Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Electrical coupling between red and green cones in primate retina

Abstract

Color vision in humans and other Old World primates depends on differences in the absorption properties of three spectral types of cone photoreceptors. Primate cones are linked by gap junctions, but it is not known to what extent the various cone types are electrically coupled through these junctions. Here we show, by using a combination of dye labeling and electrical recordings in the retina of macaque monkeys, that neighboring red and green cones are homologously and heterologously coupled by nonrectifying gap junctions. This indiscriminate coupling blurs the differences between red- and green-cone signals. The average junctional conductance is about 650 pS. Our calculations indicate that coupling between red and green cones may cause a modest decrease in human color discrimination with a comparable increase in luminance discrimination.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Dye coupling between cones.
Figure 2: Electrical coupling between adjacent red and green cones is indiscriminate.
Figure 3: Temporal frequency characteristics of electrical coupling.
Figure 4: Cone spectral sensitivity is altered by electrical coupling between red and green cones.
Figure 5: Collected results of spectral sensitivity measurements.
Figure 6: Blue cones do not receive electrical input from other types of cones.
Figure 7: Predicted effects of cone-cone coupling on human wavelength discrimination.

Similar content being viewed by others

References

  1. Baylor, D.A., Fuortes, M.G.F. & O'Bryan, P.M. Receptive fields of cones in the retina of turtle. J. Physiol. (Lond.) 214, 265–294 (1971).

    Article  CAS  Google Scholar 

  2. DeVries, S.H., Qi, X., Smith, R., Makous, W. & Sterling, P. Electrical coupling between mammalian cones. Curr. Biol. 12, 1900–1907 (2002).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  4. Tessier-Lavigne, M. & Attwell, D. The effect of photoreceptor coupling and synapse nonlinearity on signal:noise ratio in early visual processing. Proc. R. Soc. Lond. B 234, 171–197 (1988).

    Article  CAS  Google Scholar 

  5. Bennett, M.V.L. & Zukin, R.S. Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41, 495–511 (2004).

    Article  CAS  Google Scholar 

  6. Raviola, E. & Gilula, N.B. Gap junctions between photoreceptor cells in the vertebrate retina. Proc. Natl. Acad. Sci. USA 70, 1677–1681 (1973).

    Article  CAS  Google Scholar 

  7. Tsukamoto, Y., Masarachia, P., Schein, S.J. & Sterling, P. Gap junctions between the pedicles of macaque foveal cones. Vision Res. 32, 1809–1815 (1992).

    Article  CAS  Google Scholar 

  8. Kolb, H., Goede, P., Roberts, S., McDermott, R. & Gouras, P. Uniqueness of the S-cone pedicle in the human retina and consequences for color processing. J. Comp. Neurol. 386, 443–460 (1997).

    Article  CAS  Google Scholar 

  9. Dartnall, H.J.A., Bowmaker, J.K. & Mollon, J.D. Human visual pigments: microspectrophotometric results from the eyes of seven persons. Proc. R. Soc. Lond. B 220, 115–130 (1983).

    Article  CAS  Google Scholar 

  10. MacNichol, E.F., Levine, J.S., Mansfield, R.J.W., Lipetz, L.E. & Collins, B.A. Microspectrophotometry of visual pigments in primate photoreceptors. in Colour Vision (eds. Mollon, J.D. & Sharpe, L.T.) 13–38 (Academic, London, 1983).

    Google Scholar 

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

    Article  CAS  Google Scholar 

  12. Schnapf, J.L., Kraft, T.W. & Baylor, D.A. Spectral sensitivity of human cones. Nature 325, 439–441 (1987).

    Article  CAS  Google Scholar 

  13. Davidson, J.S. & Baumgarten, I.M. Glycyrrhetinic acid derivatives: a novel class of inhibitors of gap-junctional intercellular communication. J. Pharmacol. Exp. Ther. 246, 1104–1107 (1988).

    CAS  PubMed  Google Scholar 

  14. Weckstrom, M., Hardie, R.C. & Laughlin, S.B. Voltage-activated potassium channels in blowfly photoreceptors and their role in light adaptation. J. Physiol. (Lond.) 440, 635–657 (1991).

    Article  CAS  Google Scholar 

  15. Yagi, T. & Macleish, P.R. Ionic conductances of monkey solitary cone inner segments. J. Neurophysiol. 71, 656–665 (1994).

    Article  CAS  Google Scholar 

  16. Schnapf, J.L., Nunn, B.J., Meister, M. & Baylor, D.A. Visual transduction in cones of the monkey Macaca fascicularis. J. Physiol. (Lond.) 427, 681–713 (1990).

    Article  CAS  Google Scholar 

  17. Schneeweis, D.M. & Schnapf, J.L. The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. J. Neurosci. 19, 1203–1216 (1999).

    Article  CAS  Google Scholar 

  18. Slaughter, M.M. & Miller, R.F. 2-Amino-4-phosphonobutyric acid: a new pharmacological tool for retina research. Science 211, 182–185 (1981).

    Article  CAS  Google Scholar 

  19. Verweij, J., Hornstein, E.P. & Schnapf, J.L. Surround antagonism in macaque cone photoreceptors. J. Neurosci. 23, 10249–10257 (2003).

    Article  CAS  Google Scholar 

  20. Jahromi, S.S., Wentlandt, K., Piran, S. & Carlen, P.L. Anticonvulsant actions of gap junctional blockers in an in vitro seizure model. J. Neurophysiol. 88, 1893–1902 (2001).

    Article  Google Scholar 

  21. Schneeweis, D.M. & Schnapf, J.L. Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056 (1995).

    Article  CAS  Google Scholar 

  22. Hsu, A., Smith, R.G., Buchsbaum, G. & Sterling, P. Cost of cone coupling to trichromacy in primate fovea. J. Opt. Soc. Am. A 17, 635–640 (2000).

    Article  CAS  Google Scholar 

  23. Roorda, A., Metha, A.B., Lennie, P. & Williams, D.R. Packing arrangement of the three cone classes in primate retina. Vision Res. 41, 1291–1306 (2001).

    Article  CAS  Google Scholar 

  24. DeValois, R.L., Morgan, H.C., Polson, M.C., Mead, W.R. & Hull, E.M. Psychophysical studies of monkey vision. I. Macaque luminosity and color vision tests. Vision Res. 14, 53–67 (1974).

    Article  CAS  Google Scholar 

  25. Wyszecki, G. & Stiles, W.S. Color Science: Concepts and Methods, Quantitative Data and Formulae (Wiley, New York, 1982).

    Google Scholar 

  26. Field, G.D. & Rieke, F. Nonlinear signal transfer from mouse rods to bipolar cells and implications for visual sensitivity. Neuron 34, 773–785 (2002).

    Article  CAS  Google Scholar 

  27. Detwiler, P.B. & Hodgkin, A.L. Electrical coupling between cones in turtle retina. J. Physiol. (Lond.) 291s, 75–100 (1979).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  30. Mariani, A.P. The neural organization of the outer plexiform layer of the primate retina. Int. Rev. Cytol. 86, 285–320 (1983).

    Article  Google Scholar 

  31. Bumsted, K., Jasoni, C., Szel, A. & Hendrickson, A. Spatial and temporal expression of cone opsins during monkey retinal development. J. Comp. Neurol. 378, 117–134 (1997).

    Article  CAS  Google Scholar 

  32. Dacey, D.M., Diller, L.C., Verweij, J. & Williams, D.R. Physiology of L- and M-cone inputs to H1 horizontal cells in the primate retina. J. Opt. Soc. Am. A 17, 589–596 (2000).

    Article  CAS  Google Scholar 

  33. Deeb, S.S., Diller, L., Williams, D.R. & Dacey, D.M. Interindividual and topographical variations of L:M cone ratios in monkey retinas. J. Opt. Soc. Am. A 17, 538–544 (2000).

    Article  CAS  Google Scholar 

  34. Reid, R.C. & Shapley, R.M. Spatial structure of cone inputs to receptive fields in primate lateral geniculate nucleus. Nature 356, 716–718 (1992).

    Article  CAS  Google Scholar 

  35. Martin, P.R., Lee, B.B., White, A.J.R., Solomon, S.G. & Ruttiger, L. Chromatic sensitivity of ganglion cells in the peripheral primate retina. Nature 410, 933–936 (2001).

    Article  CAS  Google Scholar 

  36. Reid, R.C. & Shapley, R.M. Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus. J. Neurosci. 22, 6158–6175 (2002).

    Article  CAS  Google Scholar 

  37. Lennie, P., Haake, P.W. & Williams, D.R. The design of chromatically opponent receptive fields. in Computational Models of Visual Processing (eds. Landy, M.S. & Movshon, J.A.) 71–82 (MIT, Cambridge, 1991).

    Google Scholar 

  38. Calkins, D.J. & Sterling, P. Evidence that circuits for spatial and color vision segregate at the first retinal synapse. Neuron 24, 313–321 (1999).

    Article  CAS  Google Scholar 

  39. Diller, L. et al. L and M cone contributions to the midget and parasol ganglion cell receptive fields of macaque monkey retina. J. Neurosci. 24, 1079–1088 (2004).

    Article  CAS  Google Scholar 

  40. Li, W. & DeVries, S.H. Separate blue- and green-cone networks in the mammalian retina. Nat. Neurosci. 7, 751–756 (2004).

    Article  CAS  Google Scholar 

  41. Lee, E-J. et al. The immunocytochemical localization of connexin 36 at rod and cone gap junctions in the guinea pig retina. Eur. J. Neurosci. 18, 2925–2934 (2003).

    Article  Google Scholar 

  42. Srinivas, M. et al. Functional properties of channels formed by the neuronal gap junction protein connexin36. J. Neurosci. 19, 9848–9855 (1999).

    Article  CAS  Google Scholar 

  43. Bendat, J.S. & Piersol, A.G. Random Data: Analysis and Measurement Procedures (Wiley, New York, 2000).

    Google Scholar 

  44. Nathans, J. The evolution and physiology of human color vision: insights from molecular genetic studies of visual pigments. Neuron 24, 299–312 (1999).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Baylor, D. Copenhagen, P. Li, W. Makous, D. Schneeweis and M. Tessier-Lavigne for comments on the manuscript, D. Copenhagen for valuable assistance with confocal microscopy and S. Massey for discussions on dye labeling. This work was supported by grants EY07642, EY07001 and EY07120 from the NIH and a grant from That Man May See, Inc. Additional support was received from Research to Prevent Blindness.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Eric P Hornstein or Julie L Schnapf.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hornstein, E., Verweij, J. & Schnapf, J. Electrical coupling between red and green cones in primate retina. Nat Neurosci 7, 745–750 (2004). https://doi.org/10.1038/nn1274

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1274

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing