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Searching for Collective Behavior in a Large Network of Sensory Neurons

Gašper Tkačik, Olivier Marre, Dario Amodei and 3 more

PLoS Computational Biology · 2014 · CC BY

doi:10.1371/journal.pcbi.1003408

Abstract

Maximum entropy models are the least structured probability distributions that exactly reproduce a chosen set of statistics measured in an interacting network. Here we use this principle to construct probabilistic models which describe the correlated spiking activity of populations of up to 120 neurons in the salamander retina as it responds to natural movies. Already in groups as small as 10 neurons, interactions between spikes can no longer be regarded as small perturbations in an otherwise independent system; for 40 or more neurons pairwise interactions need to be supplemented by a global interaction that controls the distribution of synchrony in the population. Here we show that such "K-pairwise" models--being systematic extensions of the previously used pairwise Ising models--provide an excellent account of the data. We explore the properties of the neural vocabulary by: 1) estimating its entropy, which constrains the population's capacity to represent visual information; 2) classifying activity patterns into a small set of metastable collective modes; 3) showing that the neural codeword ensembles are extremely inhomogenous; 4) demonstrating that the state of individual neurons is highly predictable from the rest of the population, allowing the capacity for error correction.

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References 113

  1. 1.

    Hopfield JJ (1982 ) Neural networks and physical systems with emergent collective computational abilities. Proc Natl Acad Sci (USA)79: 2554–8

    Not in our library10.1073/pnas.79.8.2554

  2. 2.

    Amit DJ (1989) Modeling Brain Function: The World of Attractor Neural Networks. Cambridge: Cambridge University Press.

    Not in our library

  3. 3.

    Hertz J, Krogh A & Palmer RG (1991) Introduction to the Theory of Neural Computation. Redwood City: Addison Wesley.

    Not in our library

  4. 4.

    Schneidman E, Berry MJ II, Segev R (2006 ) Bialek W (2006 ) Weak pairwise correlations imply strongly correlated network states in a neural population. Nature440: 1007–1012

    Not in our library10.1038/nature04701

  5. 5.

    Shlens J, Field GD, Gaulthier JL, Grivich MI, Petrusca D, Sher A, Litke AM (2006 ) Chichilnisky EJ (2006 ) The structure of multi-neuron firing patterns in primate retina. J Neurosci26: 8254–8266

    Not in our library10.1523/jneurosci.1282-06.2006

  6. 6.

    Tkačik G, Schneidman E, Berry MJ II & Bialek W (2006) Ising models for networks of real neurons. arXiv.org: q-bio/0611072.

    Not in our library

  7. 7.

    Yu S, Huang D, Singer W (2008 ) Nikolic D (2008 ) A small world of neuronal synchrony. Cereb Cortex18: 2891–2901

    Not in our library10.1093/cercor/bhn047

  8. 8.

    Tang A, Jackson D, Hobbs J, Chen W, Smith JL, Patel H, Prieto A, Petruscam D, Grivich MI, Sher A, Hottowy P, Dabrowski W, Litke AM (2008 ) Beggs JM (2008 ) A maximum entropy model applied to spatial and temporal correlations from cortical networks in vitro. J Neurosci28: 505–518

    Not in our library10.1523/jneurosci.3359-07.2008

  9. 9.

    Tkačik G, Schneidman E, Berry MJ II & Bialek W (2009) Spin–glass models for a network of real neurons. arXiv.org: 0912.5409.

    Not in our library

  10. 10.

    Shlens J, Field GD, Gaulthier JL, Greschner M, Sher A, Litke AM (2009 ) Chichilnisky EJ (2009 ) The structure of large–scale synchronized firing in primate retina. J Neurosci29: 5022–5031

    Not in our library10.1523/jneurosci.5187-08.2009

  11. 11.

    Ohiorhenuan IE, Mechler F, Purpura KP, Schmid AM, Hu Q (2010 ) Victor JD (2010 ) Sparse coding and higher–order correlations in fine–scale cortical networks. Nature466: 617–621

    Not in our library10.1038/nature09178

  12. 12.

    Ganmor E, Segev R (2011 ) Schniedman E (2011 ) Sparse low–order interaction network underlies a highly correlated and learnable neural population code. Proc Natl Acad Sci (USA)108: 9679–9684

    Not in our library10.1073/pnas.1019641108

  13. 13.

    Vasquez JC, Marre O, Palacios AG, Berry MJ II (2012 ) Cessac B (2012 ) Gibbs distribution analysis of temporal correlations structure in retina ganglion cells. J Physiol Paris3–4: 120–127

    Not in our library10.1016/j.jphysparis.2011.11.001

  14. 14.

    Granot-Atedgi E, Tkačik G, Segev R (2013 ) Schneidman E (2013 ) Stimulus-dependent maximum entropy models of neural population codes. PLoS Comput Biol9: e1002922

    Not in our library10.1371/journal.pcbi.1002922

  15. 15.

    Ganmor E, Segev R (2011 ) Schneidman E (2011 ) The architecture of functional interaction networks in the retina. J Neurosci31: 3044–3054

    Not in our library10.1523/jneurosci.3682-10.2011

  16. 16.

    Tkačik G, Prentice JS, Victor JD (2010 ) Balasubramanian V (2010 ) Local statistics in natural scenes predict the saliency of synthetic textures. Proc Natl Acad Sci (USA)107: 18149–18154

    Not in our library10.1073/pnas.0914916107

  17. 17.

    Stephens GJ, Mora T, Tkačik G (2013 ) Bialek W (2013 ) Statistical thermodynamics of natural images. Phys Rev Lett110: 018701

    Not in our library10.1103/physrevlett.110.018701

  18. 18.

    Saremi S (2013 ) Sejnowski TJ (2013 ) Hierarchical model of natural images and the origin of scale invariance. Proc Natl Acad Sci (USA)110: 3071–3076

    Not in our library10.1073/pnas.1222618110

  19. 19.

    Lezon TR, Banavar JR, Cieplak M, Maritan A (2006 ) Federoff NV (2006 ) Using the principle of entropy maximization to infer genetic interaction networks from gene expression patterns. Proc Natl Acad Sci (USA)103: 19033–19038

    Not in our library10.1073/pnas.0609152103

  20. 20.

    Tkačik G (2007 ) Information Flow in Biological Networks. Dissertation, Princeton University

    Not in our library

  21. 21.

    Bialek W & Ranganathan R (2007) Rediscovering the power of pairwise interactions. arXiv.org: 0712.4397.

    Not in our library

  22. 22.

    Seno F, Trovato A, Banavar JR (2008 ) Maritan A (2008 ) Maximum entropy approach for deducing amino acid interactions in proteins. Phys Rev Lett100: 078102

    Not in our library10.1103/physrevlett.100.078102

  23. 23.

    Weigt M, White RA, Szurmant H, Hoch JA (2009 ) Hwa T (2009 ) Identification of direct residue contacts in protein–protein interaction by message passing. Proc Natl Acad Sci (USA)106: 67–72

    Not in our library10.1073/pnas.0805923106

  24. 24.

    Halabi N, Rivoire O, Leibler S (2009 ) Ranganathan R (2009 ) Protein sectors: Evolutionary units of three–dimensional structure. Cell138: 774–786

    Not in our library10.1016/j.cell.2009.07.038

  25. 25.

    Mora T, Walczak AM, Bialek W (2010 ) Callan CG Jr (2010 ) Maximum entropy models for antibody diversity. Proc Natl Acad Sci (USA)107: 5405–5410

    Not in our library10.1073/pnas.1001705107

  26. 26.
  27. 27.

    Sulkowska JI, Morocos F, Weigt M, Hwa T (2012 ) Onuchic JN (2012 ) Genomics–aided structure prediction. Proc Natl Acad Sci (USA)109: 10340–10345

    Not in our library10.1073/pnas.1207864109

  28. 28.

    Stephens GJ (2010 ) Bialek W (2010 ) Statistical mechanics of letters in words. Phys Rev E81: 066119

    Not in our library10.1103/physreve.81.066119

  29. 29.

    Bialek W, Cavagna A, Giardina I, Mora T, Silvestri E, Viale M (2012 ) Walczak A (2012 ) Statistical mechanics for natural flocks of birds. Proc Natl Acad Sci (USA)109: 4786–4791

    Not in our library10.1073/pnas.1118633109

  30. 30.
  31. 31.

    Mora T (2010 ) Bialek W (2010 ) Are biological systems poised at criticality?J Stat Phys144: 268–302

    Not in our library

  32. 32.

    Nirenberg S (2007 ) Victor J (2007 ) Analyzing the activity of large populations of neurons: How tractable is the problem. Curr Opin Neurobiol17: 397–400

    Not in our library10.1016/j.conb.2007.07.002

  33. 33.

    Roudi Y, Aurell E (2009 ) Hertz JA (2009 ) Statistical physics of pairwise probability models. Front Comput Neurosci3: 22

    Not in our library10.3389/neuro.10.022.2009

  34. 34.

    Roudi Y, Nirenberg S (2009 ) Latham PE (2009 ) Pairwise maximum entropy models for studying large biological systems: when they can work and when they can't. PLoS Comput Biol5: e1000380

    Not in our library10.1371/journal.pcbi.1000380

  35. 35.

    Roudi Y, Trycha J (2009 ) Hertz J (2009 ) The Ising model for neural data: model quality and approximate methods for extracting functional connectivity. Phys Rev E79: 051915

    Not in our library10.1103/physreve.79.051915

  36. 36.

    Marre O, Amodei D, Deshmukh N, Sadeghi K, Soo F, Holy TE (2012 ) Berry MJ II (2012 ) Mapping a complete neural population in the retina. J Neurosci32: 14859–14873

    Not in our library10.1523/jneurosci.0723-12.2012

  37. 37.

    Broderick T, Dudik M, Tkačik, G Schapire RE & Bialek W (2007) Faster solutions of the inverse pairwise Ising problem. arXiv.org: 0712.2437.

    Not in our library

  38. 38.

    Treves A, Panzeri S, Rolls ET, Booth M (1999 ) Wakeman EA (1999 ) Firing rate distributions and efficiency of information transmission in inferior temporal cortex neurons to natural visual stimuli. Neural Comput11: 601–631

    Not in our library10.1162/089976699300016593

  39. 39.

    Tkačik G, Marre O, Mora T, Amodei D, Berry MJ II (2013 ) Bialek W (2013 ) The simplest maximum entropy model for collective behavior in a neural network. J Stat MechP03011

    Not in our library

  40. 40.

    Okun M, Yger P, Marguet SL, Gerard-Mercier F, Benucci A, Katzner S, Busse L, Carandini M (2012 ) Harris KD (2012 ) Population rate dynamics and multi neuron firing patterns in sensory cortex. J Neurosci32: 17108–17119

    Not in our library10.1523/jneurosci.1831-12.2012

All 113 references

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