Identifying nonlinear dynamical systems via generative recurrent neural networks with applications to fMRI

A major tenet in theoretical neuroscience is that cognitive and behavioral processes are ultimately implemented in terms of the neural system dynamics. Accordingly, a major aim for the analysis of neurophysiological measurements should lie in the identification of the computational dynamics underlying task processing. Here we advance a state space model (SSM) based on generative piecewise-linear recurrent neural networks (PLRNN) to assess dynamics from neuroimaging data. In contrast to many other nonlinear time series models which have been proposed for reconstructing latent dynamics, our model is easily interpretable in neural terms, amenable to systematic dynamical systems analysis of the resulting set of equations, and can straightforwardly be transformed into an equivalent continuous-time dynamical system. The major contributions of this paper are the introduction of a new observation model suitable for functional magnetic resonance imaging (fMRI) coupled to the latent PLRNN, an efficient stepwise training procedure that forces the latent model to capture the ‘true’ underlying dynamics rather than just fitting (or predicting) the observations, and of an empirical measure based on the Kullback-Leibler divergence to evaluate from empirical time series how well this goal of approximating the underlying dynamics has been achieved. We validate and illustrate the power of our approach on simulated ‘ground-truth’ dynamical systems as well as on experimental fMRI time series, and demonstrate that the learnt dynamics harbors task-related nonlinear structure that a linear dynamical model fails to capture. Given that fMRI is one of the most common techniques for measuring brain activity non-invasively in human subjects, this approach may provide a novel step toward analyzing aberrant (nonlinear) dynamics for clinical assessment or neuroscientific research.

[1]  John R. Hershey,et al.  Approximating the Kullback Leibler Divergence Between Gaussian Mixture Models , 2007, 2007 IEEE International Conference on Acoustics, Speech and Signal Processing - ICASSP '07.

[2]  Kaustubh Supekar,et al.  Multivariate dynamical systems models for estimating causal interactions in fMRI , 2011, NeuroImage.

[3]  Pablo Varona,et al.  Robust Transient Dynamics and Brain Functions , 2011, Front. Comput. Neurosci..

[4]  Byron M. Yu,et al.  Techniques for extracting single-trial activity patterns from large-scale neural recordings , 2007, Current Opinion in Neurobiology.

[5]  John P. Cunningham,et al.  Gaussian-process factor analysis for low-dimensional single-trial analysis of neural population activity , 2008, NIPS.

[6]  A. Grinvald,et al.  Imaging Cortical Dynamics at High Spatial and Temporal Resolution with Novel Blue Voltage-Sensitive Dyes , 1999, Neuron.

[7]  Max Welling,et al.  Auto-Encoding Variational Bayes , 2013, ICLR.

[8]  Daniel Durstewitz,et al.  Attracting Dynamics of Frontal Cortex Ensembles during Memory-Guided Decision-Making , 2011, PLoS Comput. Biol..

[9]  Sylvain Arlot,et al.  A survey of cross-validation procedures for model selection , 2009, 0907.4728.

[10]  Chethan Pandarinath,et al.  Inferring single-trial neural population dynamics using sequential auto-encoders , 2017, Nature Methods.

[11]  Johan Grasman,et al.  Relaxation Oscillations , 2009, Encyclopedia of Complexity and Systems Science.

[12]  Luigi Brugnano,et al.  Iterative Solution of Piecewise Linear Systems , 2007, SIAM J. Sci. Comput..

[13]  Il Memming Park,et al.  Recursive Variational Bayesian Dual Estimation for Nonlinear Dynamics and Non-Gaussian Observations , 2017 .

[14]  Lars Buesing,et al.  Estimating state and Parameters in state space Models of Spike trains , 2015 .

[15]  R. Kass,et al.  Approximate Methods for State-Space Models , 2010, Journal of the American Statistical Association.

[16]  Christopher D. Manning,et al.  Introduction to Information Retrieval , 2010, J. Assoc. Inf. Sci. Technol..

[17]  R. Yuste,et al.  Detecting action potentials in neuronal populations with calcium imaging. , 1999, Methods.

[18]  Daniel Durstewitz,et al.  Recurrent Neural Networks in Mobile Sampling and Intervention , 2018, Schizophrenia bulletin.

[19]  Larissa Albantakis,et al.  The encoding of alternatives in multiple-choice decision-making , 2009, Proceedings of the National Academy of Sciences.

[20]  Tohru Ozaki,et al.  Time Series Modeling of Neuroscience Data , 2012 .

[21]  Jaideep Pathak,et al.  Using machine learning to replicate chaotic attractors and calculate Lyapunov exponents from data. , 2017, Chaos.

[22]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[23]  安藤 広志,et al.  20世紀の名著名論:David Marr:Vision:a Computational Investigation into the Human Representation and Processing of Visual Information , 2005 .

[24]  S. Wood Statistical inference for noisy nonlinear ecological dynamic systems , 2010, Nature.

[25]  Robert Tibshirani,et al.  The Elements of Statistical Learning: Data Mining, Inference, and Prediction, 2nd Edition , 2001, Springer Series in Statistics.

[26]  Melvin J. Hinich,et al.  Time Series Analysis by State Space Methods , 2001 .

[27]  T. Sejnowski,et al.  Neurocomputational models of working memory , 2000, Nature Neuroscience.

[28]  Joachim Haß,et al.  An Approximation to the Adaptive Exponential Integrate-and-Fire Neuron Model Allows Fast and Predictive Fitting to Physiological Data , 2012, Front. Comput. Neurosci..

[29]  Daniel Durstewitz,et al.  Psychiatric Illnesses as Disorders of Network Dynamics , 2018, 1809.06303.

[30]  S. Brunton,et al.  Discovering governing equations from data by sparse identification of nonlinear dynamical systems , 2015, Proceedings of the National Academy of Sciences.

[31]  Annika L A Nichols,et al.  A global brain state underlies C. elegans sleep behavior , 2017, Science.

[32]  A. Belger,et al.  Dynamic functional connectivity analysis reveals transient states of dysconnectivity in schizophrenia , 2014, NeuroImage: Clinical.

[33]  A S Gevins,et al.  Effects of prolonged mental work on functional brain topography. , 1990, Electroencephalography and clinical neurophysiology.

[34]  Brian Everitt,et al.  Principles of Multivariate Analysis , 2001 .

[35]  Il Memming Park,et al.  BLACK BOX VARIATIONAL INFERENCE FOR STATE SPACE MODELS , 2015, 1511.07367.

[36]  F. Takens Detecting strange attractors in turbulence , 1981 .

[37]  H. Wilson Spikes, Decisions, and Actions: The Dynamical Foundations of Neuroscience , 1999 .

[38]  Juan M. Corchado,et al.  Fight sample degeneracy and impoverishment in particle filters: A review of intelligent approaches , 2013, Expert Syst. Appl..

[39]  J J Hopfield,et al.  Neural networks and physical systems with emergent collective computational abilities. , 1982, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Xiao-Jing Wang,et al.  Probabilistic Decision Making by Slow Reverberation in Cortical Circuits , 2002, Neuron.

[41]  Wei Wu,et al.  A new look at state-space models for neural data , 2010, Journal of Computational Neuroscience.

[42]  V. Calhoun,et al.  Dynamic connectivity states estimated from resting fMRI Identify differences among Schizophrenia, bipolar disorder, and healthy control subjects , 2014, Front. Hum. Neurosci..

[43]  Ashutosh Kumar Singh,et al.  The Elements of Statistical Learning: Data Mining, Inference, and Prediction , 2010 .

[44]  M. Breakspear Dynamic models of large-scale brain activity , 2017, Nature Neuroscience.

[45]  P. Bickel,et al.  Curse-of-dimensionality revisited: Collapse of the particle filter in very large scale systems , 2008, 0805.3034.

[46]  Georgia Koppe,et al.  Temporal unpredictability of a stimulus sequence affects brain activation differently depending on cognitive task demands , 2014, NeuroImage.

[47]  E. Lorenz Deterministic nonperiodic flow , 1963 .

[48]  D. Rubin,et al.  Maximum likelihood from incomplete data via the EM - algorithm plus discussions on the paper , 1977 .

[49]  Daniel Durstewitz,et al.  Amphetamine Exerts Dose-Dependent Changes in Prefrontal Cortex Attractor Dynamics during Working Memory , 2015, The Journal of Neuroscience.

[50]  Daan Wierstra,et al.  Stochastic Backpropagation and Approximate Inference in Deep Generative Models , 2014, ICML.

[51]  Henry D. I. Abarbanel,et al.  Machine Learning: Deepest Learning as Statistical Data Assimilation Problems , 2017, Neural Computation.

[52]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[53]  Xiao-Jing Wang Synaptic reverberation underlying mnemonic persistent activity , 2001, Trends in Neurosciences.

[54]  Michel Cosnard,et al.  Computability with Low-Dimensional Dynamical Systems , 1994, Theor. Comput. Sci..

[55]  J. A. Stewart,et al.  Nonlinear Time Series Analysis , 2015 .

[56]  D. Lathrop Nonlinear Dynamics and Chaos: With Applications to Physics, Biology, Chemistry, and Engineering , 2015 .

[57]  Daniel Durstewitz,et al.  A state space approach for piecewise-linear recurrent neural networks for identifying computational dynamics from neural measurements , 2016, PLoS Comput. Biol..

[58]  Dajiang Zhu,et al.  Dynamic functional connectomics signatures for characterization and differentiation of PTSD patients , 2014, Human brain mapping.

[59]  Yoshua Bengio,et al.  A Recurrent Latent Variable Model for Sequential Data , 2015, NIPS.

[60]  W. Newsome,et al.  Context-dependent computation by recurrent dynamics in prefrontal cortex , 2013, Nature.

[61]  Guangyu R. Yang,et al.  Training Excitatory-Inhibitory Recurrent Neural Networks for Cognitive Tasks: A Simple and Flexible Framework , 2016, PLoS Comput. Biol..

[62]  Daniel Durstewitz,et al.  Self-Organizing Neural Integrator Predicts Interval Times through Climbing Activity , 2003, The Journal of Neuroscience.

[63]  Geoffrey E. Hinton,et al.  Deep Learning , 2015, Nature.

[64]  Nicolas Brunel,et al.  Analytical approximations of the firing rate of an adaptive exponential integrate-and-fire neuron in the presence of synaptic noise , 2014, Front. Comput. Neurosci..

[65]  D. Durstewitz,et al.  The Dual-State Theory of Prefrontal Cortex Dopamine Function with Relevance to Catechol-O-Methyltransferase Genotypes and Schizophrenia , 2008, Biological Psychiatry.

[66]  G. Laurent,et al.  Odor encoding as an active, dynamical process: experiments, computation, and theory. , 2001, Annual review of neuroscience.

[67]  Gustavo Deco,et al.  Editorial: Metastable Dynamics of Neural Ensembles , 2018, Front. Syst. Neurosci..

[68]  Daniel Durstewitz Advanced Data Analysis in Neuroscience , 2017 .

[69]  Masahiro Kimura,et al.  Learning dynamical systems by recurrent neural networks from orbits , 1998, Neural Networks.

[70]  Yee Whye Teh,et al.  A Fast Learning Algorithm for Deep Belief Nets , 2006, Neural Computation.

[71]  M. Hasselmo,et al.  Mechanism of Graded Persistent Cellular Activity of Entorhinal Cortex Layer V Neurons , 2006, Neuron.

[72]  F. Collins,et al.  A new initiative on precision medicine. , 2015, The New England journal of medicine.

[73]  Emery N. Brown,et al.  Estimating a State-space Model from Point Process Observations Emery N. Brown , 2022 .

[74]  Rob J. Hyndman,et al.  A note on the validity of cross-validation for evaluating autoregressive time series prediction , 2018, Comput. Stat. Data Anal..

[75]  Xiao-Jing Wang,et al.  Task representations in neural networks trained to perform many cognitive tasks , 2019, Nature Neuroscience.

[76]  Ranulfo Romo,et al.  Flexible Control of Mutual Inhibition: A Neural Model of Two-Interval Discrimination , 2005, Science.

[77]  George Sugihara,et al.  Detecting Causality in Complex Ecosystems , 2012, Science.

[78]  Daniel D. Lee,et al.  Stability of the Memory of Eye Position in a Recurrent Network of Conductance-Based Model Neurons , 2000, Neuron.

[79]  Gilles Laurent,et al.  Transient Dynamics for Neural Processing , 2008, Science.

[80]  David Marr,et al.  VISION A Computational Investigation into the Human Representation and Processing of Visual Information , 2009 .

[81]  C. Striebel,et al.  On the maximum likelihood estimates for linear dynamic systems , 1965 .

[82]  Yuan Zhao,et al.  Variational Online Learning of Neural Dynamics , 2017, Frontiers in Computational Neuroscience.

[83]  Guigang Zhang,et al.  Deep Learning , 2016, Int. J. Semantic Comput..

[84]  Gabriele M. T. D'Eleuterio,et al.  Synthesis of recurrent neural networks for dynamical system simulation , 2015, Neural Networks.

[85]  Ramón Huerta,et al.  Transient Cognitive Dynamics, Metastability, and Decision Making , 2008, PLoS Comput. Biol..

[86]  Yuichi Nakamura,et al.  Approximation of dynamical systems by continuous time recurrent neural networks , 1993, Neural Networks.

[87]  T. Başar,et al.  A New Approach to Linear Filtering and Prediction Problems , 2001 .

[88]  Christian Osendorfer,et al.  Learning Stochastic Recurrent Networks , 2014, NIPS 2014.

[89]  R. Romo,et al.  Neuronal correlates of parametric working memory in the prefrontal cortex , 1999, Nature.

[90]  Balth. van der Pol Jun. LXXXVIII. On “relaxation-oscillations” , 1926 .

[91]  Il Memming Park,et al.  Variational Joint Filtering , 2017, 1707.09049.

[92]  Ichiro Tsuda,et al.  Chaotic itinerancy and its roles in cognitive neurodynamics , 2015, Current Opinion in Neurobiology.

[93]  Sachin S. Talathi,et al.  Improving performance of recurrent neural network with relu nonlinearity , 2015, ArXiv.

[94]  Diana J. N. Armbruster,et al.  Prefrontal Cortical Mechanisms Underlying Individual Differences in Cognitive Flexibility and Stability , 2012, Journal of Cognitive Neuroscience.

[95]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[96]  Byron M. Yu,et al.  Extracting Dynamical Structure Embedded in Neural Activity , 2005, NIPS.