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Efficiency and ambiguity in an adaptive neural code

Abstract

We examine the dynamics of a neural code in the context of stimuli whose statistical properties are themselves evolving dynamically. Adaptation to these statistics occurs over a wide range of timescales—from tens of milliseconds to minutes. Rapid components of adaptation serve to optimize the information that action potentials carry about rapid stimulus variations within the local statistical ensemble, while changes in the rate and statistics of action-potential firing encode information about the ensemble itself, thus resolving potential ambiguities. The speed with which information is optimized and ambiguities are resolved approaches the physical limit imposed by statistical sampling and noise.

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Figure 1: Variance-switching experiment.
Figure 2: Input/output relations from the switching experiment.
Figure 3: Time dependence of the information transmission.
Figure 4: A stimulus with randomly modulated variance.
Figure 5: Discrimination using the statistics of interspike intervals in a switching experiment.

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References

  1. Attneave, F. Some informational aspects of visual perception. Psych. Rev. 61, 183–193 (1954).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  3. Laughlin, S. B. A simple coding procedure enhances a neuron's information capacity. Z. Naturforsch. 36c, 910–912 (1981).

    Article  Google Scholar 

  4. Rieke, F., Warland, D., de Ruyter van Steveninck, R. & Bialek, W. Spikes: Exploring the Neural Code (MIT Press, Cambridge, Massachusetts, 1997).

    MATH  Google Scholar 

  5. Berry, M. J., Warland, D. K. & Meister, M. The structure and precision of retinal spike trains. Proc. Natl Acad. Sci. USA 94, 5411–5416 (1997).

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  8. Smirnakis, S., Berry, M. J., Warland, D., Bialek, W. & Meister, M. Adaptation of retinal processing to image contrast and spatial scale. Nature 386, 67–73 (1997).

    Article  ADS  Google Scholar 

  9. de Ruyter van Steveninck, R. R., Bialek, W., Potters, M., Carlson, R. H. & Lewen, G. D. in Natural and Artificial Parallel Computation: Proc. of the Fifth NEC Res. Symp. (ed. Waltz, D. L.) 21–41 (SIAM, Philadelphia, 1996).

    Google Scholar 

  10. Brenner, N., Bialek, W. & de Ruyter van Steveninck, R. Adaptive rescaling maximizes information transmission. Neuron 26, 695–702 (2000).

    Article  CAS  Google Scholar 

  11. Wainwright, M. Visual adaptation as optimal information transmission. Vision Res. 39, 3960–3974 (1999).

    Article  CAS  Google Scholar 

  12. Francheschini, N., Riehle, A. & le Nestour, A. in Facets of Vision (eds Hardie, R. C. & Stavenga, D. G.) 360–390 (Springer, Berlin, 1989).

    Book  Google Scholar 

  13. Hausen, K. in Photoreception and Vision in Invertebrates (eds Ali, M.) 523–559 (Plenum, New York, 1984).

    Book  Google Scholar 

  14. Schilstra, C. & van Hateren, J. H. Blowfly flight and optic flow. I. Thorax kinematics and flight dynamics. J. Exp. Biol. 202, 1481–1490 (1999).

    PubMed  Google Scholar 

  15. Land, M. F. & Collett, T. S. Chasing behaviour of houseflies (Fannia canicularis). J. Comp. Physiol. 89, 331–357 (1974).

    Article  Google Scholar 

  16. Clague, H., Theunissen, F. & Miller, J. P. Effects of adaptation on neural coding by primary sensory interneurons in the cricket cercal system. J. Neurophysiol. 77, 207–220 (1997).

    Article  CAS  Google Scholar 

  17. Fairhall, A. L., Lewen, G., Bialek, W. & de Ruyter van Steveninck, R. R. in Advances in Neural Information Processing Systems 13 (eds Leen, T. K., Dietterich, T. G. & Tresp, V.) 124–130 (MIT Press, Cambridge, Massachusetts, 2001).

    Google Scholar 

  18. Thorson, J. & Biederman-Thorson, M. Distributed relaxation processes in a sensory adaptation. Science 183, 161–172 (1974).

    Article  ADS  CAS  Google Scholar 

  19. de Ruyter van Steveninck, R., Zaagman, W. H. & Mastebroek, H. A. K. Adaptation of transient responses of a movement-sensitive neuron in the visual system of the blowfly Calliphora erythrocephala. Biol. Cybern. 54, 223–226 (1986).

    Article  Google Scholar 

  20. Borst, A. & Egelhaaf, M. Temporal modulation of luminance adapts time constant of fly movement detectors. Biol. Cybern. 56, 209–215 (1987).

    Article  Google Scholar 

  21. van Hateren, J. H. Theoretical predictions of spatiotemporal receptive fields of fly LMCs, and experimental validation. J. Comp. Physiol. A 171, 157–170 (1992).

    Article  Google Scholar 

  22. Warland, D. Reading Between the Spikes: Real-time Processing in Neural Systems. Thesis, Univ. California at Berkeley (1991).

    Google Scholar 

  23. 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 

  24. Schneidman, E., Brenner, N., Tishby, N., de Ruyter van Steveninck, R. & Bialek, W. in Advances in Neural Information Processing Systems 13 (eds Leen, T. K., Dietterich, T. G. & Tresp, V.) 159–165 (MIT Press, Cambridge, Massachusetts, 2001).

    Google Scholar 

  25. deWeese, M. & Zador, A. Asymmetric dynamics in optimal variance adaptation. Neural Comp. 10, 1179–1202 (1998).

    Article  Google Scholar 

  26. 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 

  27. Nelken, I., Rotman, Y. & Yosef, O. B. Response of auditory-cortex neurons to structural features of natural sounds. Nature 397, 154–156 (1999).

    Article  ADS  CAS  Google Scholar 

  28. Hopfield, J. J. Transforming neural computations and representing time. Proc. Natl Acad. Sci. USA 93, 15440–15444 (1996).

    Article  ADS  CAS  Google Scholar 

  29. de Ruyter van Steveninck, R. & Bialek, W. Real-time performance of a movement sensitive in the blowfly visual system: information transfer in short spike sequences. Proc. R. Soc. Lond. Ser. B 234, 379–414 (1988).

    Article  ADS  Google Scholar 

  30. Perkel, D. & Bullock, T. H. Neural coding: a report based on an NRP work session. Neurosci. Res. Prog. Bull. 6, 3 (1968).

    Google Scholar 

  31. Wang, Y. & Wang, W. D. Information coding via spontaneous oscillations in neural ensembles. Phys. Rev. E 62, 1063–1068 (2000).

    Article  ADS  CAS  Google Scholar 

  32. Toib, A., Lyakhov, V. & Marom, S. Interaction between duration of activity and time course of recovery from slow inactivation in mammalian brain Na+ channels. J. Neurosci. 18, 1893–1903 (1998).

    Article  CAS  Google Scholar 

  33. Segundo, J. P., Moore, G. P., Stensaas, L. J. & Bullock, T. J. Sensitivity of the neurones in Aplysia to temporal pattern of arriving impulses. J. Exp. Biol. 40, 643–667 (1963).

    CAS  PubMed  Google Scholar 

  34. Markram, H., Gupta, A., Uziel, A., Wang, Y. & Tsodyks, M. Information processing with frequency-dependent synaptic connections. Neurobiol. Learn. Mem. 70, 101–112 (1998).

    Article  CAS  Google Scholar 

  35. Gerstner, W., Kreiter, A., Markram, H. & Herz, A. Neural codes: firing rates and beyond. Proc. Natl Acad. Sci. USA 94, 12740–12741 (1997).

    Article  ADS  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  37. Shapley, R. M. & Victor, J. D. The contrast gain control of the cat retina. Vision Res. 19, 431–434 (1979).

    Article  CAS  Google Scholar 

  38. Brown, S. & Masland, R. Spatial scale and cellular substrate of contrast adaptation by retinal ganglion cells. Nature Neurosci. 4, 44–51 (2001).

    Article  CAS  Google Scholar 

  39. Kim, K. J. & Rieke, F. Temporal contrast adaptation in the input and output signals of salamander retinal ganglion cells. J. Neurosci. 21, 287–299 (2001).

    Article  CAS  Google Scholar 

  40. Carandini, M., Heeger, D. J. & Movshon, J. A. Linearity and normalization in simple cells of the macaque primary visual cortex. J. Neurosci. 17, 8621–8644 (1997).

    Article  CAS  Google Scholar 

  41. Simoncelli, E. P. & Schwartz, O. in Advances in Neural Information Processing Systems 11 (eds Kearns, M. S., Solla, S. A. & Cohn, D. A.) 166–172 (MIT Press, Cambridge, Massachusetts, 1999).

    Google Scholar 

  42. Wiener, N. Extrapolation, Interpolation and Smoothing of Time Series (MIT Press, Cambridge, Massachusetts, 1949).

    MATH  Google Scholar 

  43. Feynman, R. P. & Hibbs, A. R. Path Integrals and Quantum Mechanics (McGraw Hill, New York, 1965).

    MATH  Google Scholar 

  44. Green, D. M. & Swets, J. A. Signal Detection Theory and Psychophysics (Wiley, New York, 1966).

    Google Scholar 

  45. de Ruyter van Steveninck, R. R. & Laughlin, S. B. The rate of information transfer at graded-potential synapses. Nature 379, 642–645 (1996).

    Article  ADS  CAS  Google Scholar 

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Acknowledgements

We thank B. AgĂĽera y Arcas, T. Adelman and N. Brenner for discussions, and R. Petersen and N. Ulanovsk for comments on the manuscript.

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Correspondence to Adrienne L. Fairhall.

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Fairhall, A., Lewen, G., Bialek, W. et al. Efficiency and ambiguity in an adaptive neural code. Nature 412, 787–792 (2001). https://doi.org/10.1038/35090500

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