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Retinal ganglion cells act largely as independent encoders

Abstract

Correlated firing among neurons is widespread in the visual system. Neighbouring neurons, in areas from retina to cortex, tend to fire together more often than would be expected by chance. The importance of this correlated firing for encoding visual information is unclear and controversial1,2,3,4,5. Here we examine its importance in the retina. We present the retina with natural stimuli and record the responses of its output cells, the ganglion cells. We then use information theoretic techniques to measure the amount of information about the stimuli that can be obtained from the cells under two conditions: when their correlated firing is taken into account, and when their correlated firing is ignored. We find that more than 90% of the information about the stimuli can be obtained from the cells when their correlated firing is ignored. This indicates that ganglion cells act largely independently to encode information, which greatly simplifies the problem of decoding their activity.

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Figure 1: Typical ganglion cell responses to the movies.
Figure 2: The degree of correlated activity and the timescale over which it occurs.
Figure 3: Per cent of information about the stimuli obtained from ganglion cell pairs when their correlated spikes were ignored, 1-ΔI/I.
Figure 4: Decoding ganglion cell responses two ways: when the responses were treated as independent, and when correlations in the responses were taken into account.

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References

  1. Gray, C. M. The temporal correlation hypothesis of visual feature integration: still alive and well. Neuron 24, 31–47 (1999).

    Article  CAS  Google Scholar 

  2. Shadlen, M. N. & Movshon, J. A. Synchrony unbound: a critical evaluation of the temporal binding hypothesis. Neuron 24, 67–77 (1999).

    Article  CAS  Google Scholar 

  3. Panzeri, S., Schultz, S. R., Treves, A. & Rolls, E. T. Correlations and the encoding of information in the nervous system. Proc. R. Soc. Lond. B 266, 1001–1012 (1999).

    Article  CAS  Google Scholar 

  4. Nirenberg, S. & Latham, P. E. Population coding in the retina. Curr. Opin. Neurobiol. 8, 488–493 (1998).

    Article  CAS  Google Scholar 

  5. Meister, M. Multineuronal codes in retinal signaling. Proc. Natl Acad. Sci. USA 93, 609–614 (1996).

    Article  ADS  CAS  Google Scholar 

  6. Meister, M., Lagnado, L. & Baylor, D. A. Concerted signaling by retinal ganglion cells. Science 270, 1207–1210 (1995).

    Article  ADS  CAS  Google Scholar 

  7. 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 

  8. Rodieck, R. W. Maintained activity of cat retinal ganglion cells. J. Neurophysiol. 30, 1043–1071 (1967).

    Article  CAS  Google Scholar 

  9. Mastronarde, D. N. Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. J. Neurophysiol. 49, 303–324 (1983).

    Article  CAS  Google Scholar 

  10. Mastronarde, D. N. Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J. Neurophysiol. 49, 325–349 (1983).

    Article  CAS  Google Scholar 

  11. Devries, S. H. Correlated firing in rabbit retinal ganglion cells. J. Neurophysiol. 81, 908–920 (1999).

    Article  CAS  Google Scholar 

  12. Chichilnisky, E. J. & Baylor, D. A. Synchronized firing by ganglion cells in monkey retina. Soc. Neurosci. Abstr. 25, 1042 (1999).

    Google Scholar 

  13. Alonso, J. M., Usrey, W. M. & Reid, R. C. Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383, 815–819 (1996).

    Article  ADS  CAS  Google Scholar 

  14. Perkel, D. H., Gerstein, G. L. & Moore, G. P. Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophys. J. 7, 419–440 (1967).

    Article  CAS  Google Scholar 

  15. Shannon, C. E. & Weaver, W. The Mathematical Theory of Communication (Univ. Illinois Press, Urbana, Illinois, 1949).

    MATH  Google Scholar 

  16. Strong, S. P., Koberle, R., de Ruyter van Steveninck, R. R. & Bialek, W. Entropy and information in neural spike trains. Phys. Rev. Lett. 80, 197–200 (1998).

    Article  ADS  CAS  Google Scholar 

  17. Cover, T. M. & Thomas, J. A. Elements of Information Theory (Wiley, New York, 1991).

    Book  Google Scholar 

  18. Reinagel, P. & Reid, R. C. Temporal coding of visual information in the thalamus. J. Neurosci. 20, 5392–5400 (2000).

    Article  CAS  Google Scholar 

  19. Ruderman, D. L. & Bialek, W. Statistics of natural images: Scaling in the woods. Phys. Rev. Lett. 73, 814–817 (1994).

    Article  ADS  CAS  Google Scholar 

  20. Carter-Dawson, L. D. & LaVail, M. M. Rods and cones in the mouse retina. I. Structural analysis using lights and electron microscopy. J. Comp. Neurol. 188, 245–262 (1979).

    Article  CAS  Google Scholar 

  21. Penn, J. S. & Williams, T. P. A new microspectrophotometric method for measuring absorbance of rat photoreceptors. Vision Res. 24, 1673–1676 (1984).

    Article  CAS  Google Scholar 

  22. Soucy, E., Wang, Y., Nirenberg, S., Nathans, J. & Meister, M. A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina. Neuron 21, 481–493 (1998).

    Article  CAS  Google Scholar 

  23. Dodd, R. L. in Program in Neurosciences 153–156 (Stanford Univ., Palo Alto, 1988).

    Google Scholar 

  24. Nirenberg, S. & Meister, M. The light response of retinal ganglion cells is truncated by a displaced amacrine circuit. Neuron 18, 637–650 (1997).

    Article  CAS  Google Scholar 

  25. 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 

  26. Bialek, W., Rieke, F., de Ruyter van Steveninck, R. R. & Warland, D. Reading a neural code. Science 252, 1854–1857 (1991).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank J. Assad, A. Pouget, T. Otis, D. Buonomano and M. Goldman for critical reviews of the manuscript. We also thank M. Jack, J. Sinclair, F. Schweizer, J. Feldman and M. Meister for helpful discussion. This work was supported by grants from the Beckman Foundation and the Klingenstein Fund (S.N.).

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Nirenberg, S., Carcieri, S., Jacobs, A. et al. Retinal ganglion cells act largely as independent encoders. Nature 411, 698–701 (2001). https://doi.org/10.1038/35079612

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