Abstract

Cone synaptic terminals couple electrically to their neighbors. This reduces the amplitude of temporally uncorrelated voltage differences between neighbors. For an achromatic stimulus coarser than the cone mosaic, the uncorrelated voltage difference between neighbors represents mostly noise; so noise is reduced more than the signal. Here coupling improves signal-to-noise ratio and enhances contrast sensitivity. But for a chromatic stimulus the uncorrelated voltage difference between neighbors of different spectral type represents mostly signal; so signal would be reduced more than the noise. This cost of cone coupling to encoding chromatic signals was evaluated using a compartmental model of the foveal cone array. When cones sensitive to middle (M) and long (L) wavelengths alternated regularly, and the conductance between a cone and all of its immediate neighbors was 1000 pS (∼2 connexons/cone pair), coupling reduced the difference between the L and M action spectra by nearly fivefold, from about 38% to 8%. However, L and M cones distribute randomly in the mosaic, forming small patches of like type, and within a patch the responses to a chromatic stimulus are correlated. In such a mosaic, coupling still reduced the difference between the L and M action spectra, but only by 2.4-fold, to about 18%. This result is independent of the L/M ratio. Thus “patchiness” of the L/M mosaic allows cone coupling to improve achromatic contrast sensitivity while minimizing the cost to chromatic sensitivity.

© 2000 Optical Society of America

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    [CrossRef] [PubMed]
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    [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [CrossRef] [PubMed]
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    [PubMed]
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  24. D. J. Calkins, S. Schein, Y. Tsukamoto, P. Sterling, “M and L cones in macaque fovea connect to midget ganglion cells via different numbers of excitatory synapses,” Nature 371, 70–72 (1994).
    [CrossRef] [PubMed]
  25. C. M. Cicerone, J. L. Nerger, “The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis,” Vision Res. 29, 115–128 (1989).
    [CrossRef] [PubMed]
  26. A. Roorda, D. R. Williams, “The arrangement of the three cone classes in the living human eye,” Nature 397, 520–522 (1999).
    [CrossRef] [PubMed]
  27. M. Neitz, J. Neitz, G. H. Jacobs, “Spectral tuning of pigments underlying red–green color vision,” Science 252, 971–974 (1991).
    [CrossRef] [PubMed]
  28. S. B. Balding, S. A. Sjoberg, M. Neitz, J. Neitz, “Real time PCR method to accurately quantitate L and M cone pigment gene expression,” Invest. Ophthalmol. Visual Sci. Suppl. 39, 959 (1998).
  29. 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]
  30. D. M. Schneeweis, J. L. Schnapf, “The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics,” J. Neurosci. 19, 1203–1216 (1999).
    [PubMed]
  31. E. N. Pugh, J. D. Mollon, “A theory of the π1 and π3 color mechanisms of Stiles,” Vision Res. 19, 293–312 (1979).
    [CrossRef]
  32. T. W. Kraft, J. Neitz, M. Neitz, “Spectra of human L cones,” Vision Res. 38, 3663–3670 (1998).
    [CrossRef]
  33. D. R. Williams, N. Sekiguchi, W. Haake, D. Brainard, O. Packer, in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 11–22.

1999 (2)

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

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

1998 (5)

S. B. Balding, S. A. Sjoberg, M. Neitz, J. Neitz, “Real time PCR method to accurately quantitate L and M cone pigment gene expression,” Invest. Ophthalmol. Visual Sci. Suppl. 39, 959 (1998).

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]

T. W. Kraft, J. Neitz, M. Neitz, “Spectra of human L cones,” Vision Res. 38, 3663–3670 (1998).
[CrossRef]

A. Hsu, Y. Tsukamoto, R. G. Smith, P. Sterling, “Functional architecture of primate rod and cone axons,” Vision Res. 38, 2539–2549 (1998).
[CrossRef]

D. J. Calkins, Y. Tsukamoto, P. Sterling, “Microcircuitry and mosaic of a blue/yellow ganglion cell in the primate retina,” J. Neurosci. 18, 3373–3385 (1998).
[PubMed]

1995 (1)

D. M. Schneeweis, J. L. Schnapf, “Photovoltage of rods and cones in the macaque retina,” Science 268, 1053–1056 (1995).
[CrossRef] [PubMed]

1994 (1)

D. J. Calkins, S. Schein, Y. Tsukamoto, P. Sterling, “M and L cones in macaque fovea connect to midget ganglion cells via different numbers of excitatory synapses,” Nature 371, 70–72 (1994).
[CrossRef] [PubMed]

1993 (1)

1992 (3)

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

Y. Tsukamoto, P. Masarachia, S. J. Schein, P. Sterling, “Gap junctions between the pedicles of macaque foveal cones,” Vision Res. 32, 1809–1815 (1992).
[CrossRef] [PubMed]

R. G. Smith, “NeuronC: a computational language for investigating functional architecture of neural circuits,” J. Neurosci. Methods 43, 83–108 (1992).
[CrossRef] [PubMed]

1991 (2)

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

M. Neitz, J. Neitz, G. H. Jacobs, “Spectral tuning of pigments underlying red–green color vision,” Science 252, 971–974 (1991).
[CrossRef] [PubMed]

1990 (1)

P. Ahnelt, C. Keri, H. Kolb, “Identification of pedicles of putative blue-sensitive cones in the human retina,” J. Comp. Neurol. 293, 39–53 (1990).
[CrossRef] [PubMed]

1989 (2)

E. M. Lasater, R. A. Normann, H. Kolb, “Signal integration at the pedicle of turtle cone photoreceptors: an anatomical and electrophysiological study,” Visual Neurosci. 2, 553–564 (1989).
[CrossRef]

C. M. Cicerone, J. L. Nerger, “The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis,” Vision Res. 29, 115–128 (1989).
[CrossRef] [PubMed]

1988 (2)

P. Sterling, M. A. Freed, R. G. Smith, “Architecture of the rod and cone circuits to the On-beta ganglion cell,” J. Neurosci. 8, 623–642 (1988).
[PubMed]

M. Tessier-Lavigne, D. Attwell, “The effect of photoreceptor coupling and synapse nonlinearity on signal: noise ratio in early visual processing,” Proc. R. Soc. London Ser. B. 234, 171–197 (1988).
[CrossRef]

1987 (1)

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).

1983 (1)

D. Johnston, T. H. Brown, “Interpretation of voltage-clamp measurements in hippocampal neurons,” J. Neurophysiol. 50, 464–486 (1983).
[PubMed]

1982 (1)

D. Attwell, F. S. Werblin, M. Wilson, “The properties of single cones isolated from the tiger salamander retina,” J. Physiol. (London) 328, 259–283 (1982).

1979 (1)

E. N. Pugh, J. D. Mollon, “A theory of the π1 and π3 color mechanisms of Stiles,” Vision Res. 19, 293–312 (1979).
[CrossRef]

1977 (1)

H. Kolb, “The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations,” J. Neurocytol. 6, 131–153 (1977).
[CrossRef] [PubMed]

1976 (1)

T. D. Lamb, E. J. Simon, “The relation between intercellular coupling and electrical noise in turtle photoreceptors,” J. Physiol. (London) 263, 257–286 (1976).

1973 (1)

E. Raviola, N. B. Gilula, “Gap junctions between photoreceptor cells in the vertebrate retina,” Proc. Natl. Acad. Sci. USA 70, 1677–1681 (1973).
[CrossRef] [PubMed]

1971 (1)

D. A. Baylor, M. G. F. Fuortes, P. M. O’Bryan, “Receptive fields of cones in the retina of the turtle,” J. Physiol. (London) 214, 265–294 (1971).

Ahnelt, P.

P. Ahnelt, C. Keri, H. Kolb, “Identification of pedicles of putative blue-sensitive cones in the human retina,” J. Comp. Neurol. 293, 39–53 (1990).
[CrossRef] [PubMed]

Allen, K. A.

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

Attwell, D.

M. Tessier-Lavigne, D. Attwell, “The effect of photoreceptor coupling and synapse nonlinearity on signal: noise ratio in early visual processing,” Proc. R. Soc. London Ser. B. 234, 171–197 (1988).
[CrossRef]

D. Attwell, F. S. Werblin, M. Wilson, “The properties of single cones isolated from the tiger salamander retina,” J. Physiol. (London) 328, 259–283 (1982).

Balding, S. B.

S. B. Balding, S. A. Sjoberg, M. Neitz, J. Neitz, “Real time PCR method to accurately quantitate L and M cone pigment gene expression,” Invest. Ophthalmol. Visual Sci. Suppl. 39, 959 (1998).

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).

D. A. Baylor, M. G. F. Fuortes, P. M. O’Bryan, “Receptive fields of cones in the retina of the turtle,” J. Physiol. (London) 214, 265–294 (1971).

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]

Brainard, D.

D. R. Williams, N. Sekiguchi, W. Haake, D. Brainard, O. Packer, in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 11–22.

Brainard, D. H.

Brown, T. H.

D. Johnston, T. H. Brown, “Interpretation of voltage-clamp measurements in hippocampal neurons,” J. Neurophysiol. 50, 464–486 (1983).
[PubMed]

Buchsbaum, G.

A. Hsu, L. Hahn, G. Buchsbaum, P. Sterling are preparing a manuscript entitled, “Why cones in the human fovea are electrically coupled.”

Calkins, D. J.

D. J. Calkins, Y. Tsukamoto, P. Sterling, “Microcircuitry and mosaic of a blue/yellow ganglion cell in the primate retina,” J. Neurosci. 18, 3373–3385 (1998).
[PubMed]

D. J. Calkins, S. Schein, Y. Tsukamoto, P. Sterling, “M and L cones in macaque fovea connect to midget ganglion cells via different numbers of excitatory synapses,” Nature 371, 70–72 (1994).
[CrossRef] [PubMed]

Cicerone, C. M.

C. M. Cicerone, J. L. Nerger, “The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis,” Vision Res. 29, 115–128 (1989).
[CrossRef] [PubMed]

Curcio, C. A.

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

De Vries, S. H.

S. H. De Vries, Houston Medical School, University of Texas, Houston, Tex. 77030 (personal communication, 1999).

Freed, M. A.

P. Sterling, M. A. Freed, R. G. Smith, “Architecture of the rod and cone circuits to the On-beta ganglion cell,” J. Neurosci. 8, 623–642 (1988).
[PubMed]

Fuortes, M. G. F.

D. A. Baylor, M. G. F. Fuortes, P. M. O’Bryan, “Receptive fields of cones in the retina of the turtle,” J. Physiol. (London) 214, 265–294 (1971).

Gilula, N. B.

E. Raviola, N. B. Gilula, “Gap junctions between photoreceptor cells in the vertebrate retina,” Proc. Natl. Acad. Sci. USA 70, 1677–1681 (1973).
[CrossRef] [PubMed]

Haake, W.

D. R. Williams, N. Sekiguchi, W. Haake, D. Brainard, O. Packer, in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 11–22.

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]

Hahn, L.

A. Hsu, L. Hahn, G. Buchsbaum, P. Sterling are preparing a manuscript entitled, “Why cones in the human fovea are electrically coupled.”

Hsu, A.

A. Hsu, Y. Tsukamoto, R. G. Smith, P. Sterling, “Functional architecture of primate rod and cone axons,” Vision Res. 38, 2539–2549 (1998).
[CrossRef]

A. Hsu, L. Hahn, G. Buchsbaum, P. Sterling are preparing a manuscript entitled, “Why cones in the human fovea are electrically coupled.”

Hurley, J. B.

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

Jack, J. J. B.

J. J. B. Jack, D. Noble, R. W. Tsien, Electric Current Flow in Excitable Cells (Clarendon, Oxford, UK, 1988).

Jacobs, G. H.

M. Neitz, J. Neitz, G. H. Jacobs, “Spectral tuning of pigments underlying red–green color vision,” Science 252, 971–974 (1991).
[CrossRef] [PubMed]

Johnston, D.

D. Johnston, T. H. Brown, “Interpretation of voltage-clamp measurements in hippocampal neurons,” J. Neurophysiol. 50, 464–486 (1983).
[PubMed]

Keri, C.

P. Ahnelt, C. Keri, H. Kolb, “Identification of pedicles of putative blue-sensitive cones in the human retina,” J. Comp. Neurol. 293, 39–53 (1990).
[CrossRef] [PubMed]

Klock, I. B.

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

Kolb, H.

P. Ahnelt, C. Keri, H. Kolb, “Identification of pedicles of putative blue-sensitive cones in the human retina,” J. Comp. Neurol. 293, 39–53 (1990).
[CrossRef] [PubMed]

E. M. Lasater, R. A. Normann, H. Kolb, “Signal integration at the pedicle of turtle cone photoreceptors: an anatomical and electrophysiological study,” Visual Neurosci. 2, 553–564 (1989).
[CrossRef]

H. Kolb, “The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations,” J. Neurocytol. 6, 131–153 (1977).
[CrossRef] [PubMed]

Kraft, T. W.

T. W. Kraft, J. Neitz, M. Neitz, “Spectra of human L cones,” Vision Res. 38, 3663–3670 (1998).
[CrossRef]

Lamb, T. D.

T. D. Lamb, E. J. Simon, “The relation between intercellular coupling and electrical noise in turtle photoreceptors,” J. Physiol. (London) 263, 257–286 (1976).

Lasater, E. M.

E. M. Lasater, R. A. Normann, H. Kolb, “Signal integration at the pedicle of turtle cone photoreceptors: an anatomical and electrophysiological study,” Visual Neurosci. 2, 553–564 (1989).
[CrossRef]

Lerea, C. L.

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

Masarachia, P.

Y. Tsukamoto, P. Masarachia, S. J. Schein, P. Sterling, “Gap junctions between the pedicles of macaque foveal cones,” Vision Res. 32, 1809–1815 (1992).
[CrossRef] [PubMed]

Milam, A. H.

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

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]

E. N. Pugh, J. D. Mollon, “A theory of the π1 and π3 color mechanisms of Stiles,” Vision Res. 19, 293–312 (1979).
[CrossRef]

Neitz, J.

T. W. Kraft, J. Neitz, M. Neitz, “Spectra of human L cones,” Vision Res. 38, 3663–3670 (1998).
[CrossRef]

S. B. Balding, S. A. Sjoberg, M. Neitz, J. Neitz, “Real time PCR method to accurately quantitate L and M cone pigment gene expression,” Invest. Ophthalmol. Visual Sci. Suppl. 39, 959 (1998).

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]

M. Neitz, J. Neitz, G. H. Jacobs, “Spectral tuning of pigments underlying red–green color vision,” Science 252, 971–974 (1991).
[CrossRef] [PubMed]

Neitz, M.

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]

S. B. Balding, S. A. Sjoberg, M. Neitz, J. Neitz, “Real time PCR method to accurately quantitate L and M cone pigment gene expression,” Invest. Ophthalmol. Visual Sci. Suppl. 39, 959 (1998).

T. W. Kraft, J. Neitz, M. Neitz, “Spectra of human L cones,” Vision Res. 38, 3663–3670 (1998).
[CrossRef]

M. Neitz, J. Neitz, G. H. Jacobs, “Spectral tuning of pigments underlying red–green color vision,” Science 252, 971–974 (1991).
[CrossRef] [PubMed]

Nerger, J. L.

C. M. Cicerone, J. L. Nerger, “The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis,” Vision Res. 29, 115–128 (1989).
[CrossRef] [PubMed]

Noble, D.

J. J. B. Jack, D. Noble, R. W. Tsien, Electric Current Flow in Excitable Cells (Clarendon, Oxford, UK, 1988).

Normann, R. A.

E. M. Lasater, R. A. Normann, H. Kolb, “Signal integration at the pedicle of turtle cone photoreceptors: an anatomical and electrophysiological study,” Visual Neurosci. 2, 553–564 (1989).
[CrossRef]

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).

O’Bryan, P. M.

D. A. Baylor, M. G. F. Fuortes, P. M. O’Bryan, “Receptive fields of cones in the retina of the turtle,” J. Physiol. (London) 214, 265–294 (1971).

Packer, O.

D. R. Williams, N. Sekiguchi, W. Haake, D. Brainard, O. Packer, in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 11–22.

Pugh, E. N.

E. N. Pugh, J. D. Mollon, “A theory of the π1 and π3 color mechanisms of Stiles,” Vision Res. 19, 293–312 (1979).
[CrossRef]

Raviola, E.

E. Raviola, N. B. Gilula, “Gap junctions between photoreceptor cells in the vertebrate retina,” Proc. Natl. Acad. Sci. USA 70, 1677–1681 (1973).
[CrossRef] [PubMed]

Roorda, A.

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

Rozental, R.

D. C. Spray, E. Scemes, R. Rozental, in Fundamental Neuroscience, M. Zigmond, F. E. Bloom, S. C. Landis, J. L. Roberts, L. R. Squire, eds. (Academic, San Diego, Calif., 1999), pp. 317–343.

Scemes, E.

D. C. Spray, E. Scemes, R. Rozental, in Fundamental Neuroscience, M. Zigmond, F. E. Bloom, S. C. Landis, J. L. Roberts, L. R. Squire, eds. (Academic, San Diego, Calif., 1999), pp. 317–343.

Schein, S.

D. J. Calkins, S. Schein, Y. Tsukamoto, P. Sterling, “M and L cones in macaque fovea connect to midget ganglion cells via different numbers of excitatory synapses,” Nature 371, 70–72 (1994).
[CrossRef] [PubMed]

Schein, S. J.

Y. Tsukamoto, P. Masarachia, S. J. Schein, P. Sterling, “Gap junctions between the pedicles of macaque foveal cones,” Vision Res. 32, 1809–1815 (1992).
[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. M. Schneeweis, J. L. Schnapf, “Photovoltage of rods and cones in the macaque retina,” Science 268, 1053–1056 (1995).
[CrossRef] [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]

D. M. Schneeweis, J. L. Schnapf, “Photovoltage of rods and cones in the macaque retina,” Science 268, 1053–1056 (1995).
[CrossRef] [PubMed]

Sekiguchi, N.

N. Sekiguchi, D. R. Williams, D. H. Brainard, “Efficiency in detection of isoluminant and isochromatic interference fringes,” J. Opt. Soc. Am. A 10, 2118–2133 (1993).
[CrossRef]

D. R. Williams, N. Sekiguchi, W. Haake, D. Brainard, O. Packer, in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 11–22.

Simon, E. J.

T. D. Lamb, E. J. Simon, “The relation between intercellular coupling and electrical noise in turtle photoreceptors,” J. Physiol. (London) 263, 257–286 (1976).

Sjoberg, S. A.

S. B. Balding, S. A. Sjoberg, M. Neitz, J. Neitz, “Real time PCR method to accurately quantitate L and M cone pigment gene expression,” Invest. Ophthalmol. Visual Sci. Suppl. 39, 959 (1998).

Sloan, K. R.

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

Smith, R. G.

A. Hsu, Y. Tsukamoto, R. G. Smith, P. Sterling, “Functional architecture of primate rod and cone axons,” Vision Res. 38, 2539–2549 (1998).
[CrossRef]

R. G. Smith, “NeuronC: a computational language for investigating functional architecture of neural circuits,” J. Neurosci. Methods 43, 83–108 (1992).
[CrossRef] [PubMed]

P. Sterling, M. A. Freed, R. G. Smith, “Architecture of the rod and cone circuits to the On-beta ganglion cell,” J. Neurosci. 8, 623–642 (1988).
[PubMed]

Spray, D. C.

D. C. Spray, E. Scemes, R. Rozental, in Fundamental Neuroscience, M. Zigmond, F. E. Bloom, S. C. Landis, J. L. Roberts, L. R. Squire, eds. (Academic, San Diego, Calif., 1999), pp. 317–343.

Sterling, P.

D. J. Calkins, Y. Tsukamoto, P. Sterling, “Microcircuitry and mosaic of a blue/yellow ganglion cell in the primate retina,” J. Neurosci. 18, 3373–3385 (1998).
[PubMed]

A. Hsu, Y. Tsukamoto, R. G. Smith, P. Sterling, “Functional architecture of primate rod and cone axons,” Vision Res. 38, 2539–2549 (1998).
[CrossRef]

D. J. Calkins, S. Schein, Y. Tsukamoto, P. Sterling, “M and L cones in macaque fovea connect to midget ganglion cells via different numbers of excitatory synapses,” Nature 371, 70–72 (1994).
[CrossRef] [PubMed]

Y. Tsukamoto, P. Masarachia, S. J. Schein, P. Sterling, “Gap junctions between the pedicles of macaque foveal cones,” Vision Res. 32, 1809–1815 (1992).
[CrossRef] [PubMed]

P. Sterling, M. A. Freed, R. G. Smith, “Architecture of the rod and cone circuits to the On-beta ganglion cell,” J. Neurosci. 8, 623–642 (1988).
[PubMed]

A. Hsu, L. Hahn, G. Buchsbaum, P. Sterling are preparing a manuscript entitled, “Why cones in the human fovea are electrically coupled.”

Tessier-Lavigne, M.

M. Tessier-Lavigne, D. Attwell, “The effect of photoreceptor coupling and synapse nonlinearity on signal: noise ratio in early visual processing,” Proc. R. Soc. London Ser. B. 234, 171–197 (1988).
[CrossRef]

Tsien, R. W.

J. J. B. Jack, D. Noble, R. W. Tsien, Electric Current Flow in Excitable Cells (Clarendon, Oxford, UK, 1988).

Tsukamoto, Y.

A. Hsu, Y. Tsukamoto, R. G. Smith, P. Sterling, “Functional architecture of primate rod and cone axons,” Vision Res. 38, 2539–2549 (1998).
[CrossRef]

D. J. Calkins, Y. Tsukamoto, P. Sterling, “Microcircuitry and mosaic of a blue/yellow ganglion cell in the primate retina,” J. Neurosci. 18, 3373–3385 (1998).
[PubMed]

D. J. Calkins, S. Schein, Y. Tsukamoto, P. Sterling, “M and L cones in macaque fovea connect to midget ganglion cells via different numbers of excitatory synapses,” Nature 371, 70–72 (1994).
[CrossRef] [PubMed]

Y. Tsukamoto, P. Masarachia, S. J. Schein, P. Sterling, “Gap junctions between the pedicles of macaque foveal cones,” Vision Res. 32, 1809–1815 (1992).
[CrossRef] [PubMed]

Werblin, F. S.

D. Attwell, F. S. Werblin, M. Wilson, “The properties of single cones isolated from the tiger salamander retina,” J. Physiol. (London) 328, 259–283 (1982).

Williams, D. R.

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

N. Sekiguchi, D. R. Williams, D. H. Brainard, “Efficiency in detection of isoluminant and isochromatic interference fringes,” J. Opt. Soc. Am. A 10, 2118–2133 (1993).
[CrossRef]

D. R. Williams, N. Sekiguchi, W. Haake, D. Brainard, O. Packer, in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 11–22.

Wilson, M.

D. Attwell, F. S. Werblin, M. Wilson, “The properties of single cones isolated from the tiger salamander retina,” J. Physiol. (London) 328, 259–283 (1982).

Invest. Ophthalmol. Visual Sci. Suppl. (1)

S. B. Balding, S. A. Sjoberg, M. Neitz, J. Neitz, “Real time PCR method to accurately quantitate L and M cone pigment gene expression,” Invest. Ophthalmol. Visual Sci. Suppl. 39, 959 (1998).

J. Comp. Neurol. (2)

P. Ahnelt, C. Keri, H. Kolb, “Identification of pedicles of putative blue-sensitive cones in the human retina,” J. Comp. Neurol. 293, 39–53 (1990).
[CrossRef] [PubMed]

C. A. Curcio, K. A. Allen, K. R. Sloan, C. L. Lerea, J. B. Hurley, I. B. Klock, A. H. Milam, “Distribution and morphology of human cone photoreceptors stained with anti-blue opsin,” J. Comp. Neurol. 312, 610–624 (1991).
[CrossRef] [PubMed]

J. Neurocytol. (1)

H. Kolb, “The organization of the outer plexiform layer in the retina of the cat: electron microscopic observations,” J. Neurocytol. 6, 131–153 (1977).
[CrossRef] [PubMed]

J. Neurophysiol. (1)

D. Johnston, T. H. Brown, “Interpretation of voltage-clamp measurements in hippocampal neurons,” J. Neurophysiol. 50, 464–486 (1983).
[PubMed]

J. Neurosci. (3)

P. Sterling, M. A. Freed, R. G. Smith, “Architecture of the rod and cone circuits to the On-beta ganglion cell,” J. Neurosci. 8, 623–642 (1988).
[PubMed]

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

D. J. Calkins, Y. Tsukamoto, P. Sterling, “Microcircuitry and mosaic of a blue/yellow ganglion cell in the primate retina,” J. Neurosci. 18, 3373–3385 (1998).
[PubMed]

J. Neurosci. Methods (1)

R. G. Smith, “NeuronC: a computational language for investigating functional architecture of neural circuits,” J. Neurosci. Methods 43, 83–108 (1992).
[CrossRef] [PubMed]

J. Opt. Soc. Am. A (1)

J. Physiol. (London) (4)

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).

D. A. Baylor, M. G. F. Fuortes, P. M. O’Bryan, “Receptive fields of cones in the retina of the turtle,” J. Physiol. (London) 214, 265–294 (1971).

T. D. Lamb, E. J. Simon, “The relation between intercellular coupling and electrical noise in turtle photoreceptors,” J. Physiol. (London) 263, 257–286 (1976).

D. Attwell, F. S. Werblin, M. Wilson, “The properties of single cones isolated from the tiger salamander retina,” J. Physiol. (London) 328, 259–283 (1982).

Nature (3)

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

D. J. Calkins, S. Schein, Y. Tsukamoto, P. Sterling, “M and L cones in macaque fovea connect to midget ganglion cells via different numbers of excitatory synapses,” Nature 371, 70–72 (1994).
[CrossRef] [PubMed]

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

NeuroReport (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]

Proc. Natl. Acad. Sci. USA (1)

E. Raviola, N. B. Gilula, “Gap junctions between photoreceptor cells in the vertebrate retina,” Proc. Natl. Acad. Sci. USA 70, 1677–1681 (1973).
[CrossRef] [PubMed]

Proc. R. Soc. London Ser. B. (1)

M. Tessier-Lavigne, D. Attwell, “The effect of photoreceptor coupling and synapse nonlinearity on signal: noise ratio in early visual processing,” Proc. R. Soc. London Ser. B. 234, 171–197 (1988).
[CrossRef]

Science (2)

D. M. Schneeweis, J. L. Schnapf, “Photovoltage of rods and cones in the macaque retina,” Science 268, 1053–1056 (1995).
[CrossRef] [PubMed]

M. Neitz, J. Neitz, G. H. Jacobs, “Spectral tuning of pigments underlying red–green color vision,” Science 252, 971–974 (1991).
[CrossRef] [PubMed]

Vision Res. (5)

C. M. Cicerone, J. L. Nerger, “The relative numbers of long-wavelength-sensitive to middle-wavelength-sensitive cones in the human fovea centralis,” Vision Res. 29, 115–128 (1989).
[CrossRef] [PubMed]

A. Hsu, Y. Tsukamoto, R. G. Smith, P. Sterling, “Functional architecture of primate rod and cone axons,” Vision Res. 38, 2539–2549 (1998).
[CrossRef]

E. N. Pugh, J. D. Mollon, “A theory of the π1 and π3 color mechanisms of Stiles,” Vision Res. 19, 293–312 (1979).
[CrossRef]

T. W. Kraft, J. Neitz, M. Neitz, “Spectra of human L cones,” Vision Res. 38, 3663–3670 (1998).
[CrossRef]

Y. Tsukamoto, P. Masarachia, S. J. Schein, P. Sterling, “Gap junctions between the pedicles of macaque foveal cones,” Vision Res. 32, 1809–1815 (1992).
[CrossRef] [PubMed]

Visual Neurosci. (1)

E. M. Lasater, R. A. Normann, H. Kolb, “Signal integration at the pedicle of turtle cone photoreceptors: an anatomical and electrophysiological study,” Visual Neurosci. 2, 553–564 (1989).
[CrossRef]

Other (5)

J. J. B. Jack, D. Noble, R. W. Tsien, Electric Current Flow in Excitable Cells (Clarendon, Oxford, UK, 1988).

D. C. Spray, E. Scemes, R. Rozental, in Fundamental Neuroscience, M. Zigmond, F. E. Bloom, S. C. Landis, J. L. Roberts, L. R. Squire, eds. (Academic, San Diego, Calif., 1999), pp. 317–343.

S. H. De Vries, Houston Medical School, University of Texas, Houston, Tex. 77030 (personal communication, 1999).

A. Hsu, L. Hahn, G. Buchsbaum, P. Sterling are preparing a manuscript entitled, “Why cones in the human fovea are electrically coupled.”

D. R. Williams, N. Sekiguchi, W. Haake, D. Brainard, O. Packer, in From Pigments to Perception, A. Valberg, B. B. Lee, eds. (Plenum, New York, 1991), pp. 11–22.

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Figures (5)

Fig. 1
Fig. 1

Diagram of the simulation. Each cone responded with a photovoltage according to the action spectrum defined by its S, M, or L pigment. The voltages were then pooled by electrical coupling at the synaptic terminal. Responses were measured separately for each cone, then averaged for cones of like type.

Fig. 2
Fig. 2

Cone coupling shifts action spectra. (a) Action spectra of isolated S, M, and L cones from Ref. 1. Shading indicates area of nonoverlap between L and M spectra [plotted in Figs. 4(a) and 5(a) below]. (b) Action spectra with 1000-pS coupling conductance. Shading, same as in (b).

Fig. 3
Fig. 3

Even modest coupling of S cone markedly shifts its action spectrum. S cone coupling varied between 0 and 200 pS; M and L cone coupling was constant at 1000 pS.

Fig. 4
Fig. 4

Coupling reduces separation of L and M action spectra. (a) Reduction is greater for a regular (alternating) array than for a random array. For a coupling strength of 1000 pS (arrows), separation between L and M spectra is twofold larger for the random array than for the regular array. (b) With coupling, peak sensitivities for L and M cones converge toward 545 nm. Convergence is steeper for the regular array.

Fig. 5
Fig. 5

L/M ratio in random array little affects separation of the action spectra or peak spectral sensitivities. (a) Area of nonoverlap for random array decreases with greater coupling, but cone ratio has no effect, except for slight dip at L/M=3. (b) Peaks of L and M action spectra plotted against L/M ratio. Peaks for isolated L and M cones are, respectively, 530 and 560 nm; i.e., they are separated by 30 nm. As the L/M ratio rises, the L peak approaches that of the isolated cone, and the M peak asymptotes to an intermediate wavelength. Despite the shift, the distance between the peaks remains constant.

Equations (3)

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y(x)=exp(-|x/λ|),
λ=coneinputresistancecouplingresistance1/2.
1-(shadedarea/totalarea).

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