Robust cortical criticality and diverse dynamics resulting from functional specification.

Despite the recognition of the layered structure and evident criticality in the cortex, how the specification of input, output, and computational layers affects the self-organized criticality has not been much explored. By constructing heterogeneous structures with a well-accepted model of leaky neurons, we find that the specification can lead to robust criticality rather insensitive to the strength of external stimuli. This naturally unifies the adaptation to strong inputs without extra synaptic plasticity mechanisms. Low degree of recurrence constitutes an alternative explanation to subcriticality other than the high-frequency inputs. Unlike fully recurrent networks where external stimuli always render subcriticality, the dynamics of networks with sufficient feedforward connections can be driven to criticality and supercriticality. These findings indicate that functional and structural specification and their interplay with external stimuli are of crucial importance for the network dynamics. The robust criticality puts forward networks of the leaky neurons as promising platforms for realizing artificial neural networks that work in the vicinity of critical points.

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

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

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

[4]  J. Touboul,et al.  Power-law statistics and universal scaling in the absence of criticality. , 2015, Physical review. E.

[5]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[6]  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.

[7]  Jochen Triesch,et al.  Spike avalanches in vivo suggest a driven, slightly subcritical brain state , 2014, Front. Syst. Neurosci..

[8]  Raoul-Martin Memmesheimer,et al.  Growing Critical: Self-Organized Criticality in a Developing Neural System. , 2018, Physical review letters.

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

[10]  R. Malenka,et al.  Synaptic Plasticity: Multiple Forms, Functions, and Mechanisms , 2008, Neuropsychopharmacology.

[11]  Robert A. Legenstein,et al.  2007 Special Issue: Edge of chaos and prediction of computational performance for neural circuit models , 2007 .

[12]  Amos Maritan,et al.  Scaling and criticality in a phenomenological renormalization group , 2020 .

[13]  M. A. Muñoz,et al.  Stochastic Amplification of Fluctuations in Cortical Up-States , 2012, PloS one.

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

[15]  M. Magnasco,et al.  Self-tuned critical anti-Hebbian networks. , 2009, Physical review letters.

[16]  William Bialek,et al.  Coarse Graining, Fixed Points, and Scaling in a Large Population of Neurons. , 2018, Physical review letters.

[17]  Amos Maritan,et al.  Testing the critical brain hypothesis using a phenomelogical renormalization group , 2020 .

[18]  Sonja Grün,et al.  Second type of criticality in the brain uncovers rich multiple-neuron dynamics , 2016, Proceedings of the National Academy of Sciences.

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

[20]  Viola Priesemann,et al.  Control of criticality and computation in spiking neuromorphic networks with plasticity , 2020, Nature Communications.

[21]  John M. Beggs,et al.  Quasicritical brain dynamics on a nonequilibrium Widom line. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  Christopher G. Langton,et al.  Computation at the edge of chaos: Phase transitions and emergent computation , 1990 .

[23]  Narayan Srinivasa,et al.  Synaptic Plasticity Enables Adaptive Self-Tuning Critical Networks , 2015, PLoS Comput. Biol..

[24]  L. F Abbott,et al.  Lapicque’s introduction of the integrate-and-fire model neuron (1907) , 1999, Brain Research Bulletin.

[25]  Moritz Helias,et al.  Distributions of covariances as a window into the operational regime of neuronal networks , 2016 .

[26]  Arianna Maffei,et al.  From Hiring to Firing: Activation of Inhibitory Neurons and Their Recruitment in Behavior , 2019, Front. Mol. Neurosci..

[27]  M. A. Muñoz,et al.  Time-series thresholding and the definition of avalanche size. , 2019, Physical review. E.

[28]  Ralf Wessel,et al.  Cortical Circuit Dynamics Are Homeostatically Tuned to Criticality In Vivo , 2019, Neuron.

[29]  Johannes Zierenberg,et al.  Homeostatic plasticity and external input shape neural network dynamics , 2018, bioRxiv.

[30]  C. Wilson,et al.  Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. , 1994, Journal of neurophysiology.

[31]  Jochen Triesch,et al.  Criticality meets learning: Criticality signatures in a self-organizing recurrent neural network , 2017, PloS one.

[32]  Changsong Zhou,et al.  Hierarchical modular structure enhances the robustness of self-organized criticality in neural networks , 2012 .

[33]  John M. Beggs,et al.  Universal critical dynamics in high resolution neuronal avalanche data. , 2012, Physical review letters.

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

[35]  K. Harris,et al.  Cortical connectivity and sensory coding , 2013, Nature.

[36]  G. Cecchi,et al.  Scale-free brain functional networks. , 2003, Physical review letters.

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

[38]  Stefan Mihalas,et al.  Self-organized criticality occurs in non-conservative neuronal networks during Up states , 2010, Nature physics.

[39]  Serena Bradde,et al.  PCA Meets RG , 2016, Journal of Statistical Physics.

[40]  Wolfgang Maass,et al.  Bayesian Computation Emerges in Generic Cortical Microcircuits through Spike-Timing-Dependent Plasticity , 2013, PLoS Comput. Biol..

[41]  J. Touboul,et al.  Can Power-Law Scaling and Neuronal Avalanches Arise from Stochastic Dynamics? , 2009, PloS one.

[42]  R. Yuste,et al.  Attractor dynamics of network UP states in the neocortex , 2003, Nature.

[43]  Evidence for Quasicritical Brain Dynamics. , 2020, Physical review letters.

[44]  Thilo Gross,et al.  Adaptive self-organization in a realistic neural network model. , 2009, Physical review. E, Statistical, nonlinear, and soft matter physics.

[45]  D. Stauffer Scaling Theory of Percolation Clusters , 1979, Complex Media and Percolation Theory.

[46]  M. A. Muñoz,et al.  Neutral Theory and Scale-Free Neural Dynamics , 2017, 1703.05079.

[47]  Carla Perrone-Capano,et al.  Activity-dependent neural network model on scale-free networks. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

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

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

[51]  John M. Beggs,et al.  Unveiling causal activity of complex networks , 2016, 1603.05659.

[52]  James P. Gleeson,et al.  Emergence of power laws in noncritical neuronal systems , 2019, Physical review. E.

[53]  M. A. Muñoz Colloquium: Criticality and dynamical scaling in living systems , 2017, Reviews of Modern Physics.

[54]  J. Sethna,et al.  Crackling noise , 2001, Nature.

[55]  Jens Wilting,et al.  Inferring collective dynamical states from widely unobserved systems , 2016, Nature Communications.

[56]  E Greenfield,et al.  Mutual information in a dilute, asymmetric neural network model. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[57]  Andrew S. Cassidy,et al.  A million spiking-neuron integrated circuit with a scalable communication network and interface , 2014, Science.

[58]  Takeshi Kaneko,et al.  Recurrent Infomax Generates Cell Assemblies, Neuronal Avalanches, and Simple Cell-Like Selectivity , 2009, Neural Computation.

[59]  Edward Ott,et al.  Dynamic regulation of resource transport induces criticality in interdependent networks of excitable units. , 2018, Physical review. E.

[60]  Gordon Pipa,et al.  SORN: A Self-Organizing Recurrent Neural Network , 2009, Front. Comput. Neurosci..

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

[62]  Sergio Martinoia,et al.  Self-organized criticality in cortical assemblies occurs in concurrent scale-free and small-world networks , 2015, Scientific Reports.

[63]  Pedro V. Carelli,et al.  Criticality between cortical states , 2018, bioRxiv.

[64]  Nils Bertschinger,et al.  Real-Time Computation at the Edge of Chaos in Recurrent Neural Networks , 2004, Neural Computation.

[65]  Woodrow L. Shew,et al.  Adaptation to sensory input tunes visual cortex to criticality , 2015, Nature Physics.