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:

Dynamic predictive coding by the retina

Nature volume 436, pages 71–77 (2005)Cite this article

Abstract

Retinal ganglion cells convey the visual image from the eye to the brain. They generally encode local differences in space and changes in time rather than the raw image intensity. This can be seen as a strategy of predictive coding, adapted through evolution to the average image statistics of the natural environment. Yet animals encounter many environments with visual statistics different from the average scene. Here we show that when this happens, the retina adjusts its processing dynamically. The spatio-temporal receptive fields of retinal ganglion cells change after a few seconds in a new environment. The changes are adaptive, in that the new receptive field improves predictive coding under the new image statistics. We show that a network model with plastic synapses can account for the large variety of observed adaptations.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Adaptation to spatial image correlations.
Figure 2: Adaptation to oriented stimuli.
Figure 3: Adaptation to temporal and spatio-temporal correlations.
Figure 4: Pattern detector model for adaptation.
Figure 5: Network plasticity model for adaptation.

Similar content being viewed by others

References

  1. Dong, D. W. & Atick, J. J. Statistics of natural time-varying images. Network 6, 345–358 (1995)

    Article  Google Scholar 

  2. Field, D. J. Relations between the statistics of natural images and the response properties of cortical cells. J. Opt. Soc. Am. A 4, 2379–2394 (1987)

    Article  ADS  CAS  Google Scholar 

  3. Srinivasan, M. V., Laughlin, S. B. & Dubs, A. Predictive coding: a fresh view of inhibition in the retina. Proc. R. Soc. Lond. B 216, 427–459 (1982)

    Article  ADS  CAS  Google Scholar 

  4. Kuffler, S. W. Discharge patterns and functional organization of mammalian retina. J. Neurophysiol. 16, 37–68 (1953)

    Article  CAS  Google Scholar 

  5. Barlow, H. B. Summation and inhibition in the frog's retina. J. Physiol. (Lond.) 119, 69–88 (1953)

    Article  CAS  Google Scholar 

  6. Meister, M. & Berry, M. J. II The neural code of the retina. Neuron 22, 435–450 (1999)

    Article  CAS  Google Scholar 

  7. Barlow, H. B. in Sensory Communication (ed. Rosenblith, W. A.) 217–234 (MIT Press, Cambridge, Massachusetts, 1961)

    Google Scholar 

  8. van Hateren, J. H. Real and optimal neural images in early vision. Nature 360, 68–70 (1992)

    Article  ADS  CAS  Google Scholar 

  9. Atick, J. J. & Redlich, A. N. What does the retina know about natural scenes? Neural Comput. 4, 196–210 (1992)

    Article  Google Scholar 

  10. Barlow, H. & Földiák, P. in The Computing Neuron (eds Durbin, R., Miall, C. & Mitchison, G.) 54–72 (Addison-Wesley, Wokingham, 1989)

    Google Scholar 

  11. Barlow, H. B. in Vision: Coding and Efficiency (ed. Blakemore, C.) 363–375 (Cambridge Univ. Press, Cambridge, 1990)

    Google Scholar 

  12. Smirnakis, S. M., Berry, M. J., Warland, D. K., Bialek, W. & Meister, M. Adaptation of retinal processing to image contrast and spatial scale. Nature 386, 69–73 (1997)

    Article  ADS  CAS  Google Scholar 

  13. Baccus, S. A. & Meister, M. Fast and slow contrast adaptation in retinal circuitry. Neuron 36, 909–919 (2002)

    Article  CAS  Google Scholar 

  14. Graham, N. V. S. Visual Pattern Analyzers (Oxford Univ. Press, New York, 1989)

    Book  Google Scholar 

  15. Mollon, J. D. in The Perceptual World (eds Von Fiendt, K. & Monstgaard, I. K.) 71–97 (Academic, London, 1977)

    Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Bloomfield, S. A. Orientation-sensitive amacrine and ganglion cells in the rabbit retina. J. Neurophysiol. 71, 1672–1691 (1994)

    Article  CAS  Google Scholar 

  18. Cook, P. B. & McReynolds, J. S. Lateral inhibition in the inner retina is important for spatial tuning of ganglion cells. Nature Neurosci. 1, 714–719 (1998)

    Article  CAS  Google Scholar 

  19. Chander, D. & Chichilnisky, E. J. Adaptation to temporal contrast in primate and salamander retina. J. Neurosci. 21, 9904–9916 (2001)

    Article  CAS  Google Scholar 

  20. Snippe, H. P., Poot, L. & van Hateren, J. H. Asymmetric dynamics of adaptation after onset and offset of flicker. J. Vis. 4, 1–12 (2004)

    Article  CAS  Google Scholar 

  21. Fairhall, A. L., Lewen, G. D., Bialek, W. & van Steveninck, R. R. D. Efficiency and ambiguity in an adaptive neural code. Nature 412, 787–792 (2001)

    Article  ADS  CAS  Google Scholar 

  22. Masland, R. H. The fundamental plan of the retina. Nature Neurosci. 4, 877–886 (2001)

    Article  CAS  Google Scholar 

  23. Yang, C. Y., Lukasiewicz, P., Maguire, G., Werblin, F. S. & Yazulla, S. Amacrine cells in the tiger salamander retina: morphology, physiology, and neurotransmitter identification. J. Comp. Neurol. 312, 19–32 (1991)

    Article  CAS  Google Scholar 

  24. Cook, P. B., Lukasiewicz, P. D. & McReynolds, J. S. Action potentials are required for the lateral transmission of glycinergic transient inhibition in the amphibian retina. J. Neurosci. 18, 2301–2308 (1998)

    Article  CAS  Google Scholar 

  25. Warland, D. K., Reinagel, P. & Meister, M. Decoding visual information from a population of retinal ganglion cells. J. Neurophysiol. 78, 2336–2350 (1997)

    Article  CAS  Google Scholar 

  26. De Valois, K. K. Spatial frequency adaptation can enhance contrast sensitivity. Vision Res. 17, 1057–1065 (1977)

    Article  CAS  Google Scholar 

  27. Blakemore, C. & Campbell, F. W. On the existence of neurones in the human visual system selectively sensitive to the orientation and size of retinal images. J. Physiol. (Lond.) 203, 237–260 (1969)

    Article  CAS  Google Scholar 

  28. Movshon, J. A. & Lennie, P. Pattern-selective adaptation in visual cortical neurones. Nature 278, 850–852 (1979)

    Article  ADS  CAS  Google Scholar 

  29. Snowden, R. J. & Hammett, S. T. Subtractive and divisive adaptation in the human visual system. Nature 355, 248–250 (1992)

    Article  ADS  CAS  Google Scholar 

  30. Bell, C. C. Memory-based expectations in electrosensory systems. Curr. Opin. Neurobiol. 11, 481–487 (2001)

    Article  CAS  Google Scholar 

  31. Aizenman, C. D., Huang, E. J., Manis, P. B. & Linden, D. J. Use-dependent changes in synaptic strength at the Purkinje cell to deep nuclear synapse. Prog. Brain Res. 124, 257–273 (2000)

    Article  CAS  Google Scholar 

  32. Gaiarsa, J. L., Caillard, O. & Ben-Ari, Y. Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci. 25, 564–570 (2002)

    Article  CAS  Google Scholar 

  33. Shapley, R. & Enroth-Cugell, C. in Progress in Retinal Research (eds Osborne, N. & Chader, G.) Vol. 3 263–346 (Pergamon, London, 1984)

    Google Scholar 

  34. Baccus, S. A. & Meister, M. Retina versus cortex; contrast adaptation in parallel visual pathways. Neuron 42, 5–7 (2004)

    Article  CAS  Google Scholar 

  35. Meister, M., Pine, J. & Baylor, D. A. Multi-neuronal signals from the retina: acquisition and analysis. J. Neurosci. Methods 51, 95–106 (1994)

    Article  CAS  Google Scholar 

  36. Chichilnisky, E. J. A simple white noise analysis of neuronal light responses. Network 12, 199–213 (2001)

    Article  CAS  Google Scholar 

  37. Cook, P. B., Lukasiewicz, P. D. & McReynolds, J. S. GABAC receptors control adaptive changes in a glycinergic inhibitory pathway in salamander retina. J. Neurosci. 20, 806–812 (2000)

    Article  CAS  Google Scholar 

  38. Schnitzer, M. J. & Meister, M. Multineuronal firing patterns in the signal from eye to brain. Neuron 37, 499–511 (2003)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank members of the Meister laboratory, H. Sompolinsky and D. Fisher for advice. This work was supported by grants from the National Eye Institute (M.M. and S.A.B.) and the Human Frontier Science Program (T.H.).Author Contributions T.H. and M.M. planned the study, T.H. and S.A.B. performed the experiments, and T.H. and M.M. completed the analysis and wrote the manuscript.

Author information

Author notes

  1. Toshihiko Hosoya

    Present address: RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama, 351-0198, Japan

  2. Stephen A. Baccus

    Present address: Department of Neurobiology, Stanford University, Stanford, California, 94305, USA

Authors and Affiliations

  1. Department of Molecular and Cellular Biology, Harvard University, Massachusetts, 02138, Cambridge, USA

    Toshihiko Hosoya, Stephen A. Baccus & Markus Meister

Authors
  1. Toshihiko Hosoya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephen A. Baccus
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Markus Meister
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Markus Meister.

Ethics declarations

Competing interests

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

Supplementary information

Supplementary Notes

This contains Supplementary Methods and Legends to accompany Supplementary Figures S1-S3 (PDF 748 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hosoya, T., Baccus, S. & Meister, M. Dynamic predictive coding by the retina. Nature 436, 71–77 (2005). https://doi.org/10.1038/nature03689

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03689

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced 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