion curves from the all-rod skate retina. Science 188:1120–1122.
Grünert, U. and Martin, P.R., 1990, Rod bipolar cells in the macaque monkey retina: Light and electron microscopy. Investigative Ophthalmology & Visual Science Supplement 31:536.
Gurevich, L., Stockton, R.A., and Slaughter, M.M., 1990, Comparisons of the waveforms of the B-wave of the ERG and ON bipolar cells. Investigative Ophthalmology & Visual Science Supplement 31:114.
Hassin, G. and Witkovsky, P., 1983, Intracellular recordings from identified photoreceptors and horizontal cells of the xenopus retina. Vision Research 23:921–932.
Hallett, P.E., 1962, Scotopic acuity and absolute threshold in brief flashes. Journal of Physiology,London, 163:175–189.
Harding, T.H. and Enroth-Cugell, C., 1978, Absolute dark sensitivity and centre size in cat retinal ganglion cells. Brain Research 153:157–162.
Hecht, S., Shlaer, S., Smith, E.L., Haig, C., and Peskin, J.C., 1938, The visual functions of a completely colorblind person. American Journal of Physiology 123:94–95.
Hecht, S., Shlaer, S., Smith, E.L., Haig, C., and Peskin, J.C., 1948, The visual functions of the complete colorblind. Journal of General Physiology 31:459–472.
Hendrickson, A., Koontz, M.A., Pourcho, R.G., Sarthy, P.V., and Goebel, D.J., 1988, Localization of glycine-containing neurons in the macaca monkey retina. Journal of comparative Neurology 273:473–487.
Hess, R.F. and Nordby, K., 1986, Spatial and temporal limits of vision in the achromat Journal of Physiology,London 371:365–385.
Hofmann, M.I., Barnes, C.S., and Hallett, P.E., 1990, Detection of briefly flashed sine-gratings in dark-adapted vision. Vision Research 30:1453–1466.
Kline, R.P., Ripps, H., and Dowling, J.E., 1978, Generation of b-wave currents in the skate retina. Proceedings of the National Academy of Sciences,U.S.A., 75:5727–5731.
Knight, R., Sanocki, E., and Buck, S.L., 1990, Field adaptation of dual rod mechanisms in the detection of 15 Hz flicker. Investigative Ophthalmology & Visual Science (supplement) 31:494.
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.
Kolb, H., 1979, The inner plexiform layer in the retina of the cat: electron microscopic observations. Journal of Neurocytology 8:295–329.
Kolb, H. and Famiglietti, E.V., 1974, Rod and cone pathways in the inner plexiform layer of cat retina. Science 186:47–49.
Kolb, H., Mariani, A., and Gallego, A., 1980, A second type of horizontal cells in the monkey retina. Journal of comparative Neurology 189:31–44.
Kolb, H. and Nelson, R., 1981, Amacrine cells of the cat retina. Vision Research 21: 1625–1633.
Kolb, H. and Nelson, R., 1983, Rod pathways in the retina of the cat. Vision Research 23:301–312
Kolb, H. and Nelson, R., 1984, Neural architecture of the cat retina. Progress in Retinal Research 3:21–60.
Kolb, H., Nelson, R., and Mariani, A., 1981, Amacrine cells, bipolar cells, and ganglion cells of the cat retina: a Golgi study. Vision Research 21:1081–1114.
Kolb, H. and West, R., 1977, Synaptic connections of the interplexiform cell in the retina of the cat. Journal of Neurocytology 6:155–170.
von Kries, J., 1894, Ober den Einfluß der Adaptation auf Licht-und Farbenempfindung und über die Funktion der Stäbchen. Bericht der naturforschenden Gesellschaft zu Freiburg im Breisgau 9 (2):61–70.
von Kries, J., 1929, Zur Theorie des Tages-und Dämmerungssehens. In A. Bethe, G. von Bergmann, G. Emden, and A. Ellinger (Eds), Handbuch der normalen und pathologischen Physiologie, Vol. XII (1), Receptionsorgane 2 (Photoreceptoren I) (pp. 679–713). Berlin: Springer-Verlag.
Lewis, S.D. and Mandelbaum, J., 1943, Achromatopsia: report of three cases. Archiv Ophthalmologica 30:225–231.
Loew, E.R. and Arden, G.B., 1985, Inhibition of cones by rods in the mammalian eye as demonstrated electrophysiologically using flashing multipoint focal stimuli. Investigative Ophthalmology & Visual Science Supplement 26:115.
MacLeod, D.I.A., 1972, Rods cancel cones in flicker. Nature 235:173–174.
MacLeod, D.I.A., 1974, Psychophysical studies of signals from rods and cones. Unpublished doctoral dissertation, Cambridge University.
Mariani, A.P., 1982, Biplexiform cells: ganglion cells of the primate retina that contact photoreceptors. Science 216:1134–1136.
Mariani, A.P., 1988, Amacrine cells of the rhesus monkey retina. Investigative Ophthalmology & Visual Science Supplement 29:198.
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.
McGuire, B.A., Stevens, J.K., and Sterling, P., 1984, Microcircuitry of bipolar cells in cat retina. Journal of Neurosciences 4:2920–2938.
Miller, R.F. and Dowling, J.E., 1970, Intracellular responses of the Müller (glial) cells of mudpuppy retina: Their relation to b-wave of the electroretinogram. Journal of Neurophysiology 33:323–341.
Müller, F., Wässle, H., and Voigt, T., 1988, Pharmacological modulation of the rod pathway in the cat retina. Journal of Neurophysiology 59:1657–1672.
Naka, K.-I., 1972, The horizontal cells. Vision Research 12:573–588.
Nakamura, Y., McGuire, B.A., and Sterling, P., 1980, Interplexiform cell in cat retina: Identification of uptake of o-[3H]aminobutyric acid and serial reconstruction. Proceedings of the National Academy of Sciences,Washington D.C.,77:658–661.
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 172:107–135.
Nelson, R., 1982, All amacrine cells quicken time course of rod signals in the cat retina. Journal of Neurophysiology 47:928–947.
Nelson, R., Famiglietti, E.V., and Kolb, H., 1978, Intracellular staining reveals different levels of stratification for on-and off-center ganglion cells in cat retina. Journal of Neurophysiology 41:472–483.
Nelson, R. and Kolb, H., 1983, Synaptic patterns and response properties of bipolar and ganglion cells in the cat retina. Vision Research 23:1183–1195.
Nelson, R. and Kolb, H., 1984, Amacrine cells in scotopic vision. Ophthalmological Research 16:21–26. Neurophysiology 54:592–614.
Nelson, R., von Lützow, A., Kolb, H., and Gouras, P., 1975, Horizontal cells in cat retina with independent dendritic systems. Science 189:137–139.
Noell, W.K., 1954, The origin of the electroretinogram. American Journal of Ophthalmology 28:78–90.
Nygaard, R.W. and Frumkes, T.E., 1985, Frequency dependence in scotopic flicker sensitivity. Vision Research 25:115–127.
Osterberg, G.A., 1935, Topography of the layer of rods and cones in the human retina. Acta ophthalmologica, Kobenhavn, supplement 6:1–102.
Parinaud, H., 1881, Des modifications pathologiques de la perception de la lumiere, des couleurs, et des formes, et des differentes especes de sensitibilite oculaire. Comptes rendus hebdomadaires des seances et memoires de la Societe de biologie, Paris, 33:222.
Pflug, R. and Nelson, R., 1986, Enhancement of red cone flicker by rod selective backgrounds in cat horizontal cells. Neuroscience Abstracts 16:402.
Polyak, S.L., 1941, The Retina. Chicago: Chicago University Press.
Raviola, E. and Gilula, N.B, 1973, Gap junctions between photoreceptor cells in the vertebrate retina. Proceedings of the National Academy of Sciences, Washington D.C., 70, 1677–1681.
Rodieck, R.W., 1988, The primate retina. Comparative Primate Biology 4, Neurosciences:302–278.
Schultze, M., 1866, Zur Anatomie und Physiologie der Retina. Archiv far mikroskopische Anatomie (und Entwicklungsmechanik) 2:175–286.
Shapley, R.M. and Enroth-Cugell, C., 1984, Visual adaptation and retinal gain controls. Progress in Retinal Research 3:263–346.
Sharpe, L.T., Fach, C., Nordby, K., and Stockman, A., 1989, The incremental threshold of the rod visual system and Weber’s law. Science 244:354–356.
Sharpe, L.T., Fach, C.C., and Stockman, A., 1991, Rod flicker perception: scotopic duality and cone intrusion (submitted).
Sharpe, L.T. and Nordby, K., 1990, The photoreceptors in the achromat. In R. F. Hess, L.T. Sharpe, and K. Nordby (Eds), Night Vision, basic, clinical and applied aspects. Cambridge: Cambridge University Press.
Sharpe, L.T., van Norren, D., and Nordby, K., 1988, Pigment regeneration, visual adaptation and spectral sensitivity in the achromat. Clinical Vision Sciences 3:9–17.
Sharpe, L.T., Stockman, A., and Macleod, D.I.A., 1989, Rod flicker perception: scotopic duality, phase lags and destructive interference. Vision Research 29:1539–1559.
Sharpe, L.T., Stockman, A., and Zrenner, E., 1990, Dual rod pathways. Perception 19: 350.
Sloan, L.L., 1954, Congenital achromatopsia: A report of 19 cases. Journal of the Optical Society of America 44:117–128.
Sloan, L.L., 1958, The photopic retinal receptors of the typical achromat. American Journal of Ophthalmology 46:81–86.
Smith, R.G., Freed, M.A., and Sterling, P., 1986, Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network. The Journal of Neuroscience 6:3505–3517.
Smith, V. C. and Pokorny, J., 1975, Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Research 15:161–171.
Steinberg, R.H., 1969, The rod after-effect in S-potentials from the cat retina. Vision Research 9:1345–1355.
Steinberg, R.H., 1971, Incremental responses to light recorded from pigment epithelial cells and horizontal cells of the cat retina. Journal of Physiology, London 217:93–110.
Steinberg, R.H., Reid, M., and Lacey, P.L., 1973, The distribution of rods and cones in the retina of the cat (Felis domesticus). Journal of comparative Neurology 148:229–248.
Sterling, P., 1983, Microcircuitry of the cat retina. Annual Review of Neuroscience 6:149–185.
Sterling, P., Freed, M., and Smith, R.G., 1986, Microcircuitry and functional architecture of the cat retina. Trends in Neuro Sciences 9:186–192.
Stockman, A., Sharpe, L.T., and Zrenner, E., 1990, Scotopic duality in the ERG and in psychophysics. Investigative Ophthalmology & Visual Science (supplement) 31:494.
Stockman, A., Sharpe, L.T., Zrenner, E., and Nordby, K., 1991, Slow and fast rod pathways in the human rod visual system (submitted)
Stockton, R.A., and Slaughter, M.M., 1987, ON bipolar cell potassium fluxes are uniquely associated with the ERG b-wave. Investigative Ophthalmology & Visual Science Supplement 28:406.
Tamura, T., Nakatani, K., and Yau, K.-W., 1989, Light adaptation in cat retinal rods. Science 245:755–758.
Toyoda, J.-I. and Tonosaki, K., 1978, Effect of polarization of horizontal cells on the on-center bipolar cells of the carp retina. Nature 276:399–400.
Wald, G., 1945, Human color vision and the spectrum. Science 101:653–658.
Wässle, H., Müller, F., Voigt, T., and Chun, M.H, 1989, Pharmacological modulation of the dark adapted cat retina. In R. Weiler, and N.N. Osborne (Eds), Neurobiology of the Inner Retina (pp. 247–259). Berlin: Springer-Verlag.
Wässle, H. and Riemann, H.J., 1978, The mosaic of nerve cells in the mammalian retina. Proceedings of the Royal Society, London, B200:441–461.
Weiler, R., 1977, Die Horizontalzellen der Karpenretina. Doctoral thesis, Universität München.
Wen, R., Tucker, J.L., and Oakley, B. I., 1990, Testing the K+/Müller cell hypothesis of the origin of the ERGB-wave. Investigative Ophthalmology & Visual Science Supplement 31:114.
Wyszecki, G. and Stiles, W.S., 1982, Color Science, concepts and methods, quantitative data and formulas (2nd Edn). New York: John Wiley.
Yang, X.-L. and Wu, S.M., 1989, Effects of background illumination on the horizontal cell responses in the tiger salamander retina. The Journal of Neuroscience 9:815–827.
Zrenner, E., Nelson, R., and Mariani, A., 1983, Intracellular recordings from a biplexiform ganglion cell in macaque retina, stained with horseradish peroxidase. Brain Research 262:181–185.
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Sharpe, L.T., Stockman, A. (1991). Dual Rod Pathways. In: Valberg, A., Lee, B.B. (eds) From Pigments to Perception. NATO ASI Series, vol 203. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3718-2_6
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