Abstract

In dialogue, two color scientists introduce the topic of color opponency, as seen from the viewpoints of color appearance (psychophysics) and measurement of nerve cell responses (physiology). Points of difference as well as points of convergence between these viewpoints are explained. Key experiments from the psychophysical and physiological literature are covered in detail to help readers from these two broad fields understand each other’s work.

© 2017 Optical Society of America

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Color coding in the primate visual pathway: a historical view

Barry B. Lee
J. Opt. Soc. Am. A 31(4) A103-A112 (2014)

References

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  1. E. Hering, “Grundzüge einer Theorie des Farbensinnes (originally published in 1874),” in Zur Lehre vom Lichtsinn (Gerald u. Söhne, 1878), pp. 107–141.
  2. R. S. Turner, “Vision studies in Germany: Helmholtz versus Hering,” Osiris 8, 80–103 (1993).
    [Crossref]
  3. T. Young, “The Bakerian lecture: on the theory of light and colours,” Philos. Trans. R. Soc. London 92, 12–48 (1802).
    [Crossref]
  4. J. D. Mollon, “The origins of modern color science,” in The Science of Color, S. K. Shevell, ed. (Optical Society of America/Elsevier, 2003), pp. 1–39.
  5. H. Helmholtz, Helmholtz’s Treatise on Physiological Optics, J. P. C. Southall, ed. (Dover, 1962), Vol. 1–2.
  6. In 1924 the Optical Society of America published an English translation of the third German edition, edited by James Southall.
  7. R. S. Turner, In the Eye’s Mind (Princeton University, 1994).
  8. D. Jameson and L. M. Hurvich, “Some quantitative aspects of an opponent-colors theory, I: chromatic responses and spectral saturation,” J. Opt. Soc. Am. 45, 546–552 (1955).
    [Crossref]
  9. The solid symbols in Fig. 2(d) are scaled by a factor that equates the units of the 500 and 700 nm lights. The factor is determined by the ratio of 500 to 700 nm light that in mixture appears neither reddish nor greenish.
  10. Open symbols in Fig. 2(d) are scaled by a factor that equates the units of the 475 and 580 nm lights. The factor is determined by the ratio of 475 to 580 nm light that in mixture appears neither yellowish nor bluish. A second scaling factor adjusts the overall height of the red–green curve (solid symbols) relative to the height of the yellow–blue curve (open symbols). This scaling is based on wavelengths perceived to have two hues of equal magnitude (for example, a wavelength that appears an orange judged to have equal parts redness and yellowness).
  11. J. D. Mollon and G. Jordan, “On the nature of unique hues,” in John Dalton’s Colour Vision Legacy, C. M. Dickinson, I. J. Murray, and D. Carden, eds. (Taylor & Francis, 1997), pp. 381–392.
  12. R. L. DeValois, I. Abramov, and G. H. Jacobs, “Analysis of response patterns of LGN cells,” J. Opt. Soc. Am. 56, 966–977 (1966).
    [Crossref]
  13. S. G. Solomon, B. B. Lee, A. J. White, L. Rüttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
    [Crossref]
  14. V. C. Smith and J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500  nm,” Vis. Res. 15, 161–171 (1975).
    [Crossref]
  15. A. Stockman and L. T. Sharpe, “The spectral sensitivities of the middle- and long-wavelength-sensitive cones derived from measurements in observers of known genotype,” Vis. Res. 40, 1711–1737 (2000).
    [Crossref]
  16. W. H. Swanson, J. Pokorny, and V. C. Smith, “Effects of temporal frequency on phase-dependent sensitivity to heterochromatic flicker,” J. Opt. Soc. Am. A 4, 2266–2273 (1987).
    [Crossref]
  17. S. G. Solomon, P. R. Martin, A. J. R. White, L. Rüttiger, and B. B. Lee, “Modulation sensitivity of ganglion cells in peripheral retina of macaque,” Vis. Res. 42, 2893–2898 (2002).
    [Crossref]
  18. V. C. Smith, B. B. Lee, J. Pokorny, P. R. Martin, and A. Valberg, “Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights,” J. Physiol. 458, 191–221 (1992).
    [Crossref]
  19. B. R. Conway, D. H. Hubel, and M. S. Livingstone, “Color contrast in macaque V1,” Cereb. Cortex 12, 915–925 (2002).
    [Crossref]
  20. E. N. Johnson, M. J. Hawken, and R. Shapley, “The orientation selectivity of color-responsive neurons in macaque V1,” J. Neurosci. 28, 8096–8106 (2008).
    [Crossref]
  21. K. Gegenfurtner, “Cortical mechanisms of colour vision,” Nat. Rev. Neurosci. 4, 563–572 (2003).
    [Crossref]
  22. J. Liu and B. A. Wandell, “Specializations for chromatic and temporal signals in human visual cortex,” J. Neurosci. 25, 3459–3468 (2005).
    [Crossref]
  23. In the proper historical context, Eq. (1) is a “hypothetical neural mechanism” of the sort disparaged by Helmholtz because it preceded the discovery of primate color-opponent neurons or even knowledge of the now-well-accepted L-, M-, and S-cone spectral sensitivity functions.
  24. K. Knoblauch and S. K. Shevell, “Relating cone signals to color appearance: failure of monotonicity in yellow/blue,” Visual Neurosci. 18, 901–906 (2001).
  25. Because we know the physical (radiometric) properties of the [RGB] monitor beams as well as the biological (photometric) properties of the human [LMS] cone receptors, we can predict what effect any RGB level within the gamut will have on the LMS receptors. Even better (and thinking the other way around), we can decide what LMS activation level we want, and set the RGB levels accordingly.
  26. The 180° direction is the same as the zero direction, of course, but the modulation begins at the other side of the circle. If you look closely you can see that the histogram peaks are displaced (that is, shifted in time) by about 180° for the opposite modulation direction.
  27. E. Zrenner and P. Gouras, “Characteristics of the blue sensitive cone mechanism in primate retinal ganglion cells,” Vis. Res. 21, 1605–1609 (1981).
    [Crossref]
  28. T. N. Wiesel and D. Hubel, “Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey,” J. Neurophysiol. 29, 1115–1156 (1966).
  29. B. B. Lee, A. Valberg, D. A. Tigwell, and J. Tryti, “An account of responses of spectrally opponent neurons in macaque lateral geniculate nucleus to successive contrast,” Proc. R. Soc. London B 230, 293–314 (1987).
  30. B. Dreher, Y. Fukada, and R. W. Rodieck, “Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old-world primates,” J. Physiol. 258, 433–452 (1976).
    [Crossref]
  31. J. D. Mollon, ““Tho she kneel’d in the place where they grew.” The uses and origins of primate colour vision,” J. Exp. Biol. 146, 21–38 (1989).
  32. J. Kremers, ed., The Primate Visual System: A Comparative Approach (Wiley, 2005).
  33. G. H. Jacobs, “Primate color vision: a comparative perspective,” Visual Neurosci. 25, 619–633 (2008).
  34. C. Tailby, S. G. Solomon, and P. Lennie, “Functional asymmetries in visual pathways carrying S-cone signals in macaque,” J. Neurosci. 28, 4078–4087 (2008).
    [Crossref]
  35. L. E. Wool, S. J. Komban, J. Kremkow, M. Jansen, X. Li, J. M. Alonso, and Q. Zaidi, “Salience of unique hues and implications for color theory,” J. Vis. 15(2), 10 (2015).
    [Crossref]
  36. Importantly, pure color changes from white are made while keeping the overall light level constant; that is, all color changes occur at constant luminance. This guarantees the threshold is mediated by a chromatic neural response.
  37. J. Krauskopf, D. R. Williams, and D. W. Heeley, “Cardinal directions of color space,” Vis. Res. 22, 1123–1131 (1982).
    [Crossref]
  38. J. M. Crook, B. B. Lee, D. A. Tigwell, and A. Valberg, “Thresholds to chromatic spots of cells in the macaque geniculate nucleus as compared to detection sensitivity in man,” J. Physiol. 392, 193–211 (1987).
    [Crossref]
  39. A. Chaparro, C. F. Stromeyer, E. P. Huang, R. E. Kronauer, and R. T. Eskew, “Colour is what the eye sees best,” Nature 361, 348–350 (1993).
    [Crossref]
  40. A. M. Derrington, J. Krauskopf, and P. Lennie, “Chromatic mechanisms in lateral geniculate nucleus of macaque,” J. Physiol. 357, 241–265 (1984).
    [Crossref]
  41. I. Ohzawa, G. Sclar, and R. D. Freeman, “Contrast gain control in the cat’s visual system,” J. Neurophysiol. 54, 651–667 (1985).
  42. C. Tailby, S. G. Solomon, and P. Lennie, “Habituation reveals fundamental chromatic mechanisms in striate cortex of macaque,” J. Neurosci. 28, 1131–1139 (2008).
    [Crossref]
  43. J. Krauskopf, D. R. Williams, M. B. Mandler, and A. M. Brown, “Higher order color mechanisms,” Vis. Res. 26, 23–32 (1986).
    [Crossref]
  44. J. Larimer, D. H. Krantz, and C. M. Cicerone, “Opponent process additivity, II: yellow/blue equilibria and nonlinear models,” Vis. Res. 15, 723–731 (1975).
    [Crossref]
  45. M. S. Livingstone and D. H. Hubel, “Anatomy and physiology of a color system in the primate visual cortex,” J. Neurosci. 4, 309–356 (1984).
  46. S. Zeki, “The representation of colours in the cerebral cortex,” Nature 284, 412–418 (1980).
    [Crossref]
  47. C. M. Stoughton and B. R. Conway, “Neural basis for unique hues,” Curr. Biol. 18, R698–R699 (2008).
    [Crossref]
  48. A. G. Leventhal, K. G. Thompson, D. Liu, Y. Zhou, and S. J. Ault, “Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex,” J. Neurosci. 15, 1808–1818 (1995).
  49. E. N. Johnson, M. J. Hawken, and R. Shapley, “The spatial transformation of color in the primary visual cortex of the macaque monkey,” Nat. Neurosci. 4, 409–416 (2001).
    [Crossref]
  50. B. R. Conway, “Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1),” J. Neurosci. 21, 2768–2783 (2001).
  51. G. D. Horwitz, E. J. Chichilnisky, and T. D. Albright, “Blue-yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1,” J. Neurophysiol. 93, 2263–2278 (2005).
    [Crossref]
  52. B. R. Conway, S. Moeller, and D. Y. Tsao, “Specialized color modules in macaque extrastriate cortex,” Neuron 56, 560–573 (2007).
    [Crossref]
  53. R. Shapley and M. J. Hawken, “Color in the cortex: single- and double-opponent cells,” Vis. Res. 51, 701–717 (2011).
    [Crossref]
  54. D. Y. Ts’o and C. D. Gilbert, “The organization of chromatic and spatial interactions in the primate striate cortex,” J. Neurosci. 8, 1712–1727 (1988).
  55. E. N. Johnson, M. J. Hawken, and R. Shapley, “Cone inputs in macaque primary visual cortex,” J. Neurophysiol. 91, 2501–2514 (2004).
    [Crossref]
  56. D. L. Ringach, G. Sapiro, and R. Shapley, “A subspace reverse-correlation technique for the study of visual neurons,” Vis. Res. 37, 2455–2464 (1997).
    [Crossref]
  57. P. Lennie, J. Krauskopf, and G. Sclar, “Chromatic mechanisms in striate cortex of macaque,” J. Neurosci. 10, 649–669 (1990).
  58. K. R. Gegenfurtner, D. C. Kiper, and J. B. Levitt, “Functional properties of neurons in macaque area V3,” J. Neurophysiol. 77, 1906–1923 (1997).
  59. G. D. Horwitz and C. A. Hass, “Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing,” Nat. Neurosci. 15, 913–919 (2012).
    [Crossref]
  60. H. Komatsu, Y. Ideura, S. Kaji, and S. Yamane, “Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey,” J. Neurosci. 12, 408–424 (1992).
  61. H. E. Smithson, “Sensory, computational and cognitive components of human colour constancy,” Philos. Trans. R. Soc. B 360, 1329–1346 (2005).
    [Crossref]
  62. S. K. Shevell and F. A. Kingdom, “Color in complex scenes,” Ann. Rev. Psychol. 59, 143–166 (2008).
    [Crossref]
  63. D. H. Foster, “Color constancy,” Vis. Res. 51, 674–700 (2011).
    [Crossref]
  64. J. Mollon, “Monge,” Visual Neurosci. 23, 297–309 (2006).
  65. M. Greschner, J. Shlens, C. Bakolitsa, G. D. Field, J. L. Gauthier, L. H. Jepson, A. Sher, A. M. Litke, and E. J. Chichilnisky, “Correlated firing among major ganglion cell types in primate retina,” J. Physiol. 589, 75–86 (2011).
    [Crossref]
  66. R. C. Kelly, M. A. Smith, J. M. Samonds, A. Kohn, A. B. Bonds, J. A. Movshon, and T. S. Lee, “Comparison of recordings from microelectrode arrays and single electrodes in the visual cortex,” J. Neurosci. 27, 261–264 (2007).
    [Crossref]

2015 (1)

L. E. Wool, S. J. Komban, J. Kremkow, M. Jansen, X. Li, J. M. Alonso, and Q. Zaidi, “Salience of unique hues and implications for color theory,” J. Vis. 15(2), 10 (2015).
[Crossref]

2012 (1)

G. D. Horwitz and C. A. Hass, “Nonlinear analysis of macaque V1 color tuning reveals cardinal directions for cortical color processing,” Nat. Neurosci. 15, 913–919 (2012).
[Crossref]

2011 (3)

D. H. Foster, “Color constancy,” Vis. Res. 51, 674–700 (2011).
[Crossref]

R. Shapley and M. J. Hawken, “Color in the cortex: single- and double-opponent cells,” Vis. Res. 51, 701–717 (2011).
[Crossref]

M. Greschner, J. Shlens, C. Bakolitsa, G. D. Field, J. L. Gauthier, L. H. Jepson, A. Sher, A. M. Litke, and E. J. Chichilnisky, “Correlated firing among major ganglion cell types in primate retina,” J. Physiol. 589, 75–86 (2011).
[Crossref]

2008 (6)

S. K. Shevell and F. A. Kingdom, “Color in complex scenes,” Ann. Rev. Psychol. 59, 143–166 (2008).
[Crossref]

C. M. Stoughton and B. R. Conway, “Neural basis for unique hues,” Curr. Biol. 18, R698–R699 (2008).
[Crossref]

G. H. Jacobs, “Primate color vision: a comparative perspective,” Visual Neurosci. 25, 619–633 (2008).

C. Tailby, S. G. Solomon, and P. Lennie, “Functional asymmetries in visual pathways carrying S-cone signals in macaque,” J. Neurosci. 28, 4078–4087 (2008).
[Crossref]

C. Tailby, S. G. Solomon, and P. Lennie, “Habituation reveals fundamental chromatic mechanisms in striate cortex of macaque,” J. Neurosci. 28, 1131–1139 (2008).
[Crossref]

E. N. Johnson, M. J. Hawken, and R. Shapley, “The orientation selectivity of color-responsive neurons in macaque V1,” J. Neurosci. 28, 8096–8106 (2008).
[Crossref]

2007 (2)

B. R. Conway, S. Moeller, and D. Y. Tsao, “Specialized color modules in macaque extrastriate cortex,” Neuron 56, 560–573 (2007).
[Crossref]

R. C. Kelly, M. A. Smith, J. M. Samonds, A. Kohn, A. B. Bonds, J. A. Movshon, and T. S. Lee, “Comparison of recordings from microelectrode arrays and single electrodes in the visual cortex,” J. Neurosci. 27, 261–264 (2007).
[Crossref]

2006 (1)

J. Mollon, “Monge,” Visual Neurosci. 23, 297–309 (2006).

2005 (4)

H. E. Smithson, “Sensory, computational and cognitive components of human colour constancy,” Philos. Trans. R. Soc. B 360, 1329–1346 (2005).
[Crossref]

G. D. Horwitz, E. J. Chichilnisky, and T. D. Albright, “Blue-yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1,” J. Neurophysiol. 93, 2263–2278 (2005).
[Crossref]

J. Liu and B. A. Wandell, “Specializations for chromatic and temporal signals in human visual cortex,” J. Neurosci. 25, 3459–3468 (2005).
[Crossref]

S. G. Solomon, B. B. Lee, A. J. White, L. Rüttiger, and P. R. Martin, “Chromatic organization of ganglion cell receptive fields in the peripheral retina,” J. Neurosci. 25, 4527–4539 (2005).
[Crossref]

2004 (1)

E. N. Johnson, M. J. Hawken, and R. Shapley, “Cone inputs in macaque primary visual cortex,” J. Neurophysiol. 91, 2501–2514 (2004).
[Crossref]

2003 (1)

K. Gegenfurtner, “Cortical mechanisms of colour vision,” Nat. Rev. Neurosci. 4, 563–572 (2003).
[Crossref]

2002 (2)

S. G. Solomon, P. R. Martin, A. J. R. White, L. Rüttiger, and B. B. Lee, “Modulation sensitivity of ganglion cells in peripheral retina of macaque,” Vis. Res. 42, 2893–2898 (2002).
[Crossref]

B. R. Conway, D. H. Hubel, and M. S. Livingstone, “Color contrast in macaque V1,” Cereb. Cortex 12, 915–925 (2002).
[Crossref]

2001 (3)

K. Knoblauch and S. K. Shevell, “Relating cone signals to color appearance: failure of monotonicity in yellow/blue,” Visual Neurosci. 18, 901–906 (2001).

E. N. Johnson, M. J. Hawken, and R. Shapley, “The spatial transformation of color in the primary visual cortex of the macaque monkey,” Nat. Neurosci. 4, 409–416 (2001).
[Crossref]

B. R. Conway, “Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1),” J. Neurosci. 21, 2768–2783 (2001).

2000 (1)

A. Stockman and L. T. Sharpe, “The spectral sensitivities of the middle- and long-wavelength-sensitive cones derived from measurements in observers of known genotype,” Vis. Res. 40, 1711–1737 (2000).
[Crossref]

1997 (2)

D. L. Ringach, G. Sapiro, and R. Shapley, “A subspace reverse-correlation technique for the study of visual neurons,” Vis. Res. 37, 2455–2464 (1997).
[Crossref]

K. R. Gegenfurtner, D. C. Kiper, and J. B. Levitt, “Functional properties of neurons in macaque area V3,” J. Neurophysiol. 77, 1906–1923 (1997).

1995 (1)

A. G. Leventhal, K. G. Thompson, D. Liu, Y. Zhou, and S. J. Ault, “Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex,” J. Neurosci. 15, 1808–1818 (1995).

1993 (2)

R. S. Turner, “Vision studies in Germany: Helmholtz versus Hering,” Osiris 8, 80–103 (1993).
[Crossref]

A. Chaparro, C. F. Stromeyer, E. P. Huang, R. E. Kronauer, and R. T. Eskew, “Colour is what the eye sees best,” Nature 361, 348–350 (1993).
[Crossref]

1992 (2)

V. C. Smith, B. B. Lee, J. Pokorny, P. R. Martin, and A. Valberg, “Responses of macaque ganglion cells to the relative phase of heterochromatically modulated lights,” J. Physiol. 458, 191–221 (1992).
[Crossref]

H. Komatsu, Y. Ideura, S. Kaji, and S. Yamane, “Color selectivity of neurons in the inferior temporal cortex of the awake macaque monkey,” J. Neurosci. 12, 408–424 (1992).

1990 (1)

P. Lennie, J. Krauskopf, and G. Sclar, “Chromatic mechanisms in striate cortex of macaque,” J. Neurosci. 10, 649–669 (1990).

1989 (1)

J. D. Mollon, ““Tho she kneel’d in the place where they grew.” The uses and origins of primate colour vision,” J. Exp. Biol. 146, 21–38 (1989).

1988 (1)

D. Y. Ts’o and C. D. Gilbert, “The organization of chromatic and spatial interactions in the primate striate cortex,” J. Neurosci. 8, 1712–1727 (1988).

1987 (3)

B. B. Lee, A. Valberg, D. A. Tigwell, and J. Tryti, “An account of responses of spectrally opponent neurons in macaque lateral geniculate nucleus to successive contrast,” Proc. R. Soc. London B 230, 293–314 (1987).

J. M. Crook, B. B. Lee, D. A. Tigwell, and A. Valberg, “Thresholds to chromatic spots of cells in the macaque geniculate nucleus as compared to detection sensitivity in man,” J. Physiol. 392, 193–211 (1987).
[Crossref]

W. H. Swanson, J. Pokorny, and V. C. Smith, “Effects of temporal frequency on phase-dependent sensitivity to heterochromatic flicker,” J. Opt. Soc. Am. A 4, 2266–2273 (1987).
[Crossref]

1986 (1)

J. Krauskopf, D. R. Williams, M. B. Mandler, and A. M. Brown, “Higher order color mechanisms,” Vis. Res. 26, 23–32 (1986).
[Crossref]

1985 (1)

I. Ohzawa, G. Sclar, and R. D. Freeman, “Contrast gain control in the cat’s visual system,” J. Neurophysiol. 54, 651–667 (1985).

1984 (2)

A. M. Derrington, J. Krauskopf, and P. Lennie, “Chromatic mechanisms in lateral geniculate nucleus of macaque,” J. Physiol. 357, 241–265 (1984).
[Crossref]

M. S. Livingstone and D. H. Hubel, “Anatomy and physiology of a color system in the primate visual cortex,” J. Neurosci. 4, 309–356 (1984).

1982 (1)

J. Krauskopf, D. R. Williams, and D. W. Heeley, “Cardinal directions of color space,” Vis. Res. 22, 1123–1131 (1982).
[Crossref]

1981 (1)

E. Zrenner and P. Gouras, “Characteristics of the blue sensitive cone mechanism in primate retinal ganglion cells,” Vis. Res. 21, 1605–1609 (1981).
[Crossref]

1980 (1)

S. Zeki, “The representation of colours in the cerebral cortex,” Nature 284, 412–418 (1980).
[Crossref]

1976 (1)

B. Dreher, Y. Fukada, and R. W. Rodieck, “Identification, classification and anatomical segregation of cells with X-like and Y-like properties in the lateral geniculate nucleus of old-world primates,” J. Physiol. 258, 433–452 (1976).
[Crossref]

1975 (2)

J. Larimer, D. H. Krantz, and C. M. Cicerone, “Opponent process additivity, II: yellow/blue equilibria and nonlinear models,” Vis. Res. 15, 723–731 (1975).
[Crossref]

V. C. Smith and J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500  nm,” Vis. Res. 15, 161–171 (1975).
[Crossref]

1966 (2)

R. L. DeValois, I. Abramov, and G. H. Jacobs, “Analysis of response patterns of LGN cells,” J. Opt. Soc. Am. 56, 966–977 (1966).
[Crossref]

T. N. Wiesel and D. Hubel, “Spatial and chromatic interactions in the lateral geniculate body of the rhesus monkey,” J. Neurophysiol. 29, 1115–1156 (1966).

1955 (1)

1802 (1)

T. Young, “The Bakerian lecture: on the theory of light and colours,” Philos. Trans. R. Soc. London 92, 12–48 (1802).
[Crossref]

Abramov, I.

Albright, T. D.

G. D. Horwitz, E. J. Chichilnisky, and T. D. Albright, “Blue-yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1,” J. Neurophysiol. 93, 2263–2278 (2005).
[Crossref]

Alonso, J. M.

L. E. Wool, S. J. Komban, J. Kremkow, M. Jansen, X. Li, J. M. Alonso, and Q. Zaidi, “Salience of unique hues and implications for color theory,” J. Vis. 15(2), 10 (2015).
[Crossref]

Ault, S. J.

A. G. Leventhal, K. G. Thompson, D. Liu, Y. Zhou, and S. J. Ault, “Concomitant sensitivity to orientation, direction, and color of cells in layers 2, 3, and 4 of monkey striate cortex,” J. Neurosci. 15, 1808–1818 (1995).

Bakolitsa, C.

M. Greschner, J. Shlens, C. Bakolitsa, G. D. Field, J. L. Gauthier, L. H. Jepson, A. Sher, A. M. Litke, and E. J. Chichilnisky, “Correlated firing among major ganglion cell types in primate retina,” J. Physiol. 589, 75–86 (2011).
[Crossref]

Bonds, A. B.

R. C. Kelly, M. A. Smith, J. M. Samonds, A. Kohn, A. B. Bonds, J. A. Movshon, and T. S. Lee, “Comparison of recordings from microelectrode arrays and single electrodes in the visual cortex,” J. Neurosci. 27, 261–264 (2007).
[Crossref]

Brown, A. M.

J. Krauskopf, D. R. Williams, M. B. Mandler, and A. M. Brown, “Higher order color mechanisms,” Vis. Res. 26, 23–32 (1986).
[Crossref]

Chaparro, A.

A. Chaparro, C. F. Stromeyer, E. P. Huang, R. E. Kronauer, and R. T. Eskew, “Colour is what the eye sees best,” Nature 361, 348–350 (1993).
[Crossref]

Chichilnisky, E. J.

M. Greschner, J. Shlens, C. Bakolitsa, G. D. Field, J. L. Gauthier, L. H. Jepson, A. Sher, A. M. Litke, and E. J. Chichilnisky, “Correlated firing among major ganglion cell types in primate retina,” J. Physiol. 589, 75–86 (2011).
[Crossref]

G. D. Horwitz, E. J. Chichilnisky, and T. D. Albright, “Blue-yellow signals are enhanced by spatiotemporal luminance contrast in macaque V1,” J. Neurophysiol. 93, 2263–2278 (2005).
[Crossref]

Cicerone, C. M.

J. Larimer, D. H. Krantz, and C. M. Cicerone, “Opponent process additivity, II: yellow/blue equilibria and nonlinear models,” Vis. Res. 15, 723–731 (1975).
[Crossref]

Conway, B. R.

C. M. Stoughton and B. R. Conway, “Neural basis for unique hues,” Curr. Biol. 18, R698–R699 (2008).
[Crossref]

B. R. Conway, S. Moeller, and D. Y. Tsao, “Specialized color modules in macaque extrastriate cortex,” Neuron 56, 560–573 (2007).
[Crossref]

B. R. Conway, D. H. Hubel, and M. S. Livingstone, “Color contrast in macaque V1,” Cereb. Cortex 12, 915–925 (2002).
[Crossref]

B. R. Conway, “Spatial structure of cone inputs to color cells in alert macaque primary visual cortex (V-1),” J. Neurosci. 21, 2768–2783 (2001).

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R. Shapley and M. J. Hawken, “Color in the cortex: single- and double-opponent cells,” Vis. Res. 51, 701–717 (2011).
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D. L. Ringach, G. Sapiro, and R. Shapley, “A subspace reverse-correlation technique for the study of visual neurons,” Vis. Res. 37, 2455–2464 (1997).
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S. K. Shevell and F. A. Kingdom, “Color in complex scenes,” Ann. Rev. Psychol. 59, 143–166 (2008).
[Crossref]

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[Crossref]

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C. Tailby, S. G. Solomon, and P. Lennie, “Habituation reveals fundamental chromatic mechanisms in striate cortex of macaque,” J. Neurosci. 28, 1131–1139 (2008).
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Other (13)

Because we know the physical (radiometric) properties of the [RGB] monitor beams as well as the biological (photometric) properties of the human [LMS] cone receptors, we can predict what effect any RGB level within the gamut will have on the LMS receptors. Even better (and thinking the other way around), we can decide what LMS activation level we want, and set the RGB levels accordingly.

The 180° direction is the same as the zero direction, of course, but the modulation begins at the other side of the circle. If you look closely you can see that the histogram peaks are displaced (that is, shifted in time) by about 180° for the opposite modulation direction.

In the proper historical context, Eq. (1) is a “hypothetical neural mechanism” of the sort disparaged by Helmholtz because it preceded the discovery of primate color-opponent neurons or even knowledge of the now-well-accepted L-, M-, and S-cone spectral sensitivity functions.

Importantly, pure color changes from white are made while keeping the overall light level constant; that is, all color changes occur at constant luminance. This guarantees the threshold is mediated by a chromatic neural response.

J. Kremers, ed., The Primate Visual System: A Comparative Approach (Wiley, 2005).

E. Hering, “Grundzüge einer Theorie des Farbensinnes (originally published in 1874),” in Zur Lehre vom Lichtsinn (Gerald u. Söhne, 1878), pp. 107–141.

J. D. Mollon, “The origins of modern color science,” in The Science of Color, S. K. Shevell, ed. (Optical Society of America/Elsevier, 2003), pp. 1–39.

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In 1924 the Optical Society of America published an English translation of the third German edition, edited by James Southall.

R. S. Turner, In the Eye’s Mind (Princeton University, 1994).

The solid symbols in Fig. 2(d) are scaled by a factor that equates the units of the 500 and 700 nm lights. The factor is determined by the ratio of 500 to 700 nm light that in mixture appears neither reddish nor greenish.

Open symbols in Fig. 2(d) are scaled by a factor that equates the units of the 475 and 580 nm lights. The factor is determined by the ratio of 475 to 580 nm light that in mixture appears neither yellowish nor bluish. A second scaling factor adjusts the overall height of the red–green curve (solid symbols) relative to the height of the yellow–blue curve (open symbols). This scaling is based on wavelengths perceived to have two hues of equal magnitude (for example, a wavelength that appears an orange judged to have equal parts redness and yellowness).

J. D. Mollon and G. Jordan, “On the nature of unique hues,” in John Dalton’s Colour Vision Legacy, C. M. Dickinson, I. J. Murray, and D. Carden, eds. (Taylor & Francis, 1997), pp. 381–392.

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Figures (5)

Fig. 1.
Fig. 1.

Color opponent axes. Hering declared red and green to be opponent colors represented along a single axis. Here, positive values on the axis are reddish, negative values are greenish, and zero represents a hue that has no redness or greenness at all—that is, unique blue, unique yellow, or white. Hering also proposed a second axis running from yellow (positive) to blue (negative), with zero for hues that have no yellowness or blueness (so unique red, unique green, or white). Any hue can be represented by two coordinate values, one on each axis. Orange, for example, has a positive value on both axes; aqua, composed of both greenness and blueness, has a negative value on both axes. White has zero on both axes (no trace of redness, greenness, yellowness, or blueness).

Fig. 2.
Fig. 2.

How to use color mixtures to characterize opponent-color mechanisms. (a) Hues that do not lie on the opponent axes have both red–green and blue–yellow components. In this case, orange has red and yellow components. By adding 500 nm (“green”) to the orange hue its reddish component can be canceled (i.e., bringing the mixture light to the R–G equilibrium locus). (b) Mixing spectral lights. The observer views a mixture of 630 nm plus a greenish-appearing wavelength (here, 500 nm), and adjusts the level of the 500 nm light until the mixture appears neither reddish nor greenish. (c) A representation of the Jameson and Hurvich color cancellation experiment in CIE space. Repeating the chromatic cancellation for wavelengths above 578 nm quantifies the redness in each of these wavelengths. (d) The resulting measurements can be plotted together as a function of all the physical wavelengths in the visible spectrum (see text).

Fig. 3.
Fig. 3.

Physiological measurement of opponency. (a) Opponency defined by nerve cell recording. The visual system of an anaesthetized monkey responds to brief pulses of light presented on a stimulus screen. The small electrical signals (action potentials) from these cells are picked up by an electrode and amplified. (b) These famous recordings by De Valois and colleagues show responses of single nerve cells in monkey visual system to lights at different wavelengths. Here the opponent process is revealed as the cell is excited by some wavelengths (in this case, long wavelengths) and inhibited by others (that is, the spike rate falls below the maintained rate). Measurements were taken at three steps of brightness attenuation, showing that the opponent characteristic does not depend heavily on brightness. (c) Other cells show blue–yellow opponent property. (d) Opponency can also be measured by responses to a mixture of wavelengths projected into the eye. The frequency of action potentials is measured as a function of time relative to the stimulus modulation. If the response to in-phase modulation (0 deg phase difference, left column) is less than the response to out-of-phase modulation (180 deg phase difference, right column), we know that something in the retina has “subtracted” the neural response to 554 nm (“green”) light from the response to 639 nm (“red”) light (upper histograms). The process can be studied in detail by changing the frequency and phase of light modulation (lower histograms). Panels (b) and (c) modified from [12]. Panel (d) modified from Solomon et al. (2005) [13].

Fig. 4.
Fig. 4.

Cone opponency defined physiologically by chromatic cardinal axes in experiments by Derrington and colleagues. (a) Projection of the stimulus set onto the CIE axes. Broken lines show the range of colors that lie within the monitor gamut. (b) Enlarged view of part of this space. Thick solid lines show two cardinal exchange axes producing selective modulation of S cones and out-of-phase modulation of M and L cones at constant luminance. Intermediate modulation directions form an ellipse in this space. (c) Here the space is reformed into a circle with cone excitation azimuth. Gray profiles show response modulation of a single nerve cell along different color modulation directions (four cycles of modulation are shown). Note that the cell is modulated maximally by exchange along the L–M axis (0–180 deg), and shows no modulation (response “null”) along the S-cone axis (90 to -90 deg). (d) A third axis (elevation) is defined by in-phase modulation of S, M, and L cones. (e) Two clusters of cells are present in monkey lateral geniculate nucleus (LGN) with preferred azimuth close to zero (L–M) or 90 (S) deg. The L–M cells prefer a combination of luminance and color exchange (elevations around 45 deg), whereas the S cells prefer near-equiluminant color exchange. (f) Unique hues (outer circle) do not align with the cardinal color axes. The points show unique hue settings made on the circumference of an S versus ML cone space circle by seven observers. Note that the settings do not align with the L–M or S axis. Note also the differences in unique hue position among observers, with little variation in unique yellow but wide variation in position of unique blue, red, and green. Data in panels (c) and (e) redrawn from [40]. Data in panel (f) redrawn from [35].

Fig. 5.
Fig. 5.

Spatial and chromatic opponent receptive fields. (a) Schematic spatial sensitivity profile of a single-opponent receptive field receiving excitatory input (L+) from long-wave sensitive cones, and inhibitory input (M−) from middle-wave sensitive cones. (b) The receptive field projection of a single-opponent field shows approximately overlapping and circularly symmetric cone-opponent inputs. (c) Schematic spatial sensitivity profile of a double-opponent receptive field. Here the receptive field comprises two opponent sub-regions which are spatially offset. (d) The receptive field projection of a double-opponent field shows complementary, orientation-selective sub-regions which produce both spatial and chromatic selectivity. Modified from [53].

Equations (2)

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(rg)λ=aLλbMλ+cSλ.
(yb)λ=dLλ+eMλfSλ,