Abstract

In the primate retina, H1 horizontal cells form an electrically coupled network and receive convergent input from long- (L-) and middle- (M-) wavelength-sensitive cones. Using an in vitro preparation of the intact retina to record the light-evoked voltage responses of H1 cells, we systematically varied the L- and M-cone stimulus contrast and measured the relative L- and M-cone input strength for 137 cells across 33 retinas from three Old World species (Macaca nemestrina, M. fascicularis, and Papio anubis). We found that the L- and the M-cone inputs were summed by the H1 cell in proportion to the stimulus cone contrast, which yielded a measure of what we term L- and M-cone contrast gain. The proportion of L-cone contrast gain was highly variable, ranging from 25% to 90% [mean ± standard deviation, (60±14)%]. This variability was accounted for by retinal location within an individual, with the temporal retina showing a consistently higher percentage of L-cone gain, and by large overall variation across individuals, with the mean percentage of L-cone gain ranging from 32% to 80%. We hypothesize that the relative L- and M-cone contrast gain is determined simply by the relative number of L and M cones in the H1 cell’s receptive field and that the variability in L- and M-cone contrast gain reflects a corresponding variability in the mosaic of L and M cones.

© 2000 Optical Society of America

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  1. V. C. Smith, J. Pokorny, “Spectral sensitivity of the foveal cone photopigments between 400 and 500 nm,” Vision Res. 15, 161–171 (1975).
    [CrossRef] [PubMed]
  2. W. A. Rushton, H. D. Baker, “Red–green sensitivity in normal vision,” Vision Res. 4, 75–85 (1964).
    [CrossRef] [PubMed]
  3. G. H. Jacobs, J. F. Deegan, “Spectral sensitivity of macaque monkeys measured with ERG flicker photometry,” Visual Neurosci. 14, 921–928 (1997).
    [CrossRef]
  4. P. Lennie, J. Pokorny, V. C. Smith, “Luminance,” J. Opt. Soc. Am. A 10, 1283–1293 (1993).
    [CrossRef] [PubMed]
  5. A. Roorda, D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397, 520–522 (1999).
    [CrossRef] [PubMed]
  6. D. H. Brainard, A. Roorda, Y. Yamauchi, J. B. Calderone, A. Metha, M. Neitz, J. Neitz, D. R. Williams, G. H. Jacobs, “Functional consequences of the relative numbers of L and M cones,” J. Opt. Soc. Am. A 17, 607–614 (2000).
    [CrossRef]
  7. B. B. Lee, P. R. Martin, A. Valberg, “The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina,” J. Physiol. (London) 404, 323–347 (1988).
  8. R. Shapley, “Parallel neural pathways and visual function,” in The Cognitive Neurosciences, M. S. Gazzaniga, E. Bizzi, I. B. Black, C. Blakemore, L. Cosmides, S. M. Kosslyn, J. E. LeDoux, J. A. Movshon, S. Pinker, M. I. Posner, P. Rakic, D. L. Schacter, J. Tooby, E. Tulving, eds. (MIT Press, Cambridge, Mass., 1995).
  9. D. M. Dacey, “Primate retina: cell types, circuits and color opponency,” in Progress in Retinal and Eye Research, N. N. Osborne, G. J. Chader, eds. (Pergamon, Oxford, UK, 1999), Vol. 18, pp. 737–763.
  10. J. Verweij, D. M. Dacey, B. B. Peterson, S. L. Buck, “Sensitivity and dynamics of rod signals in H1 horizontal cells of the macaque monkey retina,” Vision Res. 39, 3662–3672 (1999).
    [CrossRef]
  11. D. M. Dacey, B. B. Lee, D. K. Stafford, J. Pokorny, V. C. Smith, “Horizontal cells of the primate retina: cone specificity without spectral opponency,” Science 271, 656–659 (1996).
    [CrossRef] [PubMed]
  12. A. K. Goodchild, T. L. Chan, U. Grünert, “Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina,” Visual Neurosci. 13, 833–845 (1996).
    [CrossRef]
  13. S. S. Deeb, L. C. Diller, D. R. Williams, D. M. Dacey, “Interindividual and topographical variation of L:M cone ratios in monkey retinas,” J. Opt. Soc. Am. A 17, 538–544 (2000).
    [CrossRef]
  14. W. H. Swanson, T. Ueno, V. C. Smith, J. Pokorny, “Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations,” J. Opt. Soc. Am. A 4, 1992–2005 (1987).
    [CrossRef] [PubMed]
  15. D. M. Dacey, B. B. Lee, “The blue-ON opponent pathway in primate retina originates from a distinct bistratified ganglion cell type,” Nature 367, 731–735 (1994).
    [CrossRef] [PubMed]
  16. D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. (London) 390, 145–160 (1987).
  17. S. M. Dawis, “Polynomial expressions of pigment nomograms,” Vision Res. 21, 1427–1430 (1981).
    [CrossRef] [PubMed]
  18. T. D. Lamb, “Photoreceptor spectral sensitivities: common shape in the long-wavelength region,” Vision Res. 35, 3083–3091 (1995).
    [CrossRef] [PubMed]
  19. H. Wässle, B. B. Boycott, J. Röhrenbeck, “Horizontal cells in the monkey retina: cone connections and dendritic network,” Eur. J. Neurosci. 1, 421–435 (1989).
    [CrossRef] [PubMed]
  20. D. I. Vaney, “Patterns of neuronal coupling in the retina,” in Progress in Retinal and Eye Research, N. N. Osborne, G. J. Chader, eds. (Pergamon, Oxford, UK, 1994), Vol. 13, pp. 301–355.
  21. D. J. Calkins, “Synaptic organization of cone pathways in the primate retina,” in Color Vision: from Genes to Perception, K. R. Gegenfurtner, L. T. Sharpe, eds. (Cambridge U. Press, New York, 1999), pp. 163–180.
  22. D. M. Schneeweis, J. L. Schnapf, “The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics,” J. Neurosci. 19, 1203–1216 (1999).
    [PubMed]
  23. S. A. Hagstrom, J. Neitz, M. Neitz, “Variations in cone populations for red–green color vision examined by analysis of mRNA,” NeuroReport 9, 1963–1967 (1998).
    [CrossRef] [PubMed]
  24. J. Bowmaker, “Visual pigments and color vision in primates,” in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 1–10.
  25. J. D. Mollon, J. K. Bowmaker, “The spatial arrangement of cones in the primate fovea,” Nature 360, 677–679 (1992).
    [CrossRef] [PubMed]
  26. O. S. Packer, D. R. Williams, D. G. Bensinger, “Photopigment transmittance imaging of the primate photoreceptor mosaic,” J. Neurosci. 16, 2251–2260 (1996).
    [PubMed]
  27. B. B. Lee, “Receptor inputs to primate ganglion cells,” in Color Vision: from Genes to Perception, K. R. Gegenfurtner, L. T. Sharpe, eds. (Cambridge U. Press, New York, 1999), pp. 203–218.
  28. L. C. Diller, J. Verweij, D. R. Williams, D. M. Dacey, “L and M cone inputs to peripheral parasol and midget ganglion cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S817 (1999).
  29. O. S. Packer, L. C. Diller, B. B. Lee, D. M. Dacey, “Diffuse cone bipolar cells in macaque monkey retina are spatially opponent,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S790 (1999).

2000 (2)

1999 (5)

D. M. Schneeweis, J. L. Schnapf, “The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics,” J. Neurosci. 19, 1203–1216 (1999).
[PubMed]

J. Verweij, D. M. Dacey, B. B. Peterson, S. L. Buck, “Sensitivity and dynamics of rod signals in H1 horizontal cells of the macaque monkey retina,” Vision Res. 39, 3662–3672 (1999).
[CrossRef]

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

L. C. Diller, J. Verweij, D. R. Williams, D. M. Dacey, “L and M cone inputs to peripheral parasol and midget ganglion cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S817 (1999).

O. S. Packer, L. C. Diller, B. B. Lee, D. M. Dacey, “Diffuse cone bipolar cells in macaque monkey retina are spatially opponent,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S790 (1999).

1998 (1)

S. A. Hagstrom, J. Neitz, M. Neitz, “Variations in cone populations for red–green color vision examined by analysis of mRNA,” NeuroReport 9, 1963–1967 (1998).
[CrossRef] [PubMed]

1997 (1)

G. H. Jacobs, J. F. Deegan, “Spectral sensitivity of macaque monkeys measured with ERG flicker photometry,” Visual Neurosci. 14, 921–928 (1997).
[CrossRef]

1996 (3)

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

A. K. Goodchild, T. L. Chan, U. Grünert, “Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina,” Visual Neurosci. 13, 833–845 (1996).
[CrossRef]

O. S. Packer, D. R. Williams, D. G. Bensinger, “Photopigment transmittance imaging of the primate photoreceptor mosaic,” J. Neurosci. 16, 2251–2260 (1996).
[PubMed]

1995 (1)

T. D. Lamb, “Photoreceptor spectral sensitivities: common shape in the long-wavelength region,” Vision Res. 35, 3083–3091 (1995).
[CrossRef] [PubMed]

1994 (1)

D. M. Dacey, B. B. Lee, “The blue-ON opponent pathway in primate retina originates from a distinct bistratified ganglion cell type,” Nature 367, 731–735 (1994).
[CrossRef] [PubMed]

1993 (1)

1992 (1)

J. D. Mollon, J. K. Bowmaker, “The spatial arrangement of cones in the primate fovea,” Nature 360, 677–679 (1992).
[CrossRef] [PubMed]

1989 (1)

H. Wässle, B. B. Boycott, J. Röhrenbeck, “Horizontal cells in the monkey retina: cone connections and dendritic network,” Eur. J. Neurosci. 1, 421–435 (1989).
[CrossRef] [PubMed]

1988 (1)

B. B. Lee, P. R. Martin, A. Valberg, “The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina,” J. Physiol. (London) 404, 323–347 (1988).

1987 (2)

D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. (London) 390, 145–160 (1987).

W. H. Swanson, T. Ueno, V. C. Smith, J. Pokorny, “Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations,” J. Opt. Soc. Am. A 4, 1992–2005 (1987).
[CrossRef] [PubMed]

1981 (1)

S. M. Dawis, “Polynomial expressions of pigment nomograms,” Vision Res. 21, 1427–1430 (1981).
[CrossRef] [PubMed]

1975 (1)

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

1964 (1)

W. A. Rushton, H. D. Baker, “Red–green sensitivity in normal vision,” Vision Res. 4, 75–85 (1964).
[CrossRef] [PubMed]

Baker, H. D.

W. A. Rushton, H. D. Baker, “Red–green sensitivity in normal vision,” Vision Res. 4, 75–85 (1964).
[CrossRef] [PubMed]

Baylor, D. A.

D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. (London) 390, 145–160 (1987).

Bensinger, D. G.

O. S. Packer, D. R. Williams, D. G. Bensinger, “Photopigment transmittance imaging of the primate photoreceptor mosaic,” J. Neurosci. 16, 2251–2260 (1996).
[PubMed]

Bowmaker, J.

J. Bowmaker, “Visual pigments and color vision in primates,” in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 1–10.

Bowmaker, J. K.

J. D. Mollon, J. K. Bowmaker, “The spatial arrangement of cones in the primate fovea,” Nature 360, 677–679 (1992).
[CrossRef] [PubMed]

Boycott, B. B.

H. Wässle, B. B. Boycott, J. Röhrenbeck, “Horizontal cells in the monkey retina: cone connections and dendritic network,” Eur. J. Neurosci. 1, 421–435 (1989).
[CrossRef] [PubMed]

Brainard, D. H.

Buck, S. L.

J. Verweij, D. M. Dacey, B. B. Peterson, S. L. Buck, “Sensitivity and dynamics of rod signals in H1 horizontal cells of the macaque monkey retina,” Vision Res. 39, 3662–3672 (1999).
[CrossRef]

Calderone, J. B.

Calkins, D. J.

D. J. Calkins, “Synaptic organization of cone pathways in the primate retina,” in Color Vision: from Genes to Perception, K. R. Gegenfurtner, L. T. Sharpe, eds. (Cambridge U. Press, New York, 1999), pp. 163–180.

Chan, T. L.

A. K. Goodchild, T. L. Chan, U. Grünert, “Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina,” Visual Neurosci. 13, 833–845 (1996).
[CrossRef]

Dacey, D. M.

S. S. Deeb, L. C. Diller, D. R. Williams, D. M. Dacey, “Interindividual and topographical variation of L:M cone ratios in monkey retinas,” J. Opt. Soc. Am. A 17, 538–544 (2000).
[CrossRef]

L. C. Diller, J. Verweij, D. R. Williams, D. M. Dacey, “L and M cone inputs to peripheral parasol and midget ganglion cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S817 (1999).

J. Verweij, D. M. Dacey, B. B. Peterson, S. L. Buck, “Sensitivity and dynamics of rod signals in H1 horizontal cells of the macaque monkey retina,” Vision Res. 39, 3662–3672 (1999).
[CrossRef]

O. S. Packer, L. C. Diller, B. B. Lee, D. M. Dacey, “Diffuse cone bipolar cells in macaque monkey retina are spatially opponent,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S790 (1999).

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

D. M. Dacey, B. B. Lee, “The blue-ON opponent pathway in primate retina originates from a distinct bistratified ganglion cell type,” Nature 367, 731–735 (1994).
[CrossRef] [PubMed]

D. M. Dacey, “Primate retina: cell types, circuits and color opponency,” in Progress in Retinal and Eye Research, N. N. Osborne, G. J. Chader, eds. (Pergamon, Oxford, UK, 1999), Vol. 18, pp. 737–763.

Dawis, S. M.

S. M. Dawis, “Polynomial expressions of pigment nomograms,” Vision Res. 21, 1427–1430 (1981).
[CrossRef] [PubMed]

Deeb, S. S.

Deegan, J. F.

G. H. Jacobs, J. F. Deegan, “Spectral sensitivity of macaque monkeys measured with ERG flicker photometry,” Visual Neurosci. 14, 921–928 (1997).
[CrossRef]

Diller, L. C.

S. S. Deeb, L. C. Diller, D. R. Williams, D. M. Dacey, “Interindividual and topographical variation of L:M cone ratios in monkey retinas,” J. Opt. Soc. Am. A 17, 538–544 (2000).
[CrossRef]

L. C. Diller, J. Verweij, D. R. Williams, D. M. Dacey, “L and M cone inputs to peripheral parasol and midget ganglion cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S817 (1999).

O. S. Packer, L. C. Diller, B. B. Lee, D. M. Dacey, “Diffuse cone bipolar cells in macaque monkey retina are spatially opponent,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S790 (1999).

Goodchild, A. K.

A. K. Goodchild, T. L. Chan, U. Grünert, “Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina,” Visual Neurosci. 13, 833–845 (1996).
[CrossRef]

Grünert, U.

A. K. Goodchild, T. L. Chan, U. Grünert, “Horizontal cell connections with short-wavelength-sensitive cones in macaque monkey retina,” Visual Neurosci. 13, 833–845 (1996).
[CrossRef]

Hagstrom, S. A.

S. A. Hagstrom, J. Neitz, M. Neitz, “Variations in cone populations for red–green color vision examined by analysis of mRNA,” NeuroReport 9, 1963–1967 (1998).
[CrossRef] [PubMed]

Jacobs, G. H.

Lamb, T. D.

T. D. Lamb, “Photoreceptor spectral sensitivities: common shape in the long-wavelength region,” Vision Res. 35, 3083–3091 (1995).
[CrossRef] [PubMed]

Lee, B. B.

O. S. Packer, L. C. Diller, B. B. Lee, D. M. Dacey, “Diffuse cone bipolar cells in macaque monkey retina are spatially opponent,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S790 (1999).

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

D. M. Dacey, B. B. Lee, “The blue-ON opponent pathway in primate retina originates from a distinct bistratified ganglion cell type,” Nature 367, 731–735 (1994).
[CrossRef] [PubMed]

B. B. Lee, P. R. Martin, A. Valberg, “The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina,” J. Physiol. (London) 404, 323–347 (1988).

B. B. Lee, “Receptor inputs to primate ganglion cells,” in Color Vision: from Genes to Perception, K. R. Gegenfurtner, L. T. Sharpe, eds. (Cambridge U. Press, New York, 1999), pp. 203–218.

Lennie, P.

Martin, P. R.

B. B. Lee, P. R. Martin, A. Valberg, “The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina,” J. Physiol. (London) 404, 323–347 (1988).

Metha, A.

Mollon, J. D.

J. D. Mollon, J. K. Bowmaker, “The spatial arrangement of cones in the primate fovea,” Nature 360, 677–679 (1992).
[CrossRef] [PubMed]

Neitz, J.

Neitz, M.

Nunn, B. J.

D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. (London) 390, 145–160 (1987).

Packer, O. S.

O. S. Packer, L. C. Diller, B. B. Lee, D. M. Dacey, “Diffuse cone bipolar cells in macaque monkey retina are spatially opponent,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S790 (1999).

O. S. Packer, D. R. Williams, D. G. Bensinger, “Photopigment transmittance imaging of the primate photoreceptor mosaic,” J. Neurosci. 16, 2251–2260 (1996).
[PubMed]

Peterson, B. B.

J. Verweij, D. M. Dacey, B. B. Peterson, S. L. Buck, “Sensitivity and dynamics of rod signals in H1 horizontal cells of the macaque monkey retina,” Vision Res. 39, 3662–3672 (1999).
[CrossRef]

Pokorny, J.

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

P. Lennie, J. Pokorny, V. C. Smith, “Luminance,” J. Opt. Soc. Am. A 10, 1283–1293 (1993).
[CrossRef] [PubMed]

W. H. Swanson, T. Ueno, V. C. Smith, J. Pokorny, “Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations,” J. Opt. Soc. Am. A 4, 1992–2005 (1987).
[CrossRef] [PubMed]

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

Röhrenbeck, J.

H. Wässle, B. B. Boycott, J. Röhrenbeck, “Horizontal cells in the monkey retina: cone connections and dendritic network,” Eur. J. Neurosci. 1, 421–435 (1989).
[CrossRef] [PubMed]

Roorda, A.

Rushton, W. A.

W. A. Rushton, H. D. Baker, “Red–green sensitivity in normal vision,” Vision Res. 4, 75–85 (1964).
[CrossRef] [PubMed]

Schnapf, J. L.

D. M. Schneeweis, J. L. Schnapf, “The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics,” J. Neurosci. 19, 1203–1216 (1999).
[PubMed]

D. A. Baylor, B. J. Nunn, J. L. Schnapf, “Spectral sensitivity of cones of the monkey Macaca fascicularis,” J. Physiol. (London) 390, 145–160 (1987).

Schneeweis, D. M.

D. M. Schneeweis, J. L. Schnapf, “The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics,” J. Neurosci. 19, 1203–1216 (1999).
[PubMed]

Shapley, R.

R. Shapley, “Parallel neural pathways and visual function,” in The Cognitive Neurosciences, M. S. Gazzaniga, E. Bizzi, I. B. Black, C. Blakemore, L. Cosmides, S. M. Kosslyn, J. E. LeDoux, J. A. Movshon, S. Pinker, M. I. Posner, P. Rakic, D. L. Schacter, J. Tooby, E. Tulving, eds. (MIT Press, Cambridge, Mass., 1995).

Smith, V. C.

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

P. Lennie, J. Pokorny, V. C. Smith, “Luminance,” J. Opt. Soc. Am. A 10, 1283–1293 (1993).
[CrossRef] [PubMed]

W. H. Swanson, T. Ueno, V. C. Smith, J. Pokorny, “Temporal modulation sensitivity and pulse-detection thresholds for chromatic and luminance perturbations,” J. Opt. Soc. Am. A 4, 1992–2005 (1987).
[CrossRef] [PubMed]

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

Stafford, D. K.

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

Swanson, W. H.

Ueno, T.

Valberg, A.

B. B. Lee, P. R. Martin, A. Valberg, “The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina,” J. Physiol. (London) 404, 323–347 (1988).

Vaney, D. I.

D. I. Vaney, “Patterns of neuronal coupling in the retina,” in Progress in Retinal and Eye Research, N. N. Osborne, G. J. Chader, eds. (Pergamon, Oxford, UK, 1994), Vol. 13, pp. 301–355.

Verweij, J.

L. C. Diller, J. Verweij, D. R. Williams, D. M. Dacey, “L and M cone inputs to peripheral parasol and midget ganglion cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S817 (1999).

J. Verweij, D. M. Dacey, B. B. Peterson, S. L. Buck, “Sensitivity and dynamics of rod signals in H1 horizontal cells of the macaque monkey retina,” Vision Res. 39, 3662–3672 (1999).
[CrossRef]

Wässle, H.

H. Wässle, B. B. Boycott, J. Röhrenbeck, “Horizontal cells in the monkey retina: cone connections and dendritic network,” Eur. J. Neurosci. 1, 421–435 (1989).
[CrossRef] [PubMed]

Williams, D. R.

S. S. Deeb, L. C. Diller, D. R. Williams, D. M. Dacey, “Interindividual and topographical variation of L:M cone ratios in monkey retinas,” J. Opt. Soc. Am. A 17, 538–544 (2000).
[CrossRef]

D. H. Brainard, A. Roorda, Y. Yamauchi, J. B. Calderone, A. Metha, M. Neitz, J. Neitz, D. R. Williams, G. H. Jacobs, “Functional consequences of the relative numbers of L and M cones,” J. Opt. Soc. Am. A 17, 607–614 (2000).
[CrossRef]

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

L. C. Diller, J. Verweij, D. R. Williams, D. M. Dacey, “L and M cone inputs to peripheral parasol and midget ganglion cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S817 (1999).

O. S. Packer, D. R. Williams, D. G. Bensinger, “Photopigment transmittance imaging of the primate photoreceptor mosaic,” J. Neurosci. 16, 2251–2260 (1996).
[PubMed]

Yamauchi, Y.

Eur. J. Neurosci. (1)

H. Wässle, B. B. Boycott, J. Röhrenbeck, “Horizontal cells in the monkey retina: cone connections and dendritic network,” Eur. J. Neurosci. 1, 421–435 (1989).
[CrossRef] [PubMed]

Invest. Ophthalmol. Visual Sci. Suppl. (2)

L. C. Diller, J. Verweij, D. R. Williams, D. M. Dacey, “L and M cone inputs to peripheral parasol and midget ganglion cells in primate retina,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S817 (1999).

O. S. Packer, L. C. Diller, B. B. Lee, D. M. Dacey, “Diffuse cone bipolar cells in macaque monkey retina are spatially opponent,” Invest. Ophthalmol. Visual Sci. Suppl. 40, S790 (1999).

J. Neurosci. (2)

O. S. Packer, D. R. Williams, D. G. Bensinger, “Photopigment transmittance imaging of the primate photoreceptor mosaic,” J. Neurosci. 16, 2251–2260 (1996).
[PubMed]

D. M. Schneeweis, J. L. Schnapf, “The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics,” J. Neurosci. 19, 1203–1216 (1999).
[PubMed]

J. Opt. Soc. Am. A (4)

J. Physiol. (London) (2)

B. B. Lee, P. R. Martin, A. Valberg, “The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina,” J. Physiol. (London) 404, 323–347 (1988).

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Figures (6)

Fig. 1
Fig. 1

(a) Normalized quantal intensity of the red (R), green (G), and blue (B) LED’s as a function of wavelength, measured in the plane of the retina. (b) Predicted L-, M-, and S-cone spectral sensitivities (modified from Baylor et al.16).

Fig. 2
Fig. 2

(a) Example of a cone-isolating stimulus. Mean intensities of the red (R), green (G), and blue (B) LED’s were adjusted to produce equal mean quantal catches in each cone type, whereas the amplitudes of the LED’s were adjusted to modulate only M cones. (b) Predicted response of the three cone types to the stimulus shown in (a). Only M cones are modulated while L and S cones remain silent. (c) Predicted L-cone (●) and M-cone (○) contrasts for the 13 conditions in our stimulus paradigm. Arrows indicate cone contrasts for the L- and the M-cone-isolating conditions. The cone contrast of the M-cone-isolating condition described in (a) and (b) is indicated by an asterisk. (d) Traces denoted by L and M are the predicted L- and M-cone contrasts shown in (c). Trace denoted by L+M is the predicted response of an H1 cell that receives additive input from L and M cones.

Fig. 3
Fig. 3

(a) Camera lucida tracing of a Golgi-impregnated macaque H1 cell showing the cell body and axon terminal (entire axon not shown). Dotted circles are drawn around cone-contacting dendritic terminals. The cell was located 13 mm from the fovea. (b) Photomicrograph of a flat-mounted macaque retina showing a patch of the H1 cell mosaic revealed by intracellular injection of neurobiotin. Arrowheads indicate three cone pedicles demarcated by H1 cell dendritic terminals. Scale bars in (a) and (b), 10 µm. (c) Responses (upper traces) of a macaque H1 cell to L-, M-, and S-cone-isolating stimuli (lower traces) as described in Fig. 2(a).

Fig. 4
Fig. 4

(a) Responses of an H1 horizontal cell to the 13 conditions of our stimulus paradigm. Each trace is the average of at least 3 s of data. (b) Fundamental amplitude of the responses shown in (a). The lines joining the traces in (a) with the data points in (b) indicate responses to L- and M-cone-isolating stimuli. The dotted curve drawn through the data points is the fit of the model used to determine the relative L- and M-cone contrast gains. This cell had an L/(L+M) gain of 0.56 (L/M=1.27).

Fig. 5
Fig. 5

(a) Histogram of the L/(L+M) ratio for all 137 H1 horizontal cells. The L/(L+M) value is given on the bottom axis, whereas the corresponding L/M value is given on the top axis. The histogram was generated with a bin size of 0.01 along the L/(L+M) axis. There was a large variability in the relative strength of L- and M-cone signal strength, with a mean of L/(L+M)=0.60. (b) The range of L- and M-cone signal strength in 22 animals (123 cells), demonstrating a large variation in the relative strength of L- and M-cone signals in H1 cells among the animals. Error bars [standard deviation (SD), 0.0073] for measurements of the L/(L+M) ratio in one cell are included for the animal whose data are shown at the bottom of the plot.

Fig. 6
Fig. 6

Retinal location of 125 H1 cells from 25 retinas, showing the nasal–temporal and the superior–inferior meridians. Diagonal lines bisecting the meridians indicated the four retinal quadrants. The majority of cells from which recordings were made were located in the far periphery. The inset shows the relative L/(L+M) ratio for a subset of 66 cells from 13 retinas, plotted as a function of retinal quadrant (nasal: n=22; temporal: n=27; superior: n=17). Only retinas with sampled temporal cells were included, and the data were normalized to the temporal quadrant. The L/(L+M) ratio of nasal cells and superior cells was 86% and 90%, respectively, relative to that of temporal cells. Error bars are SD=0.11 for nasal cells and SD=0.16 for superior cells. The inferior quadrant was omitted because the subset included only two inferior cells.

Equations (3)

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s(λ)=1-10-0.04s(λ),
PC=allλ[Pi(λ)×sC(λ)]allλPi(λ),
Responseamplitude=WLLc+WMMc,

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