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Light adaptation in cone vision involves switching between receptor and post-receptor sites

Nature volume 449, pages 603606 (04 October 2007) | Download Citation


We see over an enormous range of mean light levels, greater than the range of output signals retinal neurons can produce. Even highlights and shadows within a single visual scene can differ 10,000-fold in intensity—exceeding the range of distinct neural signals by a factor of 100. The effectiveness of daylight vision under these conditions relies on at least two retinal mechanisms that adjust sensitivity in the 200 ms intervals between saccades1. One mechanism is in the cone photoreceptors (receptor adaptation)2,3,4,5 and the other is at a previously unknown location within the retinal circuitry that benefits from convergence of signals from multiple cones (post-receptor adaptation)6,7. Here we find that post-receptor adaptation occurs as signals are relayed from cone bipolar cells to ganglion cells. Furthermore, we find that the two adaptive mechanisms are essentially mutually exclusive: as light levels increase the main site of adaptation switches from the circuitry to the cones. These findings help explain how human cone vision encodes everyday scenes, and, more generally, how sensory systems handle the challenges posed by a diverse physical environment.

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  1. 1.

    Eye Movements and Vision (Plenum, New York, 1967)

  2. 2.

    & Visual adaptation in monkey cones: recordings of late receptor potentials. Science 170, 1423–1426 (1970)

  3. 3.

    & Light adaptation of primate cones: an analysis based on extracellular data. Vision Res. 23, 1539–1547 (1983)

  4. 4.

    , , & Visual transduction in cones of the monkey Macaca fascicularis. J. Physiol. (Lond.) 427, 681–713 (1990)

  5. 5.

    & The photovoltage of macaque cone photoreceptors: adaptation, noise, and kinetics. J. Neurosci. 19, 1203–1216 (1999)

  6. 6.

    , , , & Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. J. Opt. Soc. Am. A 7, 2223–2236 (1990)

  7. 7.

    , , & Light adaptation in the primate retina: analysis of changes in gain and dynamics of monkey retinal ganglion cells. Vis. Neurosci. 4, 75–93 (1990)

  8. 8.

    , , & Horizontal cells reveal cone type-specific adaptation in primate retina. Proc. Natl Acad. Sci. USA 96, 14611–14616 (1999)

  9. 9.

    , , & Primate horizontal cell dynamics: an analysis of sensitivity regulation in the outer retina. J. Neurophysiol. 85, 545–558 (2001)

  10. 10.

    , , & Dynamics of sensitivity regulation in primate outer retina: the horizontal cell network. J. Vis. 3, 513–526 (2003)

  11. 11.

    & Changes in time scale and sensitivity in turtle photoreceptors. J. Physiol. (Lond.) 242, 729–758 (1974)

  12. 12.

    , , & Light adaptation in cone photoreceptors of the salamander: a role for cytoplasmic calcium. J. Physiol. (Lond.) 420, 447–469 (1990)

  13. 13.

    & Morphological classification of bipolar cells of the primate retina. Eur. J. Neurosci. 3, 1069–1088 (1991)

  14. 14.

    & Fast and slow contrast adaptation in retinal circuitry. Neuron 36, 909–919 (2002)

  15. 15.

    , & Dynamic predictive coding by the retina. Nature 436, 71–77 (2005)

  16. 16.

    & Presynaptic mechanism for slow contrast adaptation in mammalian retinal ganglion cells. Neuron 50, 453–464 (2006)

  17. 17.

    , & Retinal light adaptation—evidence for a feedback mechanism. Nature 310, 314–316 (1984)

  18. 18.

    Lower-level visual processing and models of light adaptation. Annu. Rev. Psychol. 49, 503–535 (1998)

  19. 19.

    , & The time course of adaptation in macaque retinal ganglion cells. Vision Res. 36, 913–931 (1996)

  20. 20.

    , , & Efficiency and ambiguity in an adaptive neural code. Nature 412, 787–792 (2001)

  21. 21.

    A simple coding procedure enhances a neuron's information capacity. Z. Naturforsch. C 36, 910–912 (1981)

  22. 22.

    , , & Controlling the gain of rod-mediated signals in the mammalian retina. J. Neurosci. 26, 3959–3970 (2006)

  23. 23.

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

  24. 24.

    & Bandpass filtering at the rod to second-order cell synapse in salamander (Ambystoma tigrinum) retina. J. Neurosci. 23, 3796–3806 (2003)

  25. 25.

    & Photovoltage of rods and cones in the macaque retina. Science 268, 1053–1056 (1995)

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We thank D. Dacey, O. Packer, B. Peterson and T. Haun for providing primate tissue; P. Newman and M. Wixey for technical assistance; J. Cafaro, E. J. Chichilnisky, T. Doan, W. Dunn, G. Horwitz, R. Kiani, G. Murphy, F. Soo, B. Wark for comments on the manuscript; and B. Lundstrom for comments on figures. This work was supported by the National Institutes of Health (F.R.), Achievement Rewards for College Scientists Foundation (F.A.D.) and the Howard Hughes Medical Institute (F.R., and F.A.D. with a predoctoral fellowship).

Author Contributions F.A.D., M.J.L. and F.R. participated in all aspects of this work.

Author information


  1. Program in Neurobiology and Behavior,

    • Felice A. Dunn
  2. Howard Hughes Medical Institute and,

    • Fred Rieke
  3. Department of Physiology and Biophysics, University of Washington, Seattle, Washington 98195, USA

    • Fred Rieke
  4. Functional Neurobiology and Helmholtz Institute, Utrecht University, 3584 CH Utrecht, The Netherlands

    • Martin J. Lankheet


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Competing interests

Reprints and permissions information is available at www.nature.com/reprints. The authors declare no competing financial interests.

Corresponding author

Correspondence to Fred Rieke.

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