Abstract

De Valois and De Valois [Vis. Res. 33, 1053 (1993)] showed that to explain hue appearance, S-cone signals have to be combined with M versus L opponent signals in two different ways to produce red–green and yellow–blue axes, respectively. Recently, it has been shown that color appearance is normal for individuals with genetic mutations that block S-cone input to blue-ON ganglion cells. This is inconsistent with the De Valois hypothesis in which S-opponent konio-geniculate signals are combined with L-M signals at a third processing stage in cortex. Instead, here we show that color appearance, including individual differences never explained before, are predicted by a model in which S-cone signals are combined with L versus M signals in the outer retina.

© 2014 Optical Society of America

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2014 (1)

2013 (1)

M. M. C. Bijveld, M. M. van Genderen, F. P. Hoeben, A. A. Katzin, R. M. A. van Nispen, F. C. C. Riemslag, and A. M. L. Kappers, “Assessment of night vision problems in patients with congenital stationary night blindness,” PloS One 8, e62927 (2013).

2012 (5)

V. J. Volbrecht and J. L. Nerger, “Color appearance at 10 along the vertical and horizontal meridians,” J. Opt. Soc. Am. A 29, A44–A51 (2012).
[CrossRef]

S. F. O’Neil, K. C. McDermott, Y. Mizokami, J. S. Werner, M. A. Crognale, and M. A. Webster, “Tests of a functional account of the Abney effect,” J. Opt. Soc. Am. A 29, A165–A173 (2012).
[CrossRef]

M. V. Danilova and J. D. Mollon, “Foveal color perception: minimal thresholds at a boundary between perceptual categories,” Vis. Res. 62, 162–172 (2012).
[CrossRef]

S. Chen and W. Li, “A color-coding amacrine cell may provide a blue-off signal in a mammalian retina,” Nat. Neurosci. 15, 954–956 (2012).
[CrossRef]

A. Sher and S. H. DeVries, “A non-canonical pathway for mammalian blue-green color vision,” Nat. Neurosci. 15, 952–953 (2012).
[CrossRef]

2011 (2)

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
[CrossRef]

J. Neitz and M. Neitz, “The genetics of normal and defective color vision,” Vis. Res. 51, 633–651 (2011).
[CrossRef]

2010 (2)

O. S. Packer, J. Verweij, P. H. Li, J. L. Schnapf, and D. M. Dacey, “Blue-yellow opponency in primate S cone photoreceptors,” J. Neurosci. 30, 568–572 (2010).
[CrossRef]

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
[CrossRef]

2009 (1)

K. Mancuso, W. W. Hauswirth, Q. Li, T. B. Connor, J. A. Kuchenbecker, M. C. Mauck, J. Neitz, and M. Neitz, “Gene therapy for red-green colour blindness in adult primates,” Nature 461, 784–787 (2009).
[CrossRef]

2008 (2)

J. Neitz and M. Neitz, “Colour vision: the wonder of hue,” Curr. Biol. 18, R700–R702 (2008).
[CrossRef]

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]

2006 (5)

J. Duebel, S. Haverkamp, W. Schleich, G. Feng, G. J. Augustine, T. Kuner, and T. Euler, “Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon,” Neuron 49, 81–94 (2006).
[CrossRef]

H. Sun, H. E. Smithson, Q. Zaidi, and B. B. Lee, “Specificity of cone inputs to macaque retinal ganglion cells,” J. Neurophysiol. 95, 837–849 (2006).
[CrossRef]

E. O’Connor, L. E. Allen, K. Bradshaw, J. Boylan, A. T. Moore, and D. Trump, “Congenital stationary night blindness associated with mutations in GRM6 encoding glutamate receptor MGluR6,” Br. J. Ophthalmol. 90, 653–654 (2006).
[CrossRef]

B. R. Conway and M. S. Livingstone, “Spatial and temporal properties of cone signals in alert macaque primary visual cortex,” J. Neurosci. 26, 10826–10846 (2006).
[CrossRef]

D. L. Philipona and J. K. O. Regan, “Color naming, unique hues, and hue cancellation predicted from singularities in reflection properties,” Vis. Neurosci. 23, 331–339 (2006).
[CrossRef]

2005 (5)

D. M. Dacey, H.-W. Liao, B. B. Peterson, F. R. Robinson, V. C. Smith, J. Pokorny, K.-W. Yau, and P. D. Gamlin, “Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN,” Nature 433, 749–754 (2005).
[CrossRef]

H. Hofer, J. Carroll, J. Neitz, M. Neitz, and D. R. Williams, “Organization of the human trichromatic cone mosaic,” J. Neurosci. 25, 9669–9679 (2005).
[CrossRef]

I. Abramov and J. Gordon, “Seeing unique hues,” J. Opt. Soc. Am. A 22, 2143–2153 (2005).
[CrossRef]

T. P. Dryja, T. L. Mcgee, E. L. Berson, G. A. Fishman, M. A. Sandberg, K. R. Alexander, D. J. Derlacki, and A. S. Rajagopalan, “Night blindness and abnormal cone electroretinogram ON responses in patients with mutations in the GRM6 gene encoding mGluR6,” Proc. Natl. Acad. Sci. USA 102, 4884–4889 (2005).

C. Varela, R. Blanco, and P. De la Villa, “Depolarizing effect of GABA in rod bipolar cells of the mouse retina,” Vis. Res. 45, 2659–2667 (2005).
[CrossRef]

2004 (1)

R. G. Kuehni, “Variability in unique hue selection: a surprising phenomenon,” Color Res. Appl. 29, 158–162 (2004).
[CrossRef]

2003 (2)

K. Klug, S. Herr, I. T. Ngo, P. Sterling, and S. Schein, “Macaque retina contains an S-cone OFF midget pathway,” J. Neurosci. 23, 9881–9887 (2003).

D. M. Dacey and O. S. Packer, “Colour coding in the primate retina: diverse cell types and cone-specific circuitry,” Curr. Opin. Neurobiol. 13, 421–427 (2003).
[CrossRef]

2002 (3)

D. M. Dacey, B. B. Peterson, and F. R. Robinson, “Identification of an S-cone opponent OFF pathway in the Macaque monkey retina: morphology, physiology and possible circuitry,” Investig. Ophthalmol. Vis. Sci. 43, E–abstract 2983 (2002).

J. Carroll, J. Neitz, and M. Neitz, “Estimates of L∶M cone ratio from ERG flicker photometry and genetics,” J. Vis. 2(8):1, 531–542 (2002).
[CrossRef]

J. Neitz, J. Carroll, Y. Yamauchi, M. Neitz, and D. R. Williams, “Color perception is mediated by a plastic neural mechanism that is adjustable in adults,” Neuron 35, 783–792 (2002).
[CrossRef]

2001 (3)

R. G. Kuehni, “Determination of unique hues using Munsell color chips,” Color Res. Appl. 26, 61–66 (2001).
[CrossRef]

A. Valberg, “Unique hues: an old problem for a new generation,” Vis. Res. 41, 1645–1657 (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 (5)

N. Vardi, R. Duvoisin, G. Wu, and P. Sterling, “Localization of mGluR6 to dendrites of ON bipolar cells in primate retina,” J. Comp. Neurol. 423, 402–412 (2000).
[CrossRef]

D. Dacey, O. S. Packer, L. Diller, D. Brainard, B. Peterson, and B. Lee, “Center surround receptive field structure of cone bipolar cells in primate retina,” Vis. Res. 40, 1801–1811 (2000).
[CrossRef]

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]

J. Carroll, C. McMahon, M. Neitz, and J. Neitz, “Flicker-photometric electroretinogram estimates of L∶M cone photoreceptor ratio in men with photopigment spectra derived from genetics,” J. Opt. Soc. Am. A 17, 499–509 (2000).
[CrossRef]

M. A. Webster, E. Miyahara, G. Malkoc, and V. E. Raker, “Variations in normal color vision. I. Cone-opponent axes,” J. Opt. Soc. Am. A 17, 1535–1544 (2000).
[CrossRef]

1999 (4)

A. Roorda and D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397, 520–522 (1999).
[CrossRef]

B. Boycott and H. Wassle, “Parallel processing in the mammalian retina: the Proctor lecture,” Investig. Ophthalmol. Vis. Sci. 40, 1313–1327 (1999).

J. Neitz, M. Neitz, J. C. He, and S. K. Shevell, “Trichromatic color vision with only two spectrally distinct photopigments,” Nat. Neurosci. 2, 884–888 (1999).
[CrossRef]

H. Terasaki, Y. Miyake, R. Nomura, M. Horiguchi, S. Suzuki, and M. Kondo, “Blue-on-yellow perimetry in the complete type of congenital stationary night blindness,” Investig. Ophthalmol. Vis. Sci. 40, 2761–2764 (1999).

1997 (1)

V. J. Volbrecht, J. L. Nerger, and C. E. Harlow, “The bimodality of unique green revisited,” Vis. Res. 37, 407–416 (1997).
[CrossRef]

1996 (1)

D. M. Dacey, B. B. Lee, D. K. Stafford, J. Pokorny, and V. C. Smith, “Horizontal cells of the primate retina: cone specificity without spectral opponency,” Science 271, 656–659 (1996).
[CrossRef]

1995 (2)

1993 (2)

1991 (3)

1989 (1)

1988 (1)

A. C. Aho, K. Donner, C. Hyden, L. O. Larsen, and T. Reuter, “Low retinal noise in animals with low body temperature allows high visual sensitivity,” Nature 334, 348–350 (1988).
[CrossRef]

1987 (2)

1986 (1)

J. Nathans, D. Thomas, and D. S. Hogness, “Molecular genetics of human color vision: the genes encoding blue, green, and red pigments,” Science 232, 193–202 (1986).
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1984 (2)

A. P. Mariani, “Bipolar cells in monkey retina selective for the cones likely to be blue-sensitive,” Nature 308, 184–186 (1984).
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A. M. Derrington, J. Krauskopf, and P. Lennie, “Chromatic mechanisms in lateral geniculate nucleus of macaque,” J. Physiol. 357, 241–265 (1984).

1983 (1)

W. Paulus and A. Kröger-Paulus, “A new concept of retinal colour coding,” Vis. Res. 23, 529–540 (1983).
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1982 (1)

J. Krauskopf, D. R. Williams, and D. W. Heeley, “Cardinal directions of color space,” Vis. Res. 22, 1123–1131 (1982).
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1979 (1)

F. M. de Monasterio, “Signals from blue cones in “red-green” opponent-colour ganglion cells of the macaque retina,” Vis. Res. 19, 441–449 (1979).
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1977 (2)

F. M. de Monasterio and P. Gouras, “Responses of macaque ganglion cells to far violet lights,” Vis. Res. 17, 1147–1156 (1977).
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J. Gordon and I. Abramov, “Color vision in the peripheral retina. II. Hue and saturation,” J. Opt. Soc. Am. 67, 202–207 (1977).
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1975 (1)

F. M. de Monasterio, P. Gouras, and D. J. Tolhurst, “Trichromatic colour opponency in ganglion cells of the rhesus monkey,” J. Physiol. 251, 197–216 (1975).

1966 (3)

J. E. Dowling and B. B. Boycott, “Organization of the primate retina: electron microscopy,” Proc. R. Soc. B 166, 80–111 (1966).
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D. B. Judd, “Fundamental studies of color vision from 1860 to 1960,” Proc. Natl. Acad. Sci. USA 55, 1313–1330 (1966).

R. L. De Valois, I. Abramov, and G. H. Jacobs, “Analysis of response patterns of LGN cells,” J. Opt. Soc. Am. 56, 966–977 (1966).
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1957 (1)

L. M. Hurvich and D. Jameson, “An opponent-process theory of color vision,” Psycholog. Rev. 64, 384–404 (1957).
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1909 (1)

W. Abney, “On the change in hue of spectrum colours by dilution with white light,” Proc. R. Soc. London 83, 120–127 (1909).
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Abney, W.

W. Abney, “On the change in hue of spectrum colours by dilution with white light,” Proc. R. Soc. London 83, 120–127 (1909).
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Abramov, I.

Aho, A. C.

A. C. Aho, K. Donner, C. Hyden, L. O. Larsen, and T. Reuter, “Low retinal noise in animals with low body temperature allows high visual sensitivity,” Nature 334, 348–350 (1988).
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Alexander, K. R.

T. P. Dryja, T. L. Mcgee, E. L. Berson, G. A. Fishman, M. A. Sandberg, K. R. Alexander, D. J. Derlacki, and A. S. Rajagopalan, “Night blindness and abnormal cone electroretinogram ON responses in patients with mutations in the GRM6 gene encoding mGluR6,” Proc. Natl. Acad. Sci. USA 102, 4884–4889 (2005).

Allen, L. E.

E. O’Connor, L. E. Allen, K. Bradshaw, J. Boylan, A. T. Moore, and D. Trump, “Congenital stationary night blindness associated with mutations in GRM6 encoding glutamate receptor MGluR6,” Br. J. Ophthalmol. 90, 653–654 (2006).
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Augustine, G. J.

J. Duebel, S. Haverkamp, W. Schleich, G. Feng, G. J. Augustine, T. Kuner, and T. Euler, “Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon,” Neuron 49, 81–94 (2006).
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Ayama, M.

Ayde, C. J.

Berson, E. L.

T. P. Dryja, T. L. Mcgee, E. L. Berson, G. A. Fishman, M. A. Sandberg, K. R. Alexander, D. J. Derlacki, and A. S. Rajagopalan, “Night blindness and abnormal cone electroretinogram ON responses in patients with mutations in the GRM6 gene encoding mGluR6,” Proc. Natl. Acad. Sci. USA 102, 4884–4889 (2005).

Bijveld, M. M. C.

M. M. C. Bijveld, M. M. van Genderen, F. P. Hoeben, A. A. Katzin, R. M. A. van Nispen, F. C. C. Riemslag, and A. M. L. Kappers, “Assessment of night vision problems in patients with congenital stationary night blindness,” PloS One 8, e62927 (2013).

Blanco, R.

C. Varela, R. Blanco, and P. De la Villa, “Depolarizing effect of GABA in rod bipolar cells of the mouse retina,” Vis. Res. 45, 2659–2667 (2005).
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Boycott, B.

B. Boycott and H. Wassle, “Parallel processing in the mammalian retina: the Proctor lecture,” Investig. Ophthalmol. Vis. Sci. 40, 1313–1327 (1999).

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J. E. Dowling and B. B. Boycott, “Organization of the primate retina: electron microscopy,” Proc. R. Soc. B 166, 80–111 (1966).
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Boylan, J.

E. O’Connor, L. E. Allen, K. Bradshaw, J. Boylan, A. T. Moore, and D. Trump, “Congenital stationary night blindness associated with mutations in GRM6 encoding glutamate receptor MGluR6,” Br. J. Ophthalmol. 90, 653–654 (2006).
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Bradshaw, K.

E. O’Connor, L. E. Allen, K. Bradshaw, J. Boylan, A. T. Moore, and D. Trump, “Congenital stationary night blindness associated with mutations in GRM6 encoding glutamate receptor MGluR6,” Br. J. Ophthalmol. 90, 653–654 (2006).
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Brainard, D.

D. Dacey, O. S. Packer, L. Diller, D. Brainard, B. Peterson, and B. Lee, “Center surround receptive field structure of cone bipolar cells in primate retina,” Vis. Res. 40, 1801–1811 (2000).
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D. H. Brainard and A. Stockman, “Colorimetry,” in Vision and Vision Optics, M. Bass, ed., 3rd ed. (McGraw-Hill, 2009), Chap. 10, pp. 1–56.

A. Stockman and D. H. Brainard, “Color vision mechanisms,” in Vision and Vision Optics, M. Bass, ed., 3rd ed. (McGraw-Hill, 2009), Chap. 11, pp. 1–104.

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H. Hofer, J. Carroll, J. Neitz, M. Neitz, and D. R. Williams, “Organization of the human trichromatic cone mosaic,” J. Neurosci. 25, 9669–9679 (2005).
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J. Neitz, J. Carroll, Y. Yamauchi, M. Neitz, and D. R. Williams, “Color perception is mediated by a plastic neural mechanism that is adjustable in adults,” Neuron 35, 783–792 (2002).
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S. Chen and W. Li, “A color-coding amacrine cell may provide a blue-off signal in a mammalian retina,” Nat. Neurosci. 15, 954–956 (2012).
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G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
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K. Mancuso, W. W. Hauswirth, Q. Li, T. B. Connor, J. A. Kuchenbecker, M. C. Mauck, J. Neitz, and M. Neitz, “Gene therapy for red-green colour blindness in adult primates,” Nature 461, 784–787 (2009).
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G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
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Dacey, D.

D. Dacey, O. S. Packer, L. Diller, D. Brainard, B. Peterson, and B. Lee, “Center surround receptive field structure of cone bipolar cells in primate retina,” Vis. Res. 40, 1801–1811 (2000).
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Dacey, D. M.

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
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O. S. Packer, J. Verweij, P. H. Li, J. L. Schnapf, and D. M. Dacey, “Blue-yellow opponency in primate S cone photoreceptors,” J. Neurosci. 30, 568–572 (2010).
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D. M. Dacey, H.-W. Liao, B. B. Peterson, F. R. Robinson, V. C. Smith, J. Pokorny, K.-W. Yau, and P. D. Gamlin, “Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN,” Nature 433, 749–754 (2005).
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D. M. Dacey and O. S. Packer, “Colour coding in the primate retina: diverse cell types and cone-specific circuitry,” Curr. Opin. Neurobiol. 13, 421–427 (2003).
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D. M. Dacey, B. B. Peterson, and F. R. Robinson, “Identification of an S-cone opponent OFF pathway in the Macaque monkey retina: morphology, physiology and possible circuitry,” Investig. Ophthalmol. Vis. Sci. 43, E–abstract 2983 (2002).

D. M. Dacey, B. B. Lee, D. K. Stafford, J. Pokorny, and V. C. Smith, “Horizontal cells of the primate retina: cone specificity without spectral opponency,” Science 271, 656–659 (1996).
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M. V. Danilova and J. D. Mollon, “Foveal color perception: minimal thresholds at a boundary between perceptual categories,” Vis. Res. 62, 162–172 (2012).
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De la Villa, P.

C. Varela, R. Blanco, and P. De la Villa, “Depolarizing effect of GABA in rod bipolar cells of the mouse retina,” Vis. Res. 45, 2659–2667 (2005).
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de Monasterio, F. M.

F. M. de Monasterio, “Signals from blue cones in “red-green” opponent-colour ganglion cells of the macaque retina,” Vis. Res. 19, 441–449 (1979).
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F. M. de Monasterio and P. Gouras, “Responses of macaque ganglion cells to far violet lights,” Vis. Res. 17, 1147–1156 (1977).
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F. M. de Monasterio, P. Gouras, and D. J. Tolhurst, “Trichromatic colour opponency in ganglion cells of the rhesus monkey,” J. Physiol. 251, 197–216 (1975).

De Valois, K.

R. L. De Valois and K. De Valois, “A multi-stage color model,” Vis. Res. 33, 1053–1065 (1993).
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De Valois, R. L.

Derlacki, D. J.

T. P. Dryja, T. L. Mcgee, E. L. Berson, G. A. Fishman, M. A. Sandberg, K. R. Alexander, D. J. Derlacki, and A. S. Rajagopalan, “Night blindness and abnormal cone electroretinogram ON responses in patients with mutations in the GRM6 gene encoding mGluR6,” Proc. Natl. Acad. Sci. USA 102, 4884–4889 (2005).

Derrington, A. M.

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

DeVries, S. H.

A. Sher and S. H. DeVries, “A non-canonical pathway for mammalian blue-green color vision,” Nat. Neurosci. 15, 952–953 (2012).
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Diller, L.

D. Dacey, O. S. Packer, L. Diller, D. Brainard, B. Peterson, and B. Lee, “Center surround receptive field structure of cone bipolar cells in primate retina,” Vis. Res. 40, 1801–1811 (2000).
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Donner, K.

A. C. Aho, K. Donner, C. Hyden, L. O. Larsen, and T. Reuter, “Low retinal noise in animals with low body temperature allows high visual sensitivity,” Nature 334, 348–350 (1988).
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Dowling, J. E.

J. E. Dowling and B. B. Boycott, “Organization of the primate retina: electron microscopy,” Proc. R. Soc. B 166, 80–111 (1966).
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Drum, B.

Dryja, T. P.

T. P. Dryja, T. L. Mcgee, E. L. Berson, G. A. Fishman, M. A. Sandberg, K. R. Alexander, D. J. Derlacki, and A. S. Rajagopalan, “Night blindness and abnormal cone electroretinogram ON responses in patients with mutations in the GRM6 gene encoding mGluR6,” Proc. Natl. Acad. Sci. USA 102, 4884–4889 (2005).

Duebel, J.

J. Duebel, S. Haverkamp, W. Schleich, G. Feng, G. J. Augustine, T. Kuner, and T. Euler, “Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon,” Neuron 49, 81–94 (2006).
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N. Vardi, R. Duvoisin, G. Wu, and P. Sterling, “Localization of mGluR6 to dendrites of ON bipolar cells in primate retina,” J. Comp. Neurol. 423, 402–412 (2000).
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Euler, T.

J. Duebel, S. Haverkamp, W. Schleich, G. Feng, G. J. Augustine, T. Kuner, and T. Euler, “Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon,” Neuron 49, 81–94 (2006).
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Feng, G.

J. Duebel, S. Haverkamp, W. Schleich, G. Feng, G. J. Augustine, T. Kuner, and T. Euler, “Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon,” Neuron 49, 81–94 (2006).
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G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
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Fishman, G. A.

T. P. Dryja, T. L. Mcgee, E. L. Berson, G. A. Fishman, M. A. Sandberg, K. R. Alexander, D. J. Derlacki, and A. S. Rajagopalan, “Night blindness and abnormal cone electroretinogram ON responses in patients with mutations in the GRM6 gene encoding mGluR6,” Proc. Natl. Acad. Sci. USA 102, 4884–4889 (2005).

Gamlin, P. D.

D. M. Dacey, H.-W. Liao, B. B. Peterson, F. R. Robinson, V. C. Smith, J. Pokorny, K.-W. Yau, and P. D. Gamlin, “Melanopsin-expressing ganglion cells in primate retina signal colour and irradiance and project to the LGN,” Nature 433, 749–754 (2005).
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Gauthier, J. L.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
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Gouras, P.

F. M. de Monasterio and P. Gouras, “Responses of macaque ganglion cells to far violet lights,” Vis. Res. 17, 1147–1156 (1977).
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F. M. de Monasterio, P. Gouras, and D. J. Tolhurst, “Trichromatic colour opponency in ganglion cells of the rhesus monkey,” J. Physiol. 251, 197–216 (1975).

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G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
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G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
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H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
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Hauswirth, W. W.

K. Mancuso, W. W. Hauswirth, Q. Li, T. B. Connor, J. A. Kuchenbecker, M. C. Mauck, J. Neitz, and M. Neitz, “Gene therapy for red-green colour blindness in adult primates,” Nature 461, 784–787 (2009).
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Haverkamp, S.

J. Duebel, S. Haverkamp, W. Schleich, G. Feng, G. J. Augustine, T. Kuner, and T. Euler, “Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon,” Neuron 49, 81–94 (2006).
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Hoeben, F. P.

M. M. C. Bijveld, M. M. van Genderen, F. P. Hoeben, A. A. Katzin, R. M. A. van Nispen, F. C. C. Riemslag, and A. M. L. Kappers, “Assessment of night vision problems in patients with congenital stationary night blindness,” PloS One 8, e62927 (2013).

Hofer, H.

H. Hofer, J. Carroll, J. Neitz, M. Neitz, and D. R. Williams, “Organization of the human trichromatic cone mosaic,” J. Neurosci. 25, 9669–9679 (2005).
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J. Nathans, D. Thomas, and D. S. Hogness, “Molecular genetics of human color vision: the genes encoding blue, green, and red pigments,” Science 232, 193–202 (1986).
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Horiguchi, M.

H. Terasaki, Y. Miyake, R. Nomura, M. Horiguchi, S. Suzuki, and M. Kondo, “Blue-on-yellow perimetry in the complete type of congenital stationary night blindness,” Investig. Ophthalmol. Vis. Sci. 40, 2761–2764 (1999).

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L. M. Hurvich and D. Jameson, “An opponent-process theory of color vision,” Psycholog. Rev. 64, 384–404 (1957).
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A. C. Aho, K. Donner, C. Hyden, L. O. Larsen, and T. Reuter, “Low retinal noise in animals with low body temperature allows high visual sensitivity,” Nature 334, 348–350 (1988).
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Jacobs, G. H.

M. Neitz, J. Neitz, and G. H. Jacobs, “Spectral tuning of pigments underlying red-green color vision,” Nature 252, 971–974 (1991).

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Jameson, D.

L. M. Hurvich and D. Jameson, “An opponent-process theory of color vision,” Psycholog. Rev. 64, 384–404 (1957).
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Jepson, L. H.

G. D. Field, J. L. Gauthier, A. Sher, M. Greschner, T. A. Machado, L. H. Jepson, J. Shlens, D. E. Gunning, K. Mathieson, W. Dabrowski, L. Paninski, A. M. Litke, and E. J. Chichilnisky, “Functional connectivity in the retina at the resolution of photoreceptors,” Nature 467, 673–677 (2010).
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Joo, H. R.

H. R. Joo, B. B. Peterson, T. J. Haun, and D. M. Dacey, “Characterization of a novel large-field cone bipolar cell type in the primate retina: evidence for selective cone connections,” Vis. Neurosci. 28, 29–37 (2011).
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D. B. Judd, “Fundamental studies of color vision from 1860 to 1960,” Proc. Natl. Acad. Sci. USA 55, 1313–1330 (1966).

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Kappers, A. M. L.

M. M. C. Bijveld, M. M. van Genderen, F. P. Hoeben, A. A. Katzin, R. M. A. van Nispen, F. C. C. Riemslag, and A. M. L. Kappers, “Assessment of night vision problems in patients with congenital stationary night blindness,” PloS One 8, e62927 (2013).

Katzin, A. A.

M. M. C. Bijveld, M. M. van Genderen, F. P. Hoeben, A. A. Katzin, R. M. A. van Nispen, F. C. C. Riemslag, and A. M. L. Kappers, “Assessment of night vision problems in patients with congenital stationary night blindness,” PloS One 8, e62927 (2013).

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K. Klug, S. Herr, I. T. Ngo, P. Sterling, and S. Schein, “Macaque retina contains an S-cone OFF midget pathway,” J. Neurosci. 23, 9881–9887 (2003).

Kondo, M.

H. Terasaki, Y. Miyake, R. Nomura, M. Horiguchi, S. Suzuki, and M. Kondo, “Blue-on-yellow perimetry in the complete type of congenital stationary night blindness,” Investig. Ophthalmol. Vis. Sci. 40, 2761–2764 (1999).

Krauskopf, J.

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

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W. Paulus and A. Kröger-Paulus, “A new concept of retinal colour coding,” Vis. Res. 23, 529–540 (1983).
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K. Mancuso, W. W. Hauswirth, Q. Li, T. B. Connor, J. A. Kuchenbecker, M. C. Mauck, J. Neitz, and M. Neitz, “Gene therapy for red-green colour blindness in adult primates,” Nature 461, 784–787 (2009).
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J. Duebel, S. Haverkamp, W. Schleich, G. Feng, G. J. Augustine, T. Kuner, and T. Euler, “Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon,” Neuron 49, 81–94 (2006).
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A. C. Aho, K. Donner, C. Hyden, L. O. Larsen, and T. Reuter, “Low retinal noise in animals with low body temperature allows high visual sensitivity,” Nature 334, 348–350 (1988).
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Lee, B.

D. Dacey, O. S. Packer, L. Diller, D. Brainard, B. Peterson, and B. Lee, “Center surround receptive field structure of cone bipolar cells in primate retina,” Vis. Res. 40, 1801–1811 (2000).
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Figures (8)

Fig. 1.
Fig. 1.

Cone fundamentals. Spectral sensitivity functions with peaks of 559, 529, and 519 nm were corrected for lens and macular filtering to produce the curves shown here.

Fig. 2.
Fig. 2.

Family of sensitivity curves produced by the RG and BY mechanisms. Each curve represents a different value for l in Eq. (4). Highlighted in red and blue are the most probable curves in a retina with an L(L+M) cone ratio of 0.75. The upper plot are the predicted sensitivity curves for the RG mechanism and the lower for BY.

Fig. 3.
Fig. 3.

Sensitivity of the chromatic mechanisms. By changing the %L (L/(L+M)×100) cones in the observer’s retina, a family of valence curves is produced for the RG (red lines) and BY (blue lines) mechanisms. Note the null point of the BY curves shifts considerably between the three conditions plotted.

Fig. 4.
Fig. 4.

Comparison of the standard model with the BY midget ganglion cell theory proposed here. A rgb color space (a) was constructed from the Neitz fundamentals [42] and data from [57] was best fit to the space in a least squares sense (b). (c) Demonstrates the effect of varying k in Sk(L+M). This scenario is not capable of matching the 522 nm unique green of observer 2 and simultaneously passing through equal energy white (d). (e) Simulates changing k in S(kL+(1k)M), again failing to fit the data from observer 2 (f). Finally, varying k in L(kS+(1k)M) results in a good fit with the data (g) and (h).

Fig. 5.
Fig. 5.

Spectral locations of unique hues as a function of %L (L/(L+M)×100). The color of the line represents the unique hue and style of the line indicates the peak sensitivity of the L photopigment: solid=559nm, dashed=557nm, dasheddotted=555nm

Fig. 6.
Fig. 6.

BY ganglion cell theory predicts unique hue variability. A distribution of LM cone ratios (represented as %L) is plotted in the top figure. Using this data, a predicted distribution of unique green was produced (green trace) and overlaid over an observed plot from [61] (gray area). The bottom plot displays predicted distributions for unique blue and yellow.

Fig. 7.
Fig. 7.

Change in unique hues with eccentricity. Hue is expected to vary with eccentricity due to the increasing number of cones with direct input to midget ganglion cells at more eccentric locations. The eccentricity indicated here is approximate.

Fig. 8.
Fig. 8.

Schematic representation of the BY midget ganglion cell theory. A BY system is built by summing the input from L-, M-, and S-cones and then differencing this signal from an L-cone directly contacting a bipolar cell. In the case of the ON pathway, this will produce a yellow signal, while the OFF pathway will result in blue. In the case of the RG system an M-cone is differenced from neighboring cones to produce red (OFF pathway) or green (ON pathway).

Tables (3)

Tables Icon

Table 1. Proposed Mechanisms

Tables Icon

Table 2. Predicted Values of Unique Hues

Tables Icon

Table 3. Observed Values of Unique Hues

Equations (7)

Equations on this page are rendered with MathJax. Learn more.

[lrlglbmrmgmbsrsgsb]1[l(λ)m(λ)s(λ)]=[R(λ)G(λ)B(λ)],
r=RR+G+B,g=GR+G+B,b=BR+G+B.
Ax=b,
g(λ)=δ(λ)ω(ρS(λ)+(1l)M(λ)+lL(λ)),
0=λ=390750g(λ)dλ.
α(λ)=r=0ngr(λ)P(S|r)
P(S|r)=(nr)PLr(1PL)nr.

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