Sparse low-order interaction network underlies a highly correlated and learnable neural population code

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 23, 2011, Pages 9679-9684

  Ganmor, Elad ^a   Segev, Ronen ^b   Schneidman, Elad ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

Author keywords

Correlations; High order; Maximum entropy; Neural networks; Sparseness

Indexed keywords

ANIMAL CELL; ARTICLE; BRAIN FUNCTION; CELL ACTIVITY; CELL INTERACTION; CELL POPULATION; CONTROLLED STUDY; NERVE CELL NETWORK; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; RELIABILITY; RETINA NERVE CELL;

ALGORITHMS; AMBYSTOMA; ANIMALS; GANGLIA; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; PERCIFORMES; RETINA; RETINAL GANGLION CELLS; RETINAL NEURONS;

EID: 79959354385     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1019641108     Document Type: Article

References (45)

1. Perkel DH, Bullock TH (1968) Neural coding. Neurosci Res Prog Bull 6:221-348.
2. Georgopoulos AP, Schwartz AB, Kettner RE (1986) Neuronal population coding of movement direction. Science 233:1416-1419. (Pubitemid 17169374)
3. Rieke F, Warland D, de Ruyter van Steveninck RR, Bialek W (1997) Spikes: Exploring the Neural Code (MIT Press, Cambridge, MA).
4. Schnitzer MJ, Meister M (2003) Multineuronal firing patterns in the signal from eye to brain. Neuron 37:499-511. (Pubitemid 36183370)
5. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70-74. (Pubitemid 27494757)
6. Riehle A, Grün S, Diesmann M, Aertsen A (1997) Spike synchronization and rate modulation differentially involved in motor cortical function. Science 278:1950-1953. (Pubitemid 28013237)
7. Dan Y, Alonso JM, Usrey WM, Reid RC (1998) Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nat Neurosci 1:501-507.
8. Hatsopoulos NG, Ojakangas CL, Paninski L, Donoghue JP (1998) Information about movement direction obtained from synchronous activity of motor cortical neurons. Proc Natl Acad Sci USA 95:15706-15711. (Pubitemid 29018764)
9. Brown EN, Frank LM, Tang D, Quirk MC, Wilson MA (1998) A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J Neurosci 18:7411-7425. (Pubitemid 28425825)
10. Harris KD, Csicsvari J, Hirase H, Dragoi G, Buzsáki G (2003) Organization of cell assemblies in the hippocampus. Nature 424:552-556. (Pubitemid 36975776)
11. Averbeck BB, Lee D (2004) Coding and transmission of information by neural ensembles. Trends Neurosci 27:225-230. (Pubitemid 38376410)
12. Schneidman E, Bialek W, Berry MJ, 2nd (2003) Synergy, redundancy, and independence in population codes. J Neurosci 23:11539-11553.
13. Narayanan NS, Kimchi EY, Laubach M (2005) Redundancy and synergy of neuronal ensembles in motor cortex. J Neurosci 25:4207-4216. (Pubitemid 40628764)
14. Puchalla JL, Schneidman E, Harris RA, Berry MJ, 2nd (2005) Redundancy in the population code of the retina. Neuron 46:493-504. (Pubitemid 40616892)
15. Chechik G, et al. (2006) Reduction of information redundancy in the ascending auditory pathway. Neuron 51:359-368. (Pubitemid 44118713)
16. Huber D, et al. (2008) Sparse optical microstimulation in barrel cortex drives learned behaviour in freely moving mice. Nature 451:61-64.
17. Hopfield JJ, Tank DW (1986) Computing with neural circuits: A model. Science 233: 625-633. (Pubitemid 16011610)
18. LeMasson G, Marder E, Abbott LF (1993) Activity-dependent regulation of conductances in model neurons. Science 259:1915-1917. (Pubitemid 23124466)
19. Schneidman E, Berry MJ, 2nd, Segev R, Bialek W (2006) Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440:1007-1012.
20. Shlens J, et al. (2006) The structure of multi-neuron firing patterns in primate retina. J Neurosci 26:8254-8266. (Pubitemid 44309839)
21. Tkacik G, Schneidman E, Berry MJ, 2nd, Bialek W (2006) Ising models for networks of real neurons. arXiv:0611072 [q-bio].
22. Tang A, et al. (2008) A maximum entropy model applied to spatial and temporal correlations from cortical networks in vitro. J Neurosci 28:505-518.
23. Marre O, El Boustani S, Frégnac Y, Destexhe A (2009) Prediction of spatiotemporal patterns of neural activity from pairwise correlations. Phys Rev Lett 102:138101.
24. Shlens J, et al. (2009) The structure of large-scale synchronized firing in primate retina. J Neurosci 29:5022-5031.
25. Pillow JW, et al. (2008) Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature 454:995-999.
26. Martignon L, et al. (2000) Neural coding: Higher-order temporal patterns in the neurostatistics of cell assemblies. Neural Comput 12:2621-2653.
27. Ohiorhenuan IE, et al. (2010) Sparse coding and high-order correlations in fine-scale cortical networks. Nature 466:617-621.
28. Pearl J (1988) Probabilistic Reasoning in Intelligent Systems: Networks of Plausible Inference (Morgan Kaufmann, San Francisco).
29. Hinton GE, Osindero S, Teh YW (2006) A fast learning algorithm for deep belief nets. Neural Comput 18:1527-1554. (Pubitemid 44024729)
30. Swendsen RH, Wang JS (1987) Nonuniversal critical dynamics in Monte Carlo simulations. Phys Rev Lett 58:86-88.
31. Broderick T, Dudík M, Tkačik G, Schapire RE, Bialek W (2007) Faster solutions of the inverse pairwise Ising problem. arXiv:0712.2437 [q-bio.QM].
32. Cocco S, Leibler S, Monasson R (2009) Neuronal couplings between retinal ganglion cells inferred by efficient inverse statistical physics methods. Proc Natl Acad Sci USA 106:14058-14062.
33. Bethge M, Berens P (2008) Near-Maximum Entropy Models for Binary Neural Representations of Natural Images (MIT Press, Cambridge, MA), pp 97-104.
34. Olshausen BA, Field DJ (2004) Sparse coding of sensory inputs. Curr Opin Neurobiol 14:481-487. (Pubitemid 39078497)
35. Bair W, Zohary E, Newsome WT (2001) Correlated firing in macaque visual area MT: Time scales and relationship to behavior. J Neurosci 21:1676-1697. (Pubitemid 32182208)
36. Amari S (2001) Information geometry on hierarchy of probability distributions. IEEE Trans Inf Theory 47:1701-1711.
37. Schneidman E, Still S, Berry MJ, 2nd, Bialek W (2003) Network information and connected correlations. Phys Rev Lett 91:238701.
38. Besag J (1974) Spatial interaction and the statistical analysis of lattice systems. J R Stat Soc Series B Stat Methodol 36:192-236.
39. Besag J (1977) Efficiency of pseudolikelihood estimation for simple gaussian fields. Biometrika 64:616-618.
40. Santos GS, Gireesh ED, Plenz D, Nakahara H (2010) Hierarchical interaction structure of neural activities in cortical slice cultures. J Neurosci 30:8720-8733.
41. Ganmor E, Segev R, Schneidman E (2011) The architecture of functional interaction networks in the retina. J Neurosci 31:3044-3054.
42. Abbeel P, Koller D, Ng AY (2006) Learning factor graphs in polynomial time and sample complexity. J Mach Learn Res 7:1743-1788. (Pubitemid 44274019)
43. Barlow H (2001) Redundancy reduction revisited. Network 12:241-253.
44. Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193-1216. (Pubitemid 32695258)
45. Turrigiano G, Abbott LF, Marder E (1994) Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264:974-977. (Pubitemid 24196170)