Spontaneous activity emerging from an inferred network model captures complex spatio-temporal dynamics of spike data

The combination of new recording techniques in neuroscience and powerful inference methods recently held the promise to recover useful effective models, at the single neuron or network level, directly from observed data. The value of a model of course should critically depend on its ability to reproduce the dynamical behavior of the modeled system; however, few attempts have been made to inquire into the dynamics of inferred models in neuroscience, and none, to our knowledge, at the network level. Here we introduce a principled modification of a widely used generalized linear model (GLM), and learn its structural and dynamic parameters from ex-vivo spiking data. We show that the new model is able to capture the most prominent features of the highly non-stationary and non-linear dynamics displayed by the biological network, where the reference GLM largely fails. Two ingredients turn out to be key for success. The first one is a bounded transfer function that makes the single neuron able to respond to its input in a saturating fashion; beyond its biological plausibility such property, by limiting the capacity of the neuron to transfer information, makes the coding more robust in the face of the highly variable network activity, and noise. The second ingredient is a super-Poisson spikes generative probabilistic mechanism; this feature, that accounts for the fact that observations largely undersample the network, allows the model neuron to more flexibly incorporate the observed activity fluctuations. Taken together, the two ingredients, without increasing complexity, allow the model to capture the key dynamic elements. When left free to generate its spontaneous activity, the inferred model proved able to reproduce not only the non-stationary population dynamics of the network, but also part of the fine-grained structure of the dynamics at the single neuron level.

[1]  E. Halgren,et al.  Spatiotemporal dynamics of neocortical excitation and inhibition during human sleep , 2012, Proceedings of the National Academy of Sciences.

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

[3]  Andreas Herzog,et al.  Slow oscillating population activity in developing cortical networks: models and experimental results. , 2011, Journal of neurophysiology.

[4]  Hirokazu Takahashi,et al.  Locally embedded presages of global network bursts , 2017, Proceedings of the National Academy of Sciences.

[5]  Jörn Davidsen,et al.  Neuronal avalanche dynamics indicates different universality classes in neuronal cultures , 2018, Scientific Reports.

[6]  Christian Igel,et al.  Empirical evaluation of the improved Rprop learning algorithms , 2003, Neurocomputing.

[7]  Il Memming Park,et al.  Encoding and decoding in parietal cortex during sensorimotor decision-making , 2014, Nature Neuroscience.

[8]  J. Hertz,et al.  Mean field theory for nonequilibrium network reconstruction. , 2010, Physical review letters.

[9]  R. Quiroga,et al.  Principles of neural coding. , 2013 .

[10]  Alain Destexhe,et al.  Maximum entropy models reveal the correlation structure in cortical neural activity during wakefulness and sleep , 2018 .

[11]  V. Priesemann,et al.  Subsampling scaling , 2017, Nature Communications.

[12]  R. Zecchina,et al.  Inverse statistical problems: from the inverse Ising problem to data science , 2017, 1702.01522.

[13]  David J Schwab,et al.  Zipf's law and criticality in multivariate data without fine-tuning. , 2013, Physical review letters.

[14]  Geoffrey E. Hinton,et al.  Rectified Linear Units Improve Restricted Boltzmann Machines , 2010, ICML.

[15]  Sonja Grün,et al.  Bistability, non-ergodicity, and inhibition in pairwise maximum-entropy models , 2016, PLoS Comput. Biol..

[16]  Eero P. Simoncelli,et al.  Spatio-temporal correlations and visual signalling in a complete neuronal population , 2008, Nature.

[17]  Yasser Roudi,et al.  Multi-neuronal activity and functional connectivity in cell assemblies , 2015, Current Opinion in Neurobiology.

[18]  Shimon Marom,et al.  Self-organized criticality in single-neuron excitability. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  Jan Stegenga,et al.  Experimental analysis and computational modeling of interburst intervals in spontaneous activity of cortical neuronal culture , 2011, Biological Cybernetics.

[20]  Ian H. Stevenson,et al.  Bayesian Inference of Functional Connectivity and Network Structure From Spikes , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[21]  F. Lombardi,et al.  Temporal correlations in neuronal avalanche occurrence , 2016, Scientific Reports.

[22]  Steve M. Potter,et al.  An extremely rich repertoire of bursting patterns during the development of cortical cultures , 2006, BMC Neuroscience.

[23]  Matteo Marsili,et al.  The effect of nonstationarity on models inferred from neural data , 2012, 1203.5673.

[24]  J. Donoghue,et al.  Collective dynamics in human and monkey sensorimotor cortex: predicting single neuron spikes , 2009, Nature Neuroscience.

[25]  Federico Ricci-Tersenghi,et al.  Inferring Synaptic Structure in Presence of Neural Interaction Time Scales , 2014, PloS one.

[26]  Bruno B Averbeck Poisson or Not Poisson: Differences in Spike Train Statistics between Parietal Cortical Areas , 2009, Neuron.

[27]  Jos J. Eggermont The Correlative Brain , 1990 .

[28]  Uri T Eden,et al.  A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. , 2005, Journal of neurophysiology.

[29]  Gustavo Deco,et al.  Network Bursting Dynamics in Excitatory Cortical Neuron Cultures Results from the Combination of Different Adaptive Mechanism , 2013, PloS one.

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

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

[32]  José Carlos Príncipe,et al.  Modeling of Synchronized Burst in Dissociated Cortical Tissue: An Exploration of Parameter Space , 2006, The 2006 IEEE International Joint Conference on Neural Network Proceedings.

[33]  Danny Eytan,et al.  Dynamics and Effective Topology Underlying Synchronization in Networks of Cortical Neurons , 2006, The Journal of Neuroscience.

[34]  D. Plenz,et al.  Criticality in neural systems , 2014 .

[35]  James K. Lindsey,et al.  Applying Generalized Linear Models , 2000 .

[36]  Scott W. Linderman,et al.  Bayesian latent structure discovery from multi-neuron recordings , 2016, NIPS.

[37]  S. Leibler,et al.  Neuronal couplings between retinal ganglion cells inferred by efficient inverse statistical physics methods , 2009, Proceedings of the National Academy of Sciences.

[38]  Gustavo Deco,et al.  Network Events on Multiple Space and Time Scales in Cultured Neural Networks and in a Stochastic Rate Model , 2015, PLoS Comput. Biol..

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

[40]  Jonathan W. Pillow,et al.  Capturing the Dynamical Repertoire of Single Neurons with Generalized Linear Models , 2016, Neural Computation.

[41]  D. Plenz,et al.  The organizing principles of neuronal avalanches: cell assemblies in the cortex? , 2007, Trends in Neurosciences.

[42]  Klaus Obermayer,et al.  Analyzing Short-Term Noise Dependencies of Spike-Counts in Macaque Prefrontal Cortex Using Copulas and the Flashlight Transformation , 2009, PLoS Comput. Biol..

[43]  M Giugliano,et al.  Single-neuron discharge properties and network activity in dissociated cultures of neocortex. , 2004, Journal of neurophysiology.

[44]  J. Schiller,et al.  Dynamics of Excitability over Extended Timescales in Cultured Cortical Neurons , 2010, The Journal of Neuroscience.

[45]  Eero P. Simoncelli,et al.  Partitioning neuronal variability , 2014, Nature Neuroscience.

[46]  Michael J. Berry,et al.  Thermodynamics and signatures of criticality in a network of neurons , 2015, Proceedings of the National Academy of Sciences.