Compressive Sensing Inference of Neuronal Network Connectivity in Balanced Neuronal Dynamics

Determining the structure of a network is of central importance to understanding its function in both neuroscience and applied mathematics. However, recovering the structural connectivity of neuronal networks remains a fundamental challenge both theoretically and experimentally. While neuronal networks operate in certain dynamical regimes, which may influence their connectivity reconstruction, there is widespread experimental evidence of a balanced neuronal operating state in which strong excitatory and inhibitory inputs are dynamically adjusted such that neuronal voltages primarily remain near resting potential. Utilizing the dynamics of model neurons in such a balanced regime in conjunction with the ubiquitous sparse connectivity structure of neuronal networks, we develop a compressive sensing theoretical framework for efficiently reconstructing network connections by measuring individual neuronal activity in response to a relatively small ensemble of random stimuli injected over a short time scale. By tuning the network dynamical regime, we determine that the highest fidelity reconstructions are achievable in the balanced state. We hypothesize the balanced dynamics observed in vivo may therefore be a result of evolutionary selection for optimal information encoding and expect the methodology developed to be generalizable for alternative model networks as well as experimental paradigms.

[1]  Changsong Zhou,et al.  Co-emergence of multi-scale cortical activities of irregular firing, oscillations and avalanches achieves cost-efficient information capacity , 2017, PLoS Comput. Biol..

[2]  Aaditya V. Rangan,et al.  Spatiotemporal dynamics of neuronal population response in the primary visual cortex , 2013, Proceedings of the National Academy of Sciences.

[3]  Edward T. Bullmore,et al.  Efficiency and Cost of Economical Brain Functional Networks , 2007, PLoS Comput. Biol..

[4]  Kenneth D. Miller,et al.  Physiological Gain Leads to High ISI Variability in a Simple Model of a Cortical Regular Spiking Cell , 1997, Neural Computation.

[5]  Aaditya V. Rangan,et al.  Architectural and synaptic mechanisms underlying coherent spontaneous activity in V1. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[6]  W. Denk,et al.  The Big and the Small: Challenges of Imaging the Brain’s Circuits , 2011, Science.

[7]  Nicolas Brunel,et al.  Dynamics of the Instantaneous Firing Rate in Response to Changes in Input Statistics , 2005, Journal of Computational Neuroscience.

[8]  Haim Sompolinsky,et al.  Chaotic Balanced State in a Model of Cortical Circuits , 1998, Neural Computation.

[9]  Victor J. Barranca,et al.  Compressive sensing reconstruction of feed-forward connectivity in pulse-coupled nonlinear networks. , 2016, Physical review. E.

[10]  Guosong Liu,et al.  Local structural balance and functional interaction of excitatory and inhibitory synapses in hippocampal dendrites , 2004, Nature Neuroscience.

[11]  D. Tank,et al.  Simultaneous cellular-resolution optical perturbation and imaging of place cell firing fields , 2014, Nature Neuroscience.

[12]  Jieping Ye,et al.  Network Reconstruction Based on Evolutionary-Game Data via Compressive Sensing , 2011, Physical Review X.

[13]  M. Wehr,et al.  Balanced Tone-evoked Synaptic Excitation and Inhibition in Mouse Auditory Cortex Experimental Procedures Physiological Procedures Article in Press , 2022 .

[14]  David Cai,et al.  Sparsity and Compressed Coding in Sensory Systems , 2014, PLoS Comput. Biol..

[15]  Michel A. Picardo,et al.  GABAergic Hub Neurons Orchestrate Synchrony in Developing Hippocampal Networks , 2009, Science.

[16]  Changsong Zhou,et al.  Sustained Activity in Hierarchical Modular Neural Networks: Self-Organized Criticality and Oscillations , 2010, Front. Comput. Neurosci..

[17]  David Cai,et al.  Causal and structural connectivity of pulse-coupled nonlinear networks. , 2013, Physical review letters.

[18]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[19]  C.E. Shannon,et al.  Communication in the Presence of Noise , 1949, Proceedings of the IRE.

[20]  Richard F. Betzel,et al.  Resting-brain functional connectivity predicted by analytic measures of network communication , 2013, Proceedings of the National Academy of Sciences.

[21]  Rong Jin,et al.  On the Use of Dynamic Bayesian Networks in Reconstructing Functional Neuronal Networks from Spike Train Ensembles , 2010, Neural Computation.

[22]  Ben Adcock,et al.  BREAKING THE COHERENCE BARRIER: A NEW THEORY FOR COMPRESSED SENSING , 2013, Forum of Mathematics, Sigma.

[23]  Jure Leskovec,et al.  Inferring networks of diffusion and influence , 2010, KDD.

[24]  David Cai,et al.  Improved Compressive Sensing of Natural Scenes Using Localized Random Sampling , 2016, Scientific Reports.

[25]  Karl J. Friston Functional and Effective Connectivity: A Review , 2011, Brain Connect..

[26]  M. Scanziani,et al.  How Inhibition Shapes Cortical Activity , 2011, Neuron.

[27]  E. Isacoff,et al.  Light-activated ion channels for remote control of neuronal firing , 2004, Nature Neuroscience.

[28]  Dmitri B. Chklovskii,et al.  Reconstruction of Sparse Circuits Using Multi-neuronal Excitation (RESCUME) , 2009, NIPS.

[29]  Stephen Becker,et al.  Quantum state tomography via compressed sensing. , 2009, Physical review letters.

[30]  Konrad P Kording,et al.  How advances in neural recording affect data analysis , 2011, Nature Neuroscience.

[31]  Shilpa Chakravartula,et al.  Complex Networks: Structure and Dynamics , 2014 .

[32]  M. London,et al.  Sensitivity to perturbations in vivo implies high noise and suggests rate coding in cortex , 2010, Nature.

[33]  C. Gilbert Horizontal integration and cortical dynamics , 1992, Neuron.

[34]  Alan C. Evans,et al.  Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. , 2007, Cerebral cortex.

[35]  G. Tononi,et al.  Breakdown of Cortical Effective Connectivity During Sleep , 2005, Science.

[36]  Richard H. Sherman,et al.  Chaotic communications in the presence of noise , 1993, Optics & Photonics.

[37]  David Cai,et al.  Dynamics of the exponential integrate-and-fire model with slow currents and adaptation , 2014, Journal of Computational Neuroscience.

[38]  Olaf Sporns,et al.  THE HUMAN CONNECTOME: A COMPLEX NETWORK , 2011, Schizophrenia Research.

[39]  T. Sejnowski,et al.  Monitoring Spiking Activity of Many Individual Neurons in Invertebrate Ganglia. , 2015, Advances in experimental medicine and biology.

[40]  R. Segev,et al.  The Architecture of Functional Interaction Networks in the Retina , 2011, The Journal of Neuroscience.

[41]  K. Stratford,et al.  Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  Gianluigi Mongillo,et al.  Bistability and spatiotemporal irregularity in neuronal networks with nonlinear synaptic transmission. , 2012, Physical review letters.

[43]  H. Sompolinsky,et al.  Chaos in Neuronal Networks with Balanced Excitatory and Inhibitory Activity , 1996, Science.

[44]  E.J. Candes,et al.  An Introduction To Compressive Sampling , 2008, IEEE Signal Processing Magazine.

[45]  Olaf Sporns,et al.  Network structure of cerebral cortex shapes functional connectivity on multiple time scales , 2007, Proceedings of the National Academy of Sciences.

[46]  S. Frick,et al.  Compressed Sensing , 2014, Computer Vision, A Reference Guide.

[47]  M. Scanziani,et al.  Equalizing Excitation-Inhibition Ratios across Visual Cortical Neurons , 2014, Nature.

[48]  Lee E Miller,et al.  Inferring functional connections between neurons , 2008, Current Opinion in Neurobiology.

[49]  Zhi-Qin John Xu,et al.  Granger Causality Network Reconstruction of Conductance-Based Integrate-and-Fire Neuronal Systems , 2014, PloS one.

[50]  O. Sporns,et al.  Organization, development and function of complex brain networks , 2004, Trends in Cognitive Sciences.

[51]  David Cai,et al.  Network dynamics for optimal compressive-sensing input-signal recovery. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[52]  E. Candès,et al.  Stable signal recovery from incomplete and inaccurate measurements , 2005, math/0503066.

[53]  Henry Kennedy,et al.  Cortical High-Density Counterstream Architectures , 2013, Science.

[54]  R.G. Baraniuk,et al.  Compressive Sensing [Lecture Notes] , 2007, IEEE Signal Processing Magazine.

[55]  Moshe Abeles,et al.  On Embedding Synfire Chains in a Balanced Network , 2003, Neural Computation.

[56]  Michael Elad,et al.  Optimized Projections for Compressed Sensing , 2007, IEEE Transactions on Signal Processing.

[57]  Marc Timme,et al.  Revealing network connectivity from response dynamics. , 2006, Physical review letters.

[58]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[59]  Liam Paninski,et al.  A Bayesian compressed-sensing approach for reconstructing neural connectivity from subsampled anatomical data , 2012, Journal of Computational Neuroscience.

[60]  K. H. Britten,et al.  Responses of neurons in macaque MT to stochastic motion signals , 1993, Visual Neuroscience.

[61]  W. Newsome,et al.  The Variable Discharge of Cortical Neurons: Implications for Connectivity, Computation, and Information Coding , 1998, The Journal of Neuroscience.

[62]  P. Goldman-Rakic,et al.  Temporally irregular mnemonic persistent activity in prefrontal neurons of monkeys during a delayed response task. , 2003, Journal of neurophysiology.

[63]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[64]  David Cai,et al.  Balanced Active Core in Heterogeneous Neuronal Networks , 2019, Front. Comput. Neurosci..

[65]  D. McCormick,et al.  Neocortical Network Activity In Vivo Is Generated through a Dynamic Balance of Excitation and Inhibition , 2006, The Journal of Neuroscience.

[66]  T. Sejnowski,et al.  Correlated neuronal activity and the flow of neural information , 2001, Nature Reviews Neuroscience.

[67]  Nathan R. Wilson,et al.  Response Features of Parvalbumin-Expressing Interneurons Suggest Precise Roles for Subtypes of Inhibition in Visual Cortex , 2010, Neuron.

[68]  Han Huang,et al.  The impact of spike-frequency adaptation on balanced network dynamics , 2018, Cognitive Neurodynamics.

[69]  W. Senn,et al.  Multiple time scales of temporal response in pyramidal and fast spiking cortical neurons. , 2006, Journal of neurophysiology.

[70]  David A. Leopold,et al.  Dynamic functional connectivity: Promise, issues, and interpretations , 2013, NeuroImage.

[71]  Massimo Fornasier,et al.  Compressive Sensing , 2015, Handbook of Mathematical Methods in Imaging.

[72]  W. Senn,et al.  Neocortical pyramidal cells respond as integrate-and-fire neurons to in vivo-like input currents. , 2003, Journal of neurophysiology.

[73]  E. Boyden,et al.  Simultaneous whole-animal 3D-imaging of neuronal activity using light-field microscopy , 2014, Nature Methods.

[74]  Tomoki Fukai,et al.  Balanced Excitatory and Inhibitory Inputs to Cortical Neurons Decouple Firing Irregularity from Rate Modulations , 2007, The Journal of Neuroscience.

[75]  Davi D Bock,et al.  Volume electron microscopy for neuronal circuit reconstruction , 2012, Current Opinion in Neurobiology.

[76]  Nicolas Brunel,et al.  Firing Rate of the Noisy Quadratic Integrate-and-Fire Neuron , 2003, Neural Computation.

[77]  David McLaughlin,et al.  States of High Conductance in a Large-Scale Model of the Visual Cortex , 2002, Journal of Computational Neuroscience.

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

[79]  Steffen Prohaska,et al.  Large-Scale Automated Histology in the Pursuit of Connectomes , 2011, The Journal of Neuroscience.

[80]  Yaakov Tsaig,et al.  Fast Solution of $\ell _{1}$ -Norm Minimization Problems When the Solution May Be Sparse , 2008, IEEE Transactions on Information Theory.

[81]  Tim P Vogels,et al.  Signal Propagation and Logic Gating in Networks of Integrate-and-Fire Neurons , 2005, The Journal of Neuroscience.

[82]  M K Habib,et al.  Dynamics of neuronal firing correlation: modulation of "effective connectivity". , 1989, Journal of neurophysiology.

[83]  E. Marder,et al.  From the connectome to brain function , 2013, Nature Methods.

[84]  Joel A. Tropp,et al.  Signal Recovery From Random Measurements Via Orthogonal Matching Pursuit , 2007, IEEE Transactions on Information Theory.

[85]  Jeff Hasty,et al.  Delay-induced degrade-and-fire oscillations in small genetic circuits. , 2009, Physical review letters.