When are correlations strong

The inverse problem of statistical mechanics involves finding the minimal Hamiltonian that is consistent with some observed set of correlation functions. This problem has received renewed interest in the analysis of biological networks; in particular, several such networks have been described successfully by maximum entropy models consistent with pairwise correlations. These correlations are usually weak in an absolute sense (e.g., correlation coefficients ~ 0.1 or less), and this is sometimes taken as evidence against the existence of interesting collective behavior in the network. If correlations are weak, it should be possible to capture their effects in perturbation theory, so we develop an expansion for the entropy of Ising systems in powers of the correlations, carrying this out to fourth order. We then consider recent work on networks of neurons [Schneidman et al., Nature 440, 1007 (2006); Tkacik et al., arXiv:0912.5409 [q-bio.NC] (2009)], and show that even though all pairwise correlations are weak, the fact that these correlations are widespread means that their impact on the network as a whole is not captured in the leading orders of perturbation theory. More positively, this means that recent successes of maximum entropy approaches are not simply the result of correlations being weak.

[1]  E. Adrian,et al.  The impulses produced by sensory nerve endings , 1926, The Journal of physiology.

[2]  E. Adrian,et al.  The impulses produced by sensory nerve‐endings , 1926 .

[3]  E. Jaynes Information Theory and Statistical Mechanics , 1957 .

[4]  W. A. Clark,et al.  Simultaneous Studies of Firing Patterns in Several Neurons , 1964, Science.

[5]  G. P. Moore,et al.  Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. , 1967, Biophysical journal.

[6]  Daniel J. Amit,et al.  Modeling brain function: the world of attractor neural networks, 1st Edition , 1989 .

[7]  John J. Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities , 1999 .

[8]  R. Ranganathan,et al.  Evolutionarily conserved pathways of energetic connectivity in protein families. , 1999, Science.

[9]  Gürol M. Süel,et al.  Evolutionarily conserved networks of residues mediate allosteric communication in proteins , 2003, Nature Structural Biology.

[10]  Gürol M. Süel,et al.  Evolutionarily conserved networks of residues mediate allosteric communication in proteins , 2003, Nature Structural Biology.

[11]  Michael J. Berry,et al.  Network information and connected correlations. , 2003, Physical review letters.

[12]  Michael J. Berry,et al.  Recording spikes from a large fraction of the ganglion cells in a retinal patch , 2004, Nature Neuroscience.

[13]  E. Chichilnisky,et al.  30 mu m spacing 519-electrode arrays for in vitro retinal studies , 2005 .

[14]  J.P. Donoghue,et al.  Reliability of signals from a chronically implanted, silicon-based electrode array in non-human primate primary motor cortex , 2005, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[15]  Michael J. Berry,et al.  Redundancy in the Population Code of the Retina , 2005, Neuron.

[16]  W. P. Russ,et al.  Natural-like function in artificial WW domains , 2005, Nature.

[17]  W. P. Russ,et al.  Evolutionary information for specifying a protein fold , 2005, Nature.

[18]  Michael J. Berry,et al.  Ising models for networks of real neurons , 2006, q-bio/0611072.

[19]  Michael J. Berry,et al.  Weak pairwise correlations imply strongly correlated network states in a neural population , 2005, Nature.

[20]  A. Maritan,et al.  Using the principle of entropy maximization to infer genetic interaction networks from gene expression patterns , 2006, Proceedings of the National Academy of Sciences.

[21]  Jonathon Shlens,et al.  The Structure of Multi-Neuron Firing Patterns in Primate Retina , 2006, The Journal of Neuroscience.

[22]  Gašper Tkačik,et al.  Information flow in biological networks , 2007 .

[23]  W. Bialek,et al.  Rediscovering the power of pairwise interactions , 2007, 0712.4397.

[24]  Robert E. Schapire,et al.  Faster solutions of the inverse pairwise Ising problem , 2008 .

[25]  M. A. Smith,et al.  Spatial and Temporal Scales of Neuronal Correlation in Primary Visual Cortex , 2008, The Journal of Neuroscience.

[26]  John M. Beggs,et al.  A Maximum Entropy Model Applied to Spatial and Temporal Correlations from Cortical Networks In Vitro , 2008, The Journal of Neuroscience.

[27]  Michael J. Berry,et al.  Spin glass models for a network of real neurons , 2009, 0912.5409.

[28]  Thierry Mora,et al.  Constraint satisfaction problems and neural networks: A statistical physics perspective , 2008, Journal of Physiology-Paris.

[29]  T. Hwa,et al.  Identification of direct residue contacts in protein–protein interaction by message passing , 2009, Proceedings of the National Academy of Sciences.

[30]  Najeeb M. Halabi,et al.  Protein Sectors: Evolutionary Units of Three-Dimensional Structure , 2009, Cell.

[31]  Peter E. Latham,et al.  Pairwise Maximum Entropy Models for Studying Large Biological Systems: When They Can Work and When They Can't , 2008, PLoS Comput. Biol..

[32]  R. Monasson,et al.  Small-correlation expansions for the inverse Ising problem , 2008, 0811.3574.

[33]  W. Bialek,et al.  Maximum entropy models for antibody diversity , 2009, Proceedings of the National Academy of Sciences.

[34]  W. Bialek,et al.  Statistical mechanics of letters in words. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  W. Bialek,et al.  Are Biological Systems Poised at Criticality? , 2010, 1012.2242.