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Origin and effect of phototransduction noise in primate cone photoreceptors

Nature Neuroscience volume 16, pages 1692–1700 (2013)Cite this article

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Abstract

Noise in the responses of cone photoreceptors sets a fundamental limit on visual sensitivity, yet the origin of noise in mammalian cones and its relation to behavioral sensitivity are poorly understood. Our work here on primate cones improves understanding of these issues in three ways. First, we found that cone noise was not dominated by spontaneous photopigment activation or by quantal fluctuations in photon absorption, but was instead dominated by other sources, namely channel noise and fluctuations in cyclic GMP. Second, adaptation in cones, unlike that in rods, affected signal and noise differently. This difference helps to explain why thresholds for rod- and cone-mediated signals have different dependencies on background light level. Third, past estimates of noise in mammalian cones are too high to explain behavioral sensitivity. Our measurements indicate a lower level of cone noise and therefore help to reconcile physiological and behavioral estimates of cone noise and sensitivity.

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Figure 1: Temporal components of cone outer segment noise.
Figure 2: Two-electrode recordings allow pharmacological manipulation of cone phototransduction.
Figure 3: High-frequency noise arises from open and close transitions in the cGMP-gated channels.
Figure 4: An additional noise source with power in the low-to-mid frequency range causes fluctuations in cGMP.
Figure 5: Adaptation similarly affects rod signal and noise.
Figure 6: Adaptation affects cone signal and noise differently.
Figure 7: Background dependence of rod and cone detection thresholds.

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References

  1. Baylor, D.A., Matthews, G. & Yau, K.W. Two components of electrical dark noise in toad retinal rod outer segments. J. Physiol. (Lond.) 309, 591–621 (1980).

    Article  CAS  Google Scholar 

  2. Baylor, D.A., Nunn, B.J. & Schnapf, J.L. The photocurrent, noise and spectral sensitivity of rods of the monkey Macaca fascicularis. J. Physiol. (Lond.) 357, 575–607 (1984).

    Article  CAS  Google Scholar 

  3. Rieke, F. & Baylor, D.A. Molecular origin of continuous dark noise in rod photoreceptors. Biophys. J. 71, 2553–2572 (1996).

    Article  CAS  Google Scholar 

  4. Fu, Y. & Yau, K.W. Phototransduction in mouse rods and cones. Pflugers Arch. 454, 805–819 (2007).

    Article  CAS  Google Scholar 

  5. Donner, K. Noise and the absolute thresholds of cone and rod vision. Vision Res. 32, 853–866 (1992).

    Article  CAS  Google Scholar 

  6. Field, G.D., Sampath, A.P. & Rieke, F. Retinal processing near absolute threshold: from behavior to mechanism. Annu. Rev. Physiol. 67, 491–514 (2005).

    Article  CAS  Google Scholar 

  7. Schneeweis, D.M. & Schnapf, J.L. Noise and light adaptation in rods of the macaque monkey. Vis. Neurosci. 17, 659–666 (2000).

    Article  CAS  Google Scholar 

  8. Rieke, F. & Rudd, M.E. The challenges natural images pose for visual adaptation. Neuron 64, 605–616 (2009).

    Article  CAS  Google Scholar 

  9. Rieke, F. & Baylor, D.A. Origin and functional impact of dark noise in retinal cones. Neuron 26, 181–186 (2000).

    Article  CAS  Google Scholar 

  10. Fu, Y., Kefalov, V., Luo, D.G., Xue, T. & Yau, K.W. Quantal noise from human red cone pigment. Nat. Neurosci. 11, 565–571 (2008).

    Article  CAS  Google Scholar 

  11. 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 

  12. Fechner, G.T. Elemente dur psychophysik. Elemente dur psychophysik (1860).

  13. Hornstein, E.P., Verweij, J., Li, P.H. & Schnapf, J.L. Gap-junctional coupling and absolute sensitivity of photoreceptors in macaque retina. J. Neurosci. 25, 11201–11209 (2005).

    Article  CAS  Google Scholar 

  14. Luo, D.G., Yue, W.W., Ala-Laurila, P. & Yau, K.W. Activation of visual pigments by light and heat. Science 332, 1307–1312 (2011).

    Article  CAS  Google Scholar 

  15. Swarup, G. & Garbers, D.L. Stimulation of rhodopsin phosphorylation by guanine nucleotides in rod outer segments. Biochemistry 22, 1102–1106 (1983).

    Article  CAS  Google Scholar 

  16. Rieke, F. & Baylor, D.A. Single-photon detection by rod cells of the retina. Rev. Mod. Phys. 70, 1027–1036 (1998).

    Article  CAS  Google Scholar 

  17. Holcman, D. & Korenbrot, J.I. The limit of photoreceptor sensitivity: molecular mechanisms of dark noise in retinal cones. J. Gen. Physiol. 125, 641–660 (2005).

    Article  CAS  Google Scholar 

  18. Field, G.D. & Rieke, F. Mechanisms regulating variability of the single photon responses of mammalian rod photoreceptors. Neuron 35, 733–747 (2002).

    Article  CAS  Google Scholar 

  19. Dunn, F.A., Lankheet, M.J. & Rieke, F. Light adaptation in cone vision involves switching between receptor and post-receptor sites. Nature 449, 603–606 (2007).

    Article  CAS  Google Scholar 

  20. Kefalov, V.J. et al. Breaking the covalent bond–a pigment property that contributes to desensitization in cones. Neuron 46, 879–890 (2005).

    Article  CAS  Google Scholar 

  21. Rieke, F. Temporal contrast adaptation in salamander bipolar cells. J. Neurosci. 21, 9445–9454 (2001).

    Article  CAS  Google Scholar 

  22. Borghuis, B.G., Sterling, P. & Smith, R.G. Loss of sensitivity in an analog neural circuit. J. Neurosci. 29, 3045–3058 (2009).

    Article  CAS  Google Scholar 

  23. Ala-Laurila, P., Greschner, M., Chichilnisky, E.J. & Rieke, F. Cone photoreceptor contributions to noise and correlations in the retinal output. Nat. Neurosci. 14, 1309–1316 (2011).

    Article  CAS  Google Scholar 

  24. Koenig, D. & Hofer, H. The absolute threshold of cone vision. J. Vis. 11, 21 (2011).

    Article  Google Scholar 

  25. Barlow, H.B. Retinal noise and absolute threshold. J. Opt. Soc. Am. 46, 634–639 (1956).

    Article  CAS  Google Scholar 

  26. Tranchina, D., Gordon, J. & Shapley, R.M. Retinal light adaptation–evidence for a feedback mechanism. Nature 310, 314–316 (1984).

    Article  CAS  Google Scholar 

  27. 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 

  28. Burkhardt, D.A. Light adaptation and photopigment bleaching in cone photoreceptors in situ in the retina of the turtle. J. Neurosci. 14, 1091–1105 (1994).

    Article  CAS  Google Scholar 

  29. Donner, K., Copenhagen, D.R. & Reuter, T. Weber and noise adaptation in the retina of the toad Bufo marinus. J. Gen. Physiol. 95, 733–753 (1990).

    Article  CAS  Google Scholar 

  30. Demb, J.B. Functional circuitry of visual adaptation in the retina. J. Physiol. (Lond.) 586, 4377–4384 (2008).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank C. Asbury, F. Dunn, G. Horwitz and R. Sinha for helpful comments on an earlier version of the paper, and M. Cafaro and P. Newman for excellent technical assistance. Color scales were developed and made freely available for Matlab by M. Niccoli. Support was provided by the Howard Hughes Medical Institute (F.R.) and the National Eye Institute of the US National Institutes of Health (R01EY11850 to F.R.). Retinas were obtained from the Washington National Primate Research Center at the University of Washington, US National Institutes of Health grant RR00166, and from the National Center for Research Resources and the Office of Research Infrastructure Programs of the National Institutes of Health through grant Number P51 OD 010425.

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  1. Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, Seattle, Washington, USA

    Juan M Angueyra & Fred Rieke

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  1. Juan M Angueyra
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  2. Fred Rieke
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J.M.A. and F.R. conducted experiments, performed analyses and wrote the manuscript.

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Correspondence to Fred Rieke.

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The authors declare no competing financial interests.

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Angueyra, J., Rieke, F. Origin and effect of phototransduction noise in primate cone photoreceptors. Nat Neurosci 16, 1692–1700 (2013). https://doi.org/10.1038/nn.3534

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