Phase transitions and self-organized criticality in networks of stochastic spiking neurons

Phase transitions and critical behavior are crucial issues both in theoretical and experimental neuroscience. We report analytic and computational results about phase transitions and self-organized criticality (SOC) in networks with general stochastic neurons. The stochastic neuron has a firing probability given by a smooth monotonic function Φ(V) of the membrane potential V, rather than a sharp firing threshold. We find that such networks can operate in several dynamic regimes (phases) depending on the average synaptic weight and the shape of the firing function Φ. In particular, we encounter both continuous and discontinuous phase transitions to absorbing states. At the continuous transition critical boundary, neuronal avalanches occur whose distributions of size and duration are given by power laws, as observed in biological neural networks. We also propose and test a new mechanism to produce SOC: the use of dynamic neuronal gains – a form of short-term plasticity probably located at the axon initial segment (AIS) – instead of depressing synapses at the dendrites (as previously studied in the literature). The new self-organization mechanism produces a slightly supercritical state, that we called SOSC, in accord to some intuitions of Alan Turing.

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

[2]  Romain Brette,et al.  What Is the Most Realistic Single-Compartment Model of Spike Initiation? , 2015, PLoS Comput. Biol..

[3]  B. Cessac A discrete time neural network model with spiking neurons , 2007, Journal of mathematical biology.

[4]  Wulfram Gerstner,et al.  The Performance (and Limits) of Simple Neuron Models: Generalizations of the Leaky Integrate-and-Fire Model , 2012 .

[5]  L. de Arcangelis,et al.  Are dragon-king neuronal avalanches dungeons for self-organized brain activity? , 2012 .

[6]  Andreas V. M. Herz,et al.  A Universal Model for Spike-Frequency Adaptation , 2003, Neural Computation.

[7]  John M Beggs,et al.  The criticality hypothesis: how local cortical networks might optimize information processing , 2008, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[8]  J. Hopfield,et al.  Earthquake cycles and neural reverberations: Collective oscillations in systems with pulse-coupled threshold elements. , 1995, Physical review letters.

[9]  Mauro Copelli,et al.  Can dynamical synapses produce true self-organized criticality? , 2014, 1405.7740.

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

[11]  Paolo Massobrio,et al.  Criticality as a signature of healthy neural systems , 2015, Front. Syst. Neurosci..

[12]  A. M. Turing,et al.  Computing Machinery and Intelligence , 1950, The Philosophy of Artificial Intelligence.

[13]  Woodrow L. Shew,et al.  Predicting criticality and dynamic range in complex networks: effects of topology. , 2010, Physical review letters.

[14]  D. Marković,et al.  Power laws and Self-Organized Criticality in Theory and Nature , 2013, 1310.5527.

[15]  Woodrow L. Shew,et al.  Metabolite transport through glial networks stabilizes the dynamics of learning , 2016, 1605.03090.

[16]  M. A. Muñoz,et al.  Self-organization without conservation: true or just apparent scale-invariance? , 2009, 0905.1799.

[17]  Woodrow L. Shew,et al.  Inhibition causes ceaseless dynamics in networks of excitable nodes. , 2013, Physical review letters.

[18]  Boris S. Gutkin,et al.  The Effects of Spike Frequency Adaptation and Negative Feedback on the Synchronization of Neural Oscillators , 2001, Neural Computation.

[19]  Anthony N. Burkitt,et al.  A Review of the Integrate-and-fire Neuron Model: I. Homogeneous Synaptic Input , 2006, Biological Cybernetics.

[20]  S. Cooper Donald O. Hebb's synapse and learning rule: a history and commentary , 2005, Neuroscience & Biobehavioral Reviews.

[21]  Greg J. Stuart,et al.  Signal Processing in the Axon Initial Segment , 2012, Neuron.

[22]  Maria Francesca Carfora,et al.  A leaky integrate-and-fire model with adaptation for the generation of a spike train. , 2016, Mathematical biosciences and engineering : MBE.

[23]  Romain Brette,et al.  A Threshold Equation for Action Potential Initiation , 2010, PLoS Comput. Biol..

[24]  Edward Ott,et al.  Feedback control stabilization of critical dynamics via resource transport on multilayer networks: How glia enable learning dynamics in the brain. , 2016, Physical review. E.

[25]  M. Copelli,et al.  Undersampled Critical Branching Processes on Small-World and Random Networks Fail to Reproduce the Statistics of Spike Avalanches , 2014, PloS one.

[26]  L. de Arcangelis,et al.  Synaptic plasticity and neuronal refractory time cause scaling behaviour of neuronal avalanches , 2016, Scientific Reports.

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

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

[29]  Marc Benayoun,et al.  Avalanches in a Stochastic Model of Spiking Neurons , 2010, PLoS Comput. Biol..

[30]  B. Mandelbrot,et al.  RANDOM WALK MODELS FOR THE SPIKE ACTIVITY OF A SINGLE NEURON. , 1964, Biophysical journal.

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

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

[33]  Anthony N. Burkitt,et al.  A review of the integrate-and-fire neuron model: II. Inhomogeneous synaptic input and network properties , 2006, Biological Cybernetics.

[34]  Srdjan Ostojic,et al.  Two types of asynchronous activity in networks of excitatory and inhibitory spiking neurons , 2014, Nature Neuroscience.

[35]  Nicholas T. Carnevale,et al.  Simulation of networks of spiking neurons: A review of tools and strategies , 2006, Journal of Computational Neuroscience.

[36]  B Cessac,et al.  A discrete time neural network model with spiking neurons: II: Dynamics with noise , 2010, Journal of mathematical biology.

[37]  M. V. Rossum,et al.  Quantitative investigations of electrical nerve excitation treated as polarization , 2007, Biological Cybernetics.

[38]  Leo E. Lipetz,et al.  The Relation of Physiological and Psychological Aspects of Sensory Intensity , 1971 .

[39]  Mark D. McDonnell,et al.  Editorial: Neuronal Stochastic Variability: Influences on Spiking Dynamics and Network Activity , 2016, Front. Comput. Neurosci..

[40]  Hédi Soula,et al.  Spontaneous Dynamics of Asymmetric Random Recurrent Spiking Neural Networks , 2004, Neural Computation.

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

[42]  E. Presutti,et al.  Hydrodynamic Limit for Interacting Neurons , 2014, 1401.4264.

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

[44]  Joaquín J. Torres,et al.  Brain Performance versus Phase Transitions , 2015, Scientific Reports.

[45]  A. Galves,et al.  Infinite Systems of Interacting Chains with Memory of Variable Length—A Stochastic Model for Biological Neural Nets , 2012, 1212.5505.

[46]  M. A. Muñoz,et al.  Self-organization without conservation: are neuronal avalanches generically critical? , 2010, 1001.3256.

[47]  A. Galves,et al.  Modeling networks of spiking neurons as interacting processes with memory of variable length , 2015, 1502.06446.

[48]  Mauro Copelli,et al.  Correlations induced by depressing synapses in critically self-organized networks with quenched dynamics. , 2017, Physical review. E.

[49]  Guilherme Ost,et al.  A model for neural activity in the absence of external stimuli , 2014 .

[50]  Thilo Gross,et al.  Self-organized criticality as a fundamental property of neural systems , 2014, Front. Syst. Neurosci..

[51]  Guilherme Ost,et al.  Hydrodynamic Limit for Spatially Structured Interacting Neurons , 2015 .

[52]  K. Naka,et al.  S‐potentials from luminosity units in the retina of fish (Cyprinidae) , 1966, The Journal of physiology.

[53]  A. M. Turing,et al.  Computing Machinery and Intelligence , 1950, The Philosophy of Artificial Intelligence.

[54]  Bruno Cessac,et al.  A View of Neural Networks as Dynamical Systems , 2009, Int. J. Bifurc. Chaos.

[55]  Henry Markram,et al.  Neural Networks with Dynamic Synapses , 1998, Neural Computation.