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Spectral sensitivity of ON and OFF responses from the optic nerve of goldfish

Published online by Cambridge University Press:  02 June 2009

Paul J. DeMarco Jr
Affiliation:
Department of Psychology and Vision Research Center, Vanderbilt University, Nashville
Maureen K. Powers
Affiliation:
Department of Psychology and Vision Research Center, Vanderbilt University, Nashville

Abstract

The vertebrate retina processes visual information in parallel neural pathways known as the ON and OFF pathways. These pathways encode increments and decrements of light independently as excitatory responses. We examined the photopic spectral response of ON and OFF mechanisms in goldfish by measuring the sensitivity of optic nerve responses to the onset and termination of stimuli of various wavelengths. Using various adapting backgrounds, we found that the ON and OFF responses have different spectral sensitivities. The weighting of the cone inputs to the responses was estimated by an algebraic summation model. This model suggests that for the ON response, input from S-cones is stronger and more independent than for the OFF response, and M- and L-cones show stronger antagonism in the ON response than in the OFF response. The OFF response probably receives input from all cone types, but spectral antagonism is weak and its dominant input is from L-cones.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1991

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References

Adrian, E.D. & Matthews, R. (1927). The action of light on the eye. Journal of Physiology 63, 378414.CrossRefGoogle ScholarPubMed
Barlow, H.B., Fitzhugh, R. & Kuffler, S.W. (1957). Change in organization in the receptive fields of the cat's retina during dark-adaptation. Journal of Physiology 137, 338354.CrossRefGoogle ScholarPubMed
Bassi, C.J., Williams, R.C. & Powers, M.K. (1984). Light transmittance by goldfish eyes of different sizes. Vision Research 24, 14151419.CrossRefGoogle ScholarPubMed
Beauchamp, R.D. & Lovasik, J.V. (1973). Blue mechanism response of single goldfish optic fibers. Journal of Neurophysiology 36, 925939.CrossRefGoogle ScholarPubMed
Beauchamp, R.D. & Rowe, J.S. (1977). Goldfish spectral sensitivity: a conditioned heart rate measure in restrained or curarized fish. Vision Research 17, 617624.CrossRefGoogle ScholarPubMed
Beauchamp, R.D., Rowe, J.S. & O'Reilly, L.A. (1979). Goldfish spectral sensitivity: identification of the three cone mechanisms in heart-rate conditioned fish using colored adapting backgrounds. Vision Research 19, 12951302.CrossRefGoogle ScholarPubMed
Bowen, R.W., Pokorny, J. & Smith, V.C. (1989). Sawtooth contrast sensitivity: decrements have the edge. Vision Research 29, 15011509.CrossRefGoogle ScholarPubMed
Boynton, R.M., Ikeda, M. & Stiles, W.S. (1964). Interactions among chromatic mechanisms as inferred from positive and negative increments thresholds. Vision Research, 4, 87177.CrossRefGoogle ScholarPubMed
Caceci, M.S. & Cacheris, W.P. (1984). Fitting curves to data. Byte 5, 340360.Google Scholar
Cohn, T.E. & Lesley, D.J. (1975). Spatial summation of foveal increments and decrements. Vision Research, 15, 389399.CrossRefGoogle ScholarPubMed
Daw, N.W. (1967). Goldfish retina: organization for simultaneous color contrast. Science 158, 942944.CrossRefGoogle ScholarPubMed
De Monasterio, F.M. (1979). Asymmetry of on- and off-pathways of blue sensitive cones of the retina of macaques. Brain Research 166, 3948.CrossRefGoogle Scholar
Easter, S.S., Johns, P.R. & Baumann, L.R. (1977). Growth of adult goldfish eye, 1: Optics. Vision Research, 17, 469477.CrossRefGoogle Scholar
Evers, H.U. & Gouras, P. (1986). Three cone mechanisms in the primate retina: two with, one without OFF-center bipolar responses. Vision Research, 26, 245254.CrossRefGoogle ScholarPubMed
Falzett, M., Nussdorf, J.D. & Powers, M.K. (1988). Responsivity and absolute sensitivity of retinal ganglion cells in goldfish of different sizes, when measured under “psychophysical” conditions. Vision Research 28, 223237.CrossRefGoogle ScholarPubMed
Famiglietti, E.V., Kaneko, A. & Tachibana, M. (1977). Neuronal architecture of ON and OFF pathways to ganglion cells in carp retina. Science 198, 12671269.CrossRefGoogle Scholar
Hárosi, F.I. (1976). Spectral relations of cone pigments in goldfish. Journal of General Physiology 68, 6580.CrossRefGoogle ScholarPubMed
Hartline, H.K. (1938). The response of single optic nerve fibers of vertebrate eye to illumination of the retina. American Journal Physiology 121, 400415.CrossRefGoogle Scholar
Hashimoto, Y., Abe, M. & Inokuchi, M. (1980). Identification of interplexiform cell in dace retina by dye-injection method. Brain Research 197, 331340.CrossRefGoogle ScholarPubMed
Hawryshyn, C.W. & Beauchamp, R. (1985). Ultraviolet photosensitivity in goldfish: an independent U.V. retinal mechanism. Vision Research, 25, 1120.CrossRefGoogle ScholarPubMed
Herrick, R.M. (1956). Foveal luminance discrimination as a function of the decrement or increment in luminance. Journal of Comparative Physiology and Psychology 49, 437443.CrossRefGoogle ScholarPubMed
Hubel, D.H. & Wiesel, T.N. (1960). Receptive fields of optic nerve fibers in the spider monkey. Journal of Physiology 154, 572580.CrossRefGoogle ScholarPubMed
Krauskopf, J. (1980). Discrimination and detection of changes in luminance. Vision Research 20, 671677.CrossRefGoogle ScholarPubMed
Kretz, R., Rager, G. & Norton, T.T. (1986). Laminar organization of on and off regions and ocular dominance in the striate cortex of the tree shrew (Tupaia belangeri). Journal of Comparative Neurology 251, 135145.CrossRefGoogle Scholar
Kuffler, S.W. (1953). Discharge patterns and functional organization of mammalian retina. Journal of Neurophysiology 16, 3768.CrossRefGoogle ScholarPubMed
LeVay, S., McConnell, S.K. & Luskin, M.B. (1987). Functional organization of primary visual cortex in the mink (Mustela vison), and a comparison with the cat. Journal of Comparative Neurology 257, 422441.CrossRefGoogle Scholar
Mackintosh, R.M., Bilotta, J. & Abramov, I. (1987). Contributions of short-wavelength cones to goldfish retinal ganglion cells. Journal of Comparative Physiology A 161, 8594.CrossRefGoogle Scholar
Malpeli, J.G., & Schiller, P.H. (1978). Lack of blue off-center cells in the visual system of the monkey. Brain Research 141, 385389.CrossRefGoogle ScholarPubMed
Marks, W.B. (1965). Visual pigments of single goldfish cones. Journal of Physiology 178, 1432.CrossRefGoogle ScholarPubMed
Mills, S.L., & Sperling, H.G. (1990). Red/green opponency in the rhesus macaque ERG spectral sensitivity is reduced by bicuculline. Visual Neuroscience 5, 217221.CrossRefGoogle ScholarPubMed
Muntz, W.R.A. (1962). Microelectrode recordings from the diencephalon of the frog (Rana Pipens), and a blue-sensitive system. Journal of Neurophysiology 25, 699711.CrossRefGoogle Scholar
Naka, K.-I. (1976). Neuronal circuitry in the catfish retina. Investigative Ophthalmology 15, 926934.Google Scholar
Nelson, R., Famiglietti, E.V., & Kolb, H. (1978). Intracellular staining reveals different levels of stratification for ON- and OFF-center ganglion cells in cat retina. Journal of Neurophysiology 41, 472483.CrossRefGoogle ScholarPubMed
Neumeyer, C. (1984). On spectral sensitivity of the goldfish: evidence for neural interactions between different “cone mechanisms”. Vision Research, 24, 12231231.CrossRefGoogle ScholarPubMed
Neumeyer, C., & Arnold, K. (1989). Tetrachromatic color vision in the goldfish becomes trichromatic under white adaptation light of moderate intensity. Vision Research, 29, 17191727.CrossRefGoogle ScholarPubMed
Olsen, B.T., Schneider, T., & Zrenner, E. (1986). Characteristics of rod driven off-responses in cat ganglion cells. Vision Research, 26, 835845.CrossRefGoogle ScholarPubMed
Patel, A.S., & Jones, R.W. (1968). Increment and decrement visual thresholds. Journal of the Optical Society of America 58, 696699.CrossRefGoogle ScholarPubMed
Powers, M.K. (1978). Light-adapted spectral sensitivity of the goldfish: a reflex measure. Vision Research, 18, 11311136.CrossRefGoogle ScholarPubMed
Rashbass, C. (1970). The visibility of transient changes in luminance. Journal of Physiology 210, 165186.CrossRefGoogle ScholarPubMed
Roufs, J.A.J. (1974). Dynamic properties of vision–IV: Thresholds of decremental flashes, incremental flashes, and doublets in relation to flicker fusion. Vision Research, 14, 831852.CrossRefGoogle Scholar
Schiller, P.H. (1984). The connections of the retinal on and off pathways to the lateral geniculate nucleus of the monkey. Vision Research, 24, 923932.CrossRefGoogle Scholar
Shefner, J.M., & Levine, M.W. (1976). A psychophysical demonstration of goldfish trichromacy. Vision Research, 16, 671673.CrossRefGoogle ScholarPubMed
Short, A.D. (1966). Decremental and incremental thresholds. Journal of Physiology 185, 646654.CrossRefGoogle Scholar
Sperling, H.G., & Harwerth, R.S. (1971). Red-green cone interactions in the increment-threshold spectral sensitivity of primates. Science 72, 180184.CrossRefGoogle Scholar
Thorpe, S.A. (1972). The effect of chromatic adaptation and temperature on the spectral sensitivity of the goldfish (Carassius auratus). Doctoral Thesis, Brown University.Google Scholar
va, Duk B.W., & Spekreijse, H. (1984). Color fundamentals deduced from carp ganglion cell responses. Vision Research, 24, 211220.Google Scholar
Wagner, H.G., MacNichol, E.F., & Wolbrasht, M.L. (1960). The response properties of single ganglion cells in the goldfish retina. Journal of General Physiology 43, 4562.CrossRefGoogle ScholarPubMed
Werblin, F.S., & Dowling, J.E. (1969). Organization of the retina of the mudpuppy (Necturus maculosus), II: Intracellular recordings. Journal of Neurophysiology 32, 339355.CrossRefGoogle Scholar
Wheeler, T.G. (1979). Retinal on and off responses convey different chromatic information to the CNS. Brain Research 160, 145149.CrossRefGoogle ScholarPubMed
Witkovsky, P. (1965). The spectral sensitivity of retinal ganglion cells in the carp. Vision Research, 5, 603614.CrossRefGoogle ScholarPubMed
Wolbarsht, M.L., Wagner, H.G., & MacNichol, E.F. (1961). The origin of “on” and “off” responses of retinal ganglion cells. The Visual System: Neurophysiology and Psychophysics, ed. Jung, R. and Kornhuber, H.H. pp. 163170.Berlin: Springer-Verlag.Google Scholar
Yager, D. (1967). Behavioral measures and theoretical analysis of spectral sensitivity and spectral saturation in the goldfish(Carassius auratus). Vision Research 7, 707727.CrossRefGoogle ScholarPubMed
Yager, D. (1969). Behavioral measures of spectral sensitivity in the goldfish following chromatic adaption. Vision Research, 9, 179186.CrossRefGoogle Scholar
Zemon, V., Gordon, J., & Welch, J. (1988). Asymmetries in ON and OFF visual pathways of humans revealed using contrast-evoked cortical potentials. Visual Neuroscience 1, 145150.CrossRefGoogle Scholar
Zrenner, E., & Gouras, P. (1981). Characteristics of the blue-sensitive cone mechanism in primate retinal ganglion cells. Vision Research, 21, 16051609.CrossRefGoogle ScholarPubMed