Undersampled Critical Branching Processes on Small-World and Random Networks Fail to Reproduce the Statistics of Spike Avalanches

The power-law size distributions obtained experimentally for neuronal avalanches are an important evidence of criticality in the brain. This evidence is supported by the fact that a critical branching process exhibits the same exponent . Models at criticality have been employed to mimic avalanche propagation and explain the statistics observed experimentally. However, a crucial aspect of neuronal recordings has been almost completely neglected in the models: undersampling. While in a typical multielectrode array hundreds of neurons are recorded, in the same area of neuronal tissue tens of thousands of neurons can be found. Here we investigate the consequences of undersampling in models with three different topologies (two-dimensional, small-world and random network) and three different dynamical regimes (subcritical, critical and supercritical). We found that undersampling modifies avalanche size distributions, extinguishing the power laws observed in critical systems. Distributions from subcritical systems are also modified, but the shape of the undersampled distributions is more similar to that of a fully sampled system. Undersampled supercritical systems can recover the general characteristics of the fully sampled version, provided that enough neurons are measured. Undersampling in two-dimensional and small-world networks leads to similar effects, while the random network is insensitive to sampling density due to the lack of a well-defined neighborhood. We conjecture that neuronal avalanches recorded from local field potentials avoid undersampling effects due to the nature of this signal, but the same does not hold for spike avalanches. We conclude that undersampled branching-process-like models in these topologies fail to reproduce the statistics of spike avalanches.

[1]  T. E. Harris,et al.  The Theory of Branching Processes. , 1963 .

[2]  S. Hastings,et al.  Spatial Patterns for Discrete Models of Diffusion in Excitable Media , 1978 .

[3]  Tang,et al.  Self-Organized Criticality: An Explanation of 1/f Noise , 2011 .

[4]  A. Fisher,et al.  The Theory of Critical Phenomena: An Introduction to the Renormalization Group , 1992 .

[5]  Drossel,et al.  Self-organized critical forest-fire model. , 1992, Physical review letters.

[6]  Stanley,et al.  Self-organized branching processes: Mean-field theory for avalanches. , 1995, Physical review letters.

[7]  Duncan J. Watts,et al.  Collective dynamics of ‘small-world’ networks , 1998, Nature.

[8]  R. Dickman,et al.  Nonequilibrium Phase Transitions in Lattice Models , 1999 .

[9]  A Vespignani,et al.  Avalanche and spreading exponents in systems with absorbing states. , 1999, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[10]  Mauro Copelli,et al.  Physics of psychophysics: Stevens and Weber-Fechner laws are transfer functions of excitable media. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  John M. Beggs,et al.  Neuronal Avalanches in Neocortical Circuits , 2003, The Journal of Neuroscience.

[12]  M. Lavine,et al.  Long-Lasting Novelty-Induced Neuronal Reverberation during Slow-Wave Sleep in Multiple Forebrain Areas , 2004, PLoS biology.

[13]  G. Buzsáki Large-scale recording of neuronal ensembles , 2004, Nature Neuroscience.

[14]  Mauro Copelli,et al.  Signal compression in the sensory periphery , 2005, Neurocomputing.

[15]  John M Beggs,et al.  Critical branching captures activity in living neural networks and maximizes the number of metastable States. , 2005, Physical review letters.

[16]  O. Kinouchi,et al.  Intensity coding in two-dimensional excitable neural networks , 2004, q-bio/0409032.

[17]  Mauro Copelli,et al.  Response of electrically coupled spiking neurons: a cellular automaton approach. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[18]  L. de Arcangelis,et al.  Self-organized criticality model for brain plasticity. , 2006, Physical review letters.

[19]  O. Kinouchi,et al.  Optimal dynamical range of excitable networks at criticality , 2006, q-bio/0601037.

[20]  M. Copelli,et al.  Excitable scale free networks , 2007, q-bio/0703004.

[21]  V. Torre,et al.  On the Dynamics of the Spontaneous Activity in Neuronal Networks , 2007, PloS one.

[22]  J. M. Herrmann,et al.  Dynamical synapses causing self-organized criticality in neural networks , 2007, 0712.1003.

[23]  Viola Priesemann,et al.  Subsampling effects in neuronal avalanche distributions recorded in vivo , 2009, BMC Neuroscience.

[24]  R. E. Crist,et al.  Multielectrode Recording in Behaving Monkeys , 2008 .

[25]  L. L. Bologna,et al.  Self-organization and neuronal avalanches in networks of dissociated cortical neurons , 2008, Neuroscience.

[26]  Mauro Copelli,et al.  Dynamic range of hypercubic stochastic excitable media. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  M. Copelli,et al.  Deterministic excitable media under Poisson drive: power law responses, spiral waves, and dynamic range. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  D. Plenz,et al.  Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3 , 2008, Proceedings of the National Academy of Sciences.

[29]  Woodrow L. Shew,et al.  Neuronal Avalanches Imply Maximum Dynamic Range in Cortical Networks at Criticality , 2009, The Journal of Neuroscience.

[30]  Antonio C. Roque,et al.  A Computational Study on the Role of Gap Junctions and Rod Ih Conductance in the Enhancement of the Dynamic Range of the Retina , 2009, PloS one.

[31]  J. M. Herrmann,et al.  Phase transitions towards criticality in a neural system with adaptive interactions. , 2009, Physical review letters.

[32]  D. Plenz,et al.  Spontaneous cortical activity in awake monkeys composed of neuronal avalanches , 2009, Proceedings of the National Academy of Sciences.

[33]  D. Chialvo Emergent complex neural dynamics , 2010, 1010.2530.

[34]  D. B. Leitch,et al.  Neuron densities vary across and within cortical areas in primates , 2010, Proceedings of the National Academy of Sciences.

[35]  M. Nicolelis,et al.  Spike Avalanches Exhibit Universal Dynamics across the Sleep-Wake Cycle , 2010, PloS one.

[36]  L. de Arcangelis,et al.  Learning as a phenomenon occurring in a critical state , 2010, Proceedings of the National Academy of Sciences.

[37]  Tânia Tomé,et al.  Critical behavior of the susceptible-infected-recovered model on a square lattice. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[38]  Woodrow L. Shew,et al.  Information Capacity and Transmission Are Maximized in Balanced Cortical Networks with Neuronal Avalanches , 2010, The Journal of Neuroscience.

[39]  C. Schroeder,et al.  How Local Is the Local Field Potential? , 2011, Neuron.

[40]  K. Linkenkaer-Hansen,et al.  Critical-State Dynamics of Avalanches and Oscillations Jointly Emerge from Balanced Excitation/Inhibition in Neuronal Networks , 2012, The Journal of Neuroscience.

[41]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[42]  E. Ott,et al.  Statistical properties of avalanches in networks. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[43]  Woodrow L. Shew,et al.  The Functional Benefits of Criticality in the Cortex , 2013, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[44]  M Girardi-Schappo,et al.  Critical avalanches and subsampling in map-based neural networks coupled with noisy synapses. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[45]  Viola Priesemann,et al.  Neuronal Avalanches Differ from Wakefulness to Deep Sleep – Evidence from Intracranial Depth Recordings in Humans , 2013, PLoS Comput. Biol..

[46]  M. A. Muñoz,et al.  Griffiths phases and the stretching of criticality in brain networks , 2013, Nature Communications.