Skip to main content

Advertisement

Log in

Characterizing the fine structure of a neural sensory code through information distortion

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

We present an application of the information distortion approach to neural coding. The approach allows the discovery of neural symbols and the corresponding stimulus space of a neuron or neural ensemble simultaneously and quantitatively, making few assumptions about the nature of either code or relevant features. The neural codebook is derived by quantizing sensory stimuli and neural responses into small reproduction sets, and optimizing the quantization to minimize the information distortion function. The application of this approach to the analysis of coding in sensory interneurons involved a further restriction of the space of allowed quantizers to a smaller family of parametric distributions. We show that, for some cells in this system, a significant amount of information is encoded in patterns of spikes that would not be discovered through analyses based on linear stimulus-response measures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Aldworth, Z. N. (2007). Characterization of the neural codebook in an invertebrate sensory system. PhD thesis, Montana State University, Bozeman.

  • Baba, Y., Hirota, K., & Yamaguchi, T. (1991). Morphology and response properties of wind-sensitive non-giant interneurons in the terminal abdominal ganglion of crickets. Zoological Science, 8, 437–445.

    Google Scholar 

  • Barlow, H. B. (1961). Possible princilples underlying the transformation of sensory messages. In W. A. Rosenblith, (Ed.), Sensory communications. Cambridge: MIT Press.

    Google Scholar 

  • Bialek, W., de Ruyter van Steveninck, R. R., & Tishby, N. (2006). Efficient representation as a design principle for neural coding and computation. In 2006 IEEE international symposium on information theory (pp. 659–663).

  • Biernacki, C., Celeux, G., Govaert, G., & Langrognet, F. (2006). Model-based cluster and discriminant analysis with the mixmod software. Computational Statistics & Data Analysis, 51/2, 587–600.

    Article  Google Scholar 

  • Bishop, C. M. (1998). Neural networks for pattern recognition. New York: Oxford University Press.

    Google Scholar 

  • Bodnar, D., Miller, J. P., & Jacobs, G. A. (1991). Anatomy and physiology of identified wind-sensitive local interneurons in the cricket cercal sensory system. Journal of Comparative Physiology A, 168, 553–564.

    Article  CAS  Google Scholar 

  • Buhler, J., & Tompa, M. (2001). Finding motifs using random projections. In Proceedings of the fifth annual international conference on computational biology (pp. 69–76). New York: ACM.

    Google Scholar 

  • Chechick, G., Globerson, A., Tishby, N., Anderson, M., Young, E. D., & Nelken, I. (2002). Group redundancy measures reveals redundancy reduction in the auditory pathway. In T. G. Dietterich, S. Becker, & Z. Ghahramani, (Eds.) Advances in neural information processing systems (Vol. 14, pp. 173–180). Cambridge: MIT.

    Google Scholar 

  • Clague, H., Theunissen, F., & Miller, J. P. (1997). The effects of adaptation on neural coding by primary sensor interneurons in the cricket cercal system. Journal of Neurophysiology, 77, 207–220.

    CAS  PubMed  Google Scholar 

  • Cover, T., & Thomas, J. (1991). Elements of information theory. New York: Wiley.

    Book  Google Scholar 

  • Dhillon, I. S., Mallela, S., & Modha, D. S. (2003). Information-theoretic co-clustering. In The ninth ACM SIGKDD international conference on knowledge discovery and data mining (KDD 03) (pp. 89–98). New York: ACM.

    Chapter  Google Scholar 

  • Dimitrov, A. G., & Miller, J. P. (2001). Neural coding and decoding: communication channels and quantization. Network: Computation in Neural Systems, 12, 441–472.

    CAS  Google Scholar 

  • Dimitrov, A. G., Miller, J. P., Gedeon, T., Aldworth, Z., & Parker, A. E. (2003). Analysis of neural coding through quantization with an information-based distortion measure. Network: Computation in Neural Systems, 14, 151–176.

    Google Scholar 

  • Efron, B., & Tibshirani, R. J. (1993). An Introduction to the bootstrap. Monographs on Statistics & Applied Probability. New York: Chapman & Hall/CRC.

    Google Scholar 

  • Gedeon, T., Parker, A. E., & Dimitrov, A. G. (2003). Information distortion and neural coding. Canadian Applied Mathematics Quarterly, 10, 33–70.

    Google Scholar 

  • Gersho, A., & Gray, R. M. (1992). Vector quantization and signal compression. Kluwer.

  • Gnatzy, W., & Heusslein, R. (1986). Digger wasp against crickets. I. Receptors involved in the antipredator strategies of the prey. Naturwissenschaften, 73, 212–215.

    Article  Google Scholar 

  • Heinzel, H. G., & Dambach, M. (1987) Traveling air vortex rings as potential communication signals in a cricket. Journal of Comparative Physiology A, 160, 79–88.

    Article  Google Scholar 

  • Hirota, K., Sonoda, Y., Baba, Y., & Yamaguchi, T. (1993). Distinction in morphology and behavioral role between dorsal and ventral groups of cricket giant interneurons. Zoological Science, 10(4), 705–709.

    Google Scholar 

  • Jacobs, G. A., Miller, J. P., & Aldworth, Z. (2008). Computational mechanisms of mechanosensory processing in the cricket. Journal of Experimental Biology, 211(11), 1819–1828.

    Article  PubMed  Google Scholar 

  • Jacobs, G. A., & Murphey, R. K. (1987). Segmental origins of the cricket giant interneuron system. Journal of Comparative Neurology, 265, 145–157.

    Article  CAS  PubMed  Google Scholar 

  • Jaynes, E. T. (1982). On the rationale of maximum-entropy methods. Proceedings of the IEEE, 70, 939–952.

    Article  Google Scholar 

  • Johnson, D. H., Gruner, C. M., Baggerly, K., & Seshagiri, C. (2001). Information-theoretic analysis of the neural code. Journal of Computational Neuroscience, 10(1), 47–70.

    Article  CAS  PubMed  Google Scholar 

  • Kamper, G., & Kleindienst, H.-U. (1990). Oscillation of cricket sensory hairs in a low frequency sound field. Journal of Comparative Physiology A, 167, 193–200.

    Article  Google Scholar 

  • Kanou, M., & Shimozawa, T. A. (1984). Threshold analysis of cricket cercal interneurons by an alternating air-current stimulus. Journal of Comparative Physiology A, 154, 357–365.

    Article  Google Scholar 

  • Kass, R. E., Ventura, V., & Brown, E. N. (2005). Statistical issues in the analysis of neural data. Journal of Neurophysiology, 94, 8–25.

    Article  PubMed  Google Scholar 

  • Kjaer, T. W., Hertz, J. A., & Richmond, B. J. (1994). Decoding cortical neuronal signals: Network models, information estimation and spatial tuning. Journal of Computational Neuroscience, 1(1–2), 109–139.

    Article  CAS  PubMed  Google Scholar 

  • Landolfa, M., & Jacobs, G. A. (1995). Direction sensitivity of the filiform hair population of the cricket cercal system. Journal of Comparative Physiology A, 177, 759–766.

    Google Scholar 

  • Landolfa, M. A., & Miller, J. P. (1995). Stimulus-response properties of cricket cercal filiform hair receptors. Journal of Comparative Physiology A, 177, 749–757.

    Google Scholar 

  • Marmarelis, P. Z., & Marmarelis, V. Z. (1978). The white noise method in system identification. In Analysis of physiological systems. New York: Plenum.

    Google Scholar 

  • Miller, J. P., Jacobs, G. A., & Theunissen, F. E. (1991). Representation of sensory information in the cricket cercal sensory system. I. Response properties of the primary interneurons. Journal of Neurophysiology, 66, 1680–1689.

    CAS  PubMed  Google Scholar 

  • Mumey, B., Sarkar, A., Gedeon, T., Dimitrov, A. G., Miller, J. P. (2004). Finding neural codes using random projections. Neurocomputing, 58–60, 19–25.

    Article  Google Scholar 

  • Osborne, L. C. (1997). Biomechanical properties underlying sensory processing in mechanosensory hairs in the cricket cercal sensory system. PhD thesis, University of California, Berkeley.

  • Paninski, L., Pillow, J., & Simoncelli, E. (2005). Maximum likelihood estimation of a stochastic integrate-and-fire neural model. Neural Computation, 17, 1480–1507.

    Article  PubMed  Google Scholar 

  • Parker, A. E., Dimitrov, A. G., & Gedeon, T. (2010). Symmetry breaking in soft clustering decoding of neural codes. IEEE Transactions on Information Theory, 56(2), 901–927.

    Article  Google Scholar 

  • Pillow, J. W., Shlens, J., Paninski, L., Sher, A., Litke, A., Simoncelli, E., et al. (2008). Spatio-temporal correlations and visual signaling in a complete neuronal population. Nature, 454, 995–999.

    Article  CAS  PubMed  Google Scholar 

  • Pillow, J. W., & Simoncelli, E. P. (2006). Dimensionality reduction in neural models: An information-theoretic generalization of spike-triggered average and covariance analysis. Journal of Vision, 6, 414–428.

    Article  PubMed  Google Scholar 

  • Rieke, F., Warland, D., de Ruyter van Steveninck, R. R., & Bialek, W. (1997). Spikes: Exploring the neural code. MIT.

  • Roddey, J. C., Girish, B., & Miller, J. P. (2000). Assessing the performance of neural encoding models in the presence of noise. Journal of Computational Neuroscience, 8, 95–112.

    Article  CAS  PubMed  Google Scholar 

  • Roddey, J. C., & Jacobs, G. A. (1996). Information theoretic analysis of dynamical encoding by filiform mechanoreceptors in the cricket cercal system. Journal of Neurophysiology, 75, 1365–1376.

    CAS  PubMed  Google Scholar 

  • Rose, K. (1998). Deteministic annealing for clustering, compression, classification, regerssion, and related optimization problems. Proceedings of the IEEE, 86(11), 2210–2239.

    Article  Google Scholar 

  • Sakai, H. M. (1992). White-Noise Analysis in Neurophysiology. Physiological Reviews, 72, 491–505.

    CAS  PubMed  Google Scholar 

  • Schneidman, E., Brenner, N., Tishby, N., de Ruyter van Steveninck, R. R., & Bialek, W. (2000). Universality and individuality in a neural code. In NIPS (pp. 159–165).

  • Shamir, R., & Sharan, R. (2000). Click: A clustering algorithm with applications to gene expression analysis. In Proceedings of intelligent systems for molecular biology (ISMB) (pp. 307–316).

  • Shannon, C. E. (1948). A mathematical theory of communication. Bell System Technical Journal, 27, 623–656.

    Google Scholar 

  • Shimozawa, T., & Kanou, M. (1984a). The aerodynamics and sensory physiology of a range fractionation in the cercal filiform sensilla of the cricket gryllus bimaculatus. Journal of Comparative Physiology A, 155, 495–505.

    Article  Google Scholar 

  • Shimozawa, T., & Kanou, M. (1984b). Varieties of filiform hairs: Range fractionation by sensory afferents and cercal interneurons of a cricket. Journal of Comparative Physiology A, 155, 485–493.

    Article  Google Scholar 

  • Slonim, N., & Tishby, N. (2000). Agglomerative information bottleneck. In S. A. Solla, T. K. Leen, & K.-R. Müller, (Eds.), Advances in Neural Information Processing Systems (Vol. 12, pp. 617–623). MIT.

  • Stout, J. F., DeHaan, C. H., & McGhee, R. W. (1983). Attractiveness of the male acheta domesticus calling song to females. I. Dependence on each of the calling song features. Journal of Comparative Physiology, 153, 509–521.

    Article  Google Scholar 

  • Theunissen, F., Roddey, J. C., Stufflebeam, S., Clague, H., & Miller, J. P. (1996). Information theoretic analysis of dynamical encoding by four primary sensory interneurons in the cricket cercal system. Journal of Neurophysiology, 75, 1345–1359.

    CAS  PubMed  Google Scholar 

  • Theunissen, F. E., & Miller, J. P. (1991). Representation of sensory information in the cricket cercal sensory system. II. Information theoretic calculation of system accuracy and optimal tuning curve width of four primary interneurons. Journal of Neurophysiology, 66, 1690–1703.

    CAS  PubMed  Google Scholar 

  • Tishby, N., Pereira, F., & Bialek, W. (1999). The information bottleneck method. In Proceedings of The 37th annual Allerton conference on communication, control and computing. University of Illinois.

  • Victor, J. D. (1979). Nonlinear systems analysis: comparison of white noise and sum of sinusoids in biological systems. Proceedings of the National Academy of Sciences of the United States of America, 76(2), 996-998.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the two anonymous reviewers for their dedicated work and extremely useful comments that lead to the improvement of this article, and to Dr. John Miller for useful comments and hosting us at the Center for Computational Biology of Montana State University throughout most of the development of this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alexander G. Dimitrov.

Additional information

Action Editor: Aurel A. Lazar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dimitrov, A.G., Cummins, G.I., Baker, A. et al. Characterizing the fine structure of a neural sensory code through information distortion. J Comput Neurosci 30, 163–179 (2011). https://doi.org/10.1007/s10827-010-0261-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-010-0261-4

Keywords

Navigation