Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-23T19:17:33.220Z Has data issue: false hasContentIssue false
  • English
  • Français

Paradoxical shifts in human color sensitivity caused by constructive and destructive interference between signals from the same cone class

Published online by Cambridge University Press:  06 September 2006

ANDREW STOCKMAN ,
ETHAN D. MONTAG  and
DANIEL J. PLUMMER
ANDREW STOCKMAN
Affiliation:
Institute of Ophthalmology, University College London, London, United Kingdom
ETHAN D. MONTAG
Affiliation:
Rochester Institute of Technology, Center for Imaging Science, Munsell Color Science Laboratory, Rochester, New York
DANIEL J. PLUMMER
Affiliation:
Department of Psychology, University of California San Diego, La Jolla, California
Get access Rights & Permissions [Opens in a new window]

Abstract

Paradoxical shifts in human color (spectral) sensitivity occur on deep-red (658 nm) background fields. As the radiance of the deep-red background is increased from low to moderate levels, the spectral sensitivity for detecting 15-Hz flicker shifts toward shorter wavelengths, although by more than is predicted by selective chromatic adaptation (e.g., Eisner & MacLeod, 1981; Stromeyer et al., 1987; Stockman et al., 1993). Remarkably, though, at higher background radiances, the spectral sensitivity then shifts precipitously back towards longer wavelengths. Here, we show that both effects are due in large part to destructive and constructive interference between signals generated by the same cone type. Contrary to the conventional model of the human visual system, the M- and L-cone types contribute not just the customary fast signals to the achromatic or luminance pathway, but also slower signals of the same or opposite sign. The predominant signs of the slow M- and L-cone signals change with background radiance, but always remain spectrally opposed (M-L or L-M). Consequently, when the slow and fast signals from one cone type destructively interfere, as they do near 15 Hz, those from the other cone type constructively interfere, causing the paradoxical shifts in spectral sensitivity. The shift in spectral sensitivity towards longer wavelengths is accentuated at higher temporal frequencies by a suppression of fast M-cone signals by deep-red fields.

Keywords

Color visionSpectral sensitivityPostreceptoral channelsFlicker sensitivityPhase differencesLuminanceChromatic
Type
TEMPORAL FACTORS
Information
Visual Neuroscience , Volume 23 , Issue 3-4 , May 2006 , pp. 471 - 478
Copyright
© 2006 Cambridge University Press

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

Auerbach, E. & Wald, G. (1955). The participation of different types of cones in human light and dark adaptation. American Journal of Ophthalmology 39, 24–40.CrossRefGoogle Scholar
Benardete, E.A. & Kaplan, E. (1997). The receptive field of primate P retinal ganglion cell, I: Linear dynamics. Visual Neuroscience 14, 169–185.CrossRefGoogle Scholar
Boynton, R.M. (1979). Human Color Vision. New York: Holt, Rinehart and Winston.
Burns, S.A. & Elsner, A.E. (1985). Color matching at high luminances: The color-match-area effect and photopigment bleaching. Journal of the Optical Society of America A 2, 698–704.CrossRefGoogle Scholar
Burns, S.A. & Elsner, A.E., eds. (1989). Localizing Color Vision Deficiencies in Eye Disease, Vol. IX. Dordrecht: Kluwer Academic Publishers.
Cicerone, C.M. & Nerger, J.L. (1989). The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis. Vision Research 29, 115–128.CrossRefGoogle Scholar
Conway, B.R. (2001). Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1). Journal of Neuroscience 21, 2768–2783.Google Scholar
Cornsweet, T.N., Fowler, H., Rabedeau, R.G., Whalen, R.E., & Williams, D.R. (1958). Changes in the perceived color of very bright stimuli. Science 128, 898–899.CrossRefGoogle Scholar
Cottaris, N.P. & De Valois, R.L. (1998). Temporal dynamics of chromatic tuning in macaque primary visual cortex. Nature 395, 896–900.CrossRefGoogle Scholar
De Lange, H. (1958). Research into the dynamic nature of the human fovea-cortex systems with intermittent and modulated light. II. Phase shift in brightness and delay in color perception. Journal of the Optical Society of America 48, 784–789.Google Scholar
Derrington, A.M., Krauskopf, J., & Lennie, P. (1984). Chromatic mechanisms in lateral geniculate nucleus of macaque. Journal of Physiology 357, 241–265.CrossRefGoogle Scholar
De Vries, H. (1948). The heredity of the relative numbers of red and green receptors in the human eye. Genetica 24, 199–212.Google Scholar
Eisner, A. & MacLeod, D.I.A. (1980). Blue sensitive cones do not contribute to luminance. Journal of the Optical Society of America 70, 121–123.CrossRefGoogle Scholar
Eisner, A. & MacLeod, D.I.A. (1981). Flicker photometric study of chromatic adaptation: Selective suppression of cone inputs by colored backgrounds. Journal of the Optical Society of America 71, 705–718.CrossRefGoogle Scholar
Estévez, O. & Spekreijse, H. (1974). A spectral compensation method for determining the flicker characteristics of the human color mechanisms. Vision Research 14, 823–830.CrossRefGoogle Scholar
Gouras, P. (1974). Opponent-colour cells in different layers of foveal striate cortex. Journal of Physiology 238, 583–602.CrossRefGoogle Scholar
Gouras, P. & Zrenner, E. (1979). Enhancement of luminance flicker by color-opponent mechanisms. Science 205, 587–589.CrossRefGoogle Scholar
Guth, S.L., Alexander, J.V., Chumbly, J.I., Gillman, C.B., & Patterson, M.M. (1968). Factors affecting luminance additivity at threshold. Vision Research 8, 913–928.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215–243.CrossRefGoogle Scholar
Johnson, E.N., Hawken, M.J., & Shapley, R. (2004). Cone inputs in macaque primary visual cortex. Journal of Neurophysiology 91, 2501–2514.CrossRefGoogle Scholar
Lankheet, M.J.M., Lennie, P., & Krauskopf, J. (1998). Temporal-chromatic interactions in LGN P-cells. Visual Neuroscience 15, 47–54.CrossRefGoogle Scholar
Lee, B.B., Martin, P.R., & Valberg, A. (1989). Sensitivity of macaque retinal ganglion cells to chromatic and luminance flicker. Journal of Physiology 414, 223–243.CrossRefGoogle Scholar
Lee, B.B., Pokorny, J., Smith, V.C., & Kremers, J. (1994). Responses to pulses and sinusoids in macaque ganglion cells. Vision Research 34, 3081–3096.CrossRefGoogle Scholar
Lee, B.B. & Sun, H. (2004). Chromatic input to cells of the magnocellular pathway: Mean chromaticity and the relative phase of modulated lights. Visual Neuroscience 21, 309–314.CrossRefGoogle Scholar
Lennie, P., Krauskopf, J., & Sclar, G. (1990). Chromatic mechanisms in striate cortex of macaque. Journal of Neuroscience 10, 649–669.Google Scholar
Luther, R. (1927). Aus dem Gebiet der Farbreizmetrik. Zeitschrift für technische Physik 8, 540–558.Google Scholar
MacLeod, D.I.A., Stockman, A., & Vivian, J.A. (1985). Flicker photometric approximations to cone sensitivities under bleaching and transient adaptation conditions. Perception 14, A17.Google Scholar
Mahroo, O.A.R. & Lamb, T.D. (2004). Recovery of the human photopic electroretinogram after bleaching exposures: Estimation of pigment regeneration kinetics. Journal of Physiology 554, 417–437.CrossRefGoogle Scholar
Pokorny, J., Smith, V.C., Lee, B.B., & Yeh, T. (2001). Temporal sensitivity of macaque ganglion cells to lights of different chromaticity. Color Research Applications 26, S140–S144.3.0.CO;2-N>CrossRefGoogle Scholar
Reeves, A., Wu, S., & Schirillo, J. (1998). The effect of photon noise on the detection of white flashes. Vision Research 38, 691–703.CrossRefGoogle Scholar
Rushton, W.A.H. & Henry, G.H. (1968). Bleaching and regeneration of cone pigments in man. Vision Research 8, 617–631.CrossRefGoogle Scholar
Rushton, W.A.H., Powell, D.S., & White, K.D. (1973). The spectral sensitivities of the “red” and “green” cones in the normal eye. Vision Research 13, 2003–2015.CrossRefGoogle Scholar
Schmolesky, M.T., Wang, Y., Hanes, D.P., Thompson, K.G., Leutgeb, S., Schall, J.D., & Leventhal, A.G. (1998). Signal timing across the macaque visual system. Journal of Neurophysiology 79, 3272–3278.Google Scholar
Schrödinger, E. (1925). Über das Verhältnis der Vierfarben zur Dreifarbentheorie. Sitzungberichte Abt 2a, Mathematik, Astronomie, Physik, Meteorologie und Mechanik Akademie der Wissenschaften in Wien, Mathematisch-Naturwissenschaftliche Klasse 134, 471.Google Scholar
Sharpe, L.T., Stockman, A., Jagla, W., & Jägle, H. (2005). A luminous efficiency function, V*(l), for daylight adaptation. Journal of Vision 5, 948–968.Google Scholar
Smith, V.C., Lee, B.B., Pokorny, J., Martin, P.R., & Valberg, A. (1992). Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights. Journal of Physiology 458, 191–221.CrossRefGoogle Scholar
Smith, V.C. & Pokorny, J. (1975). Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm. Vision Research 15, 161–171.CrossRefGoogle Scholar
Smith, V.C, Pokorny, J., & van Norren, D. (1983). Densitometric measurement of human cone photopigment kinetics. Vision Research 23, 517–524.CrossRefGoogle Scholar
Stockman, A. (2001). Multiple cone inputs to luminance. Investigative Ophthalmology and Visual Science (Suppl.) 42, S320.Google Scholar
Stockman, A., MacLeod, D.I.A., & DePriest, D.D. (1991a). The temporal properties of the human short-wave photoreceptors and their associated pathways. Vision Research 31, 189–208.Google Scholar
Stockman, A., MacLeod, D.I.A., & Vivien, J.A. (1993). Isolation of the middle- and long-wavelength sensitive cones in normal trichromats. Journal of the Optical Society of America A 10, 2471–2490.CrossRefGoogle Scholar
Stockman, A., Montag, E.D., & MacLeod, D.I.A. (1991b). Large changes in phase delay on intense bleaching backgrounds. Investigative Ophthalmology and Visual Science (Suppl.) 32, 841.Google Scholar
Stockman, A. & Plummer, D.J. (1994). The luminance channel can be opponent?? Investigative Ophthalmology and Visual Science (Suppl.) 35, 1572.Google Scholar
Stockman, A. & Plummer, D.J. (2005a). Spectrally-opponent inputs to the human luminance pathway: Slow +L and −M cone inputs revealed by low to moderate long-wavelength adaptation. Journal of Physiology 566, 77–91.Google Scholar
Stockman, A. & Plummer, D.J. (2005b). Long-wavelength adaptation reveals slow, spectrally-opponent inputs to the human luminance pathway. Journal of Vision 5, 702–716.Google Scholar
Stockman, A., Plummer, D.J., & Montag, E.D. (2005). Spectrally-opponent inputs to the human luminance pathway: Slow +M and −L cone inputs revealed by intense long-wavelength adaptation. Journal of Physiology 566, 61–76.CrossRefGoogle Scholar
Stockman, A. & Sharpe, L.T. (1999). Cone spectral sensitivities and color matching. In Color Vision: From Genes to Perception, eds. Gegenfurtner, K. & Sharpe, L.T., pp. 53–87. Cambridge: Cambridge University Press.
Stockman, A. & Sharpe, L.T. (2000). Spectral sensitivities of the middle- and long-wavelength sensitive cones derived from measurements in observers of known genotype. Vision Research 40, 1711–1737.CrossRefGoogle Scholar
Stromeyer, C.F., III, Chaparro, A., Tolias, A.S., & Kronauer, R.E. (1997). Colour adaptation modifies the long-wave versus middle-wave cone weights and temporal phases in human luminance (but not red-green) mechanism. Journal of Physiology 499, 227–254.CrossRefGoogle Scholar
Stromeyer, C.F., III, Cole, G.R., & Kronauer, R.E. (1987). Chromatic suppression of cone inputs to the luminance flicker mechanisms. Vision Research 27, 1113–1137.Google Scholar
Vidyasagar, T.R., Kulikowski, J.J., Lipnicki, D.M., & Dreher, B. (2002). Convergence of parvocellular and magnocellular information channels in the primary visual cortex of the macaque. European Journal of Neuroscience 16, 945–956.CrossRefGoogle Scholar
Vos, J.J. & Walraven, P.L. (1971). On the derivation of the foveal receptor primaries. Vision Research 11, 799–818.CrossRefGoogle Scholar
Walls, G.L. (1955). A branched-pathway schema for the color-vision system and some of the evidence for it. American Journal of Ophthalmology 39, 8–23.CrossRefGoogle Scholar
Walraven, P.L. (1974). A closer look at the tritanopic confusion point. Vision Research 14, 1339–1343.CrossRefGoogle Scholar