Learning neural connectivity from firing activity: efficient algorithms with provable guarantees on topology

The connectivity of a neuronal network has a major effect on its functionality and role. It is generally believed that the complex network structure of the brain provides a physiological basis for information processing. Therefore, identifying the network’s topology has received a lot of attentions in neuroscience and has been the center of many research initiatives such as Human Connectome Project. Nevertheless, direct and invasive approaches that slice and observe the neural tissue have proven to be time consuming, complex and costly. As a result, the inverse methods that utilize firing activity of neurons in order to identify the (functional) connections have gained momentum recently, especially in light of rapid advances in recording technologies; It will soon be possible to simultaneously monitor the activities of tens of thousands of neurons in real time. While there are a number of excellent approaches that aim to identify the functional connections from firing activities, the scalability of the proposed techniques plays a major challenge in applying them on large-scale datasets of recorded firing activities. In exceptional cases where scalability has not been an issue, the theoretical performance guarantees are usually limited to a specific family of neurons or the type of firing activities. In this paper, we formulate the neural network reconstruction as an instance of a graph learning problem, where we observe the behavior of nodes/neurons (i.e., firing activities) and aim to find the links/connections. We develop a scalable learning mechanism and derive the conditions under which the estimated graph for a network of Leaky Integrate and Fire (LIf) neurons matches the true underlying synaptic connections. We then validate the performance of the algorithm using artificially generated data (for benchmarking) and real data recorded from multiple hippocampal areas in rats.

[1]  Wulfram Gerstner,et al.  SPIKING NEURON MODELS Single Neurons , Populations , Plasticity , 2002 .

[2]  Simona Cocco,et al.  Fast inference of interactions in assemblies of stochastic integrate-and-fire neurons from spike recordings , 2011, Journal of Computational Neuroscience.

[3]  J. Schur Bemerkungen zur Theorie der beschränkten Bilinearformen mit unendlich vielen Veränderlichen. , 1911 .

[4]  Andreas Moller,et al.  A CMOS-based sensor array for in-vitro neural tissue interfacing with 4225 recording sites and 1024 stimulation sites , 2014, 2014 IEEE Biomedical Circuits and Systems Conference (BioCAS) Proceedings.

[5]  Aurel A. Lazar,et al.  Functional Identification of Spike-Processing Neural Circuits , 2014, Neural Computation.

[6]  Haim Sompolinsky,et al.  Learning Precisely Timed Spikes , 2014, Neuron.

[7]  H. Dale Pharmacology and Nerve-Endings , 1935 .

[8]  Emery N. Brown,et al.  A Granger Causality Measure for Point Process Models of Ensemble Neural Spiking Activity , 2011, PLoS Comput. Biol..

[9]  Joshua T. Vogelstein,et al.  A Bayesian approach for inferring neuronal connectivity from calcium fluorescent imaging data , 2011, 1107.4228.

[10]  Thomas Hofmann,et al.  Communication-Efficient Distributed Dual Coordinate Ascent , 2014, NIPS.

[11]  Eero P. Simoncelli,et al.  Biases in white noise analysis due to non-Poisson spike generation , 2003, Neurocomputing.

[12]  Amin Karbasi,et al.  Learning network structures from firing patterns , 2016, 2016 IEEE International Conference on Acoustics, Speech and Signal Processing (ICASSP).

[13]  Richard G. Baraniuk,et al.  A Field Guide to Forward-Backward Splitting with a FASTA Implementation , 2014, ArXiv.

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

[15]  Rebecca Willett,et al.  Tracking Dynamic Point Processes on Networks , 2014, IEEE Transactions on Information Theory.

[16]  L. Paninski Maximum likelihood estimation of cascade point-process neural encoding models , 2004, Network.

[17]  R. Kass,et al.  Multiple neural spike train data analysis: state-of-the-art and future challenges , 2004, Nature Neuroscience.

[18]  Carolina Gutierrez Herrera,et al.  An integrated microprobe for the brain , 2015, Nature Biotechnology.

[19]  Liam Paninski,et al.  Fast inference in generalized linear models via expected log-likelihoods , 2013, Journal of Computational Neuroscience.

[20]  Nicolas Brunel,et al.  Efficient supervised learning in networks with binary synapses , 2007, BMC Neuroscience.

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

[22]  Benjamin F. Grewe,et al.  High-speed in vivo calcium imaging reveals neuronal network activity with near-millisecond precision , 2010, Nature Methods.

[23]  Eve Marder,et al.  Successful Reconstruction of a Physiological Circuit with Known Connectivity from Spiking Activity Alone , 2013, PLoS Comput. Biol..

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

[25]  Louis K. Scheffer,et al.  Toward large-scale connectome reconstructions , 2014, Current Opinion in Neurobiology.

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

[27]  Mark A. Davenport,et al.  Learning network structure via Hawkes processes , 2015 .

[28]  Stephen J. Wright,et al.  Sparse Reconstruction by Separable Approximation , 2008, IEEE Transactions on Signal Processing.

[29]  Moritz Deger,et al.  Reconstruction of recurrent synaptic connectivity of thousands of neurons from simulated spiking activity , 2015, Journal of Computational Neuroscience.

[30]  G. Buzsáki,et al.  Theta Oscillations Provide Temporal Windows for Local Circuit Computation in the Entorhinal-Hippocampal Loop , 2009, Neuron.

[31]  Guan-Yu Chen,et al.  Three-Dimensional Reconstruction of Brain-wide Wiring Networks in Drosophila at Single-Cell Resolution , 2011, Current Biology.

[32]  Wulfram Gerstner,et al.  Spiking Neuron Models , 2002 .

[33]  Michael Schmitt,et al.  On the Complexity of Learning for Spiking Neurons with Temporal Coding , 1999, Inf. Comput..

[34]  Thomas K. Berger,et al.  A synaptic organizing principle for cortical neuronal groups , 2011, Proceedings of the National Academy of Sciences.

[35]  Marc Timme,et al.  Inferring Synaptic Connectivity from Spatio-Temporal Spike Patterns , 2011, Front. Comput. Neurosci..

[36]  G. Buzsáki,et al.  NeuroGrid: recording action potentials from the surface of the brain , 2014, Nature Neuroscience.

[37]  Daniel Soudry,et al.  Efficient "Shotgun" Inference of Neural Connectivity from Highly Sub-sampled Activity Data , 2015, PLoS Comput. Biol..