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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

Abstract

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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Acknowledgements

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.

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Affiliations

  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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https://doi.org/10.1038/nature06150

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