Adaptive, locally linear models of complex dynamics

Significance Natural phenomena are teeming with temporal complexity, but such dynamics, however fascinating, offer substantial obstacles to quantitative understanding. We introduce a general method based on the simple idea that even complicated time series are locally linear. Our analysis transforms dynamical data into a parameterized space of linear models, and we detail a hierarchical clustering of this space into dynamical categories. The linear models reveal fine-scaled, interpretable states in the posture behavior and global brain activity of the nematode Caenorhabditis elegans. Furthermore, we find that the population of stable and unstable oscillations suggests a near-critical dynamics across both brains and behavior. We expect our approach to be widely applicable. The dynamics of complex systems generally include high-dimensional, nonstationary, and nonlinear behavior, all of which pose fundamental challenges to quantitative understanding. To address these difficulties, we detail an approach based on local linear models within windows determined adaptively from data. While the dynamics within each window are simple, consisting of exponential decay, growth, and oscillations, the collection of local parameters across all windows provides a principled characterization of the full time series. To explore the resulting model space, we develop a likelihood-based hierarchical clustering, and we examine the eigenvalues of the linear dynamics. We demonstrate our analysis with the Lorenz system undergoing stable spiral dynamics and in the standard chaotic regime. Applied to the posture dynamics of the nematode Caenorhabditis elegans, our approach identifies fine-grained behavioral states and model dynamics which fluctuate about an instability boundary, and we detail a bifurcation in a transition from forward to backward crawling. We analyze whole-brain imaging in C. elegans and show that global brain dynamics is damped away from the instability boundary by a decrease in oxygen concentration. We provide additional evidence for such near-critical dynamics from the analysis of electrocorticography in monkey and the imaging of a neural population from mouse visual cortex at single-cell resolution.

[1]  Pawel Romanczuk,et al.  Collective motion due to individual escape and pursuit response. , 2008, Physical review letters.

[2]  Ryan P. Adams,et al.  Mapping Sub-Second Structure in Mouse Behavior , 2015, Neuron.

[3]  Eli J. Cornblath,et al.  Distributed rhythm generators underlie Caenorhabditis elegans forward locomotion , 2017, bioRxiv.

[4]  Andrew J Majda,et al.  Conceptual dynamical models for turbulence , 2014, Proceedings of the National Academy of Sciences.

[5]  William Bialek,et al.  Searching for collective behavior in a small brain. , 2018, Physical review. E.

[6]  Nigel Collier,et al.  Change-Point Detection in Time-Series Data by Relative Density-Ratio Estimation , 2012, Neural Networks.

[7]  Andrew J Rennekamp,et al.  Toward a Choate View of Fate , 2018, Cell.

[8]  Mark J Alkema,et al.  Excitatory motor neurons are local oscillators for backward locomotion , 2017, eLife.

[9]  Jaideep Srivastava,et al.  Event detection from time series data , 1999, KDD '99.

[10]  Mw Hirsch,et al.  Chaos In Dynamical Systems , 2016 .

[11]  G. Wainrib,et al.  Topological and dynamical complexity of random neural networks. , 2012, Physical review letters.

[12]  Steven L. Brunton,et al.  Chaos as an intermittently forced linear system , 2016, Nature Communications.

[13]  Joshua W Shaevitz,et al.  Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans , 2015, Proceedings of the National Academy of Sciences.

[14]  D. Hawkins POINT ESTIMATION OF THE PARAMETERS OF PIECEWISE REGRESSION MODELS. , 1976 .

[15]  Stephen E. Levinson,et al.  Autoregressive Hidden Markov Model and the Speech Signal , 2015, Complex Adaptive Systems.

[16]  G. R. Luckhurst,et al.  Director alignment by crossed electric and magnetic fields: a deuterium NMR study. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[17]  Gordon J. Berman,et al.  Measuring behavior across scales , 2017, BMC Biology.

[18]  M. Brauner,et al.  Caenorhabditis elegans selects distinct crawling and swimming gaits via dopamine and serotonin , 2011, Proceedings of the National Academy of Sciences.

[19]  Yanchun Liang,et al.  Weighted Change-Point Method for Detecting Differential Gene Expression in Breast Cancer Microarray Data , 2012, PloS one.

[20]  P. Schmid,et al.  Dynamic mode decomposition of numerical and experimental data , 2008, Journal of Fluid Mechanics.

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

[22]  Bingni W. Brunton,et al.  Extracting spatial–temporal coherent patterns in large-scale neural recordings using dynamic mode decomposition , 2014, Journal of Neuroscience Methods.

[23]  Emery N Brown,et al.  Dynamics of Propofol-Induced Loss of Consciousness Across Primate Neocortex , 2016, The Journal of Neuroscience.

[24]  N. A. Croll Behavioural analysis of nematode movement. , 1975, Advances in parasitology.

[25]  Yvonne Freer,et al.  Autoregressive Hidden Markov Models for the Early Detection of Neonatal Sepsis , 2014, IEEE Journal of Biomedical and Health Informatics.

[26]  Avelino Javer,et al.  Recurrent Neural Networks with Interpretable Cells Predict and Classify Worm Behaviour , 2017, NIPS 2017.

[27]  Toru Yanagawa,et al.  Loss of Consciousness Is Associated with Stabilization of Cortical Activity , 2015, The Journal of Neuroscience.

[28]  P. Suñé,et al.  Positive Outcomes Influence the Rate and Time to Publication, but Not the Impact Factor of Publications of Clinical Trial Results , 2013, PloS one.

[29]  René Vidal,et al.  The alignment distance on Spaces of Linear Dynamical Systems , 2013, 52nd IEEE Conference on Decision and Control.

[30]  Johannes Zierenberg,et al.  Operating in a Reverberating Regime Enables Rapid Tuning of Network States to Task Requirements , 2018, Front. Syst. Neurosci..

[31]  Carsten O. Daub,et al.  Transcriptional Dynamics Reveal Critical Roles for Non-coding RNAs in the Immediate-Early Response , 2015, PLoS Comput. Biol..

[32]  B. Webb,et al.  Searching for motifs in the behaviour of larval Drosophila melanogaster and Caenorhabditis elegans reveals continuity between behavioural states , 2015, Journal of The Royal Society Interface.

[33]  Guillermo A. Cecchi,et al.  Dynamical and Statistical Criticality in a Model of Neural Tissue , 2008, 0808.3996.

[34]  Ying Chen,et al.  A local vector autoregressive framework and its applications to multivariate time series monitoring and forecasting , 2013 .

[35]  Faicel Chamroukhi,et al.  Joint segmentation of multivariate time series with hidden process regression for human activity recognition , 2013, Neurocomputing.

[36]  Greg J. Stephens,et al.  Dimensionality and Dynamics in the Behavior of C. elegans , 2007, PLoS Comput. Biol..

[37]  Eric Jones,et al.  SciPy: Open Source Scientific Tools for Python , 2001 .

[38]  Mason Klein,et al.  Pan-neuronal imaging in roaming Caenorhabditis elegans , 2015, Proceedings of the National Academy of Sciences.

[39]  Arthur E. Hoerl,et al.  Ridge Regression: Biased Estimation for Nonorthogonal Problems , 2000, Technometrics.

[40]  L. F. Abbott,et al.  Generating Coherent Patterns of Activity from Chaotic Neural Networks , 2009, Neuron.

[41]  L. Avery,et al.  The Geometry of Locomotive Behavioral States in C. elegans , 2013, PloS one.

[42]  F. Santosa,et al.  Linear inversion of ban limit reflection seismograms , 1986 .

[43]  A. Bhardwaj,et al.  In situ click chemistry generation of cyclooxygenase-2 inhibitors , 2017, Nature Communications.

[44]  R. Yuste,et al.  Comprehensive machine learning analysis of Hydra behavior reveals a stable basal behavioral repertoire , 2018, eLife.

[45]  Theodore H. Schwartz,et al.  Dynamical criticality during induction of anesthesia in human ECoG recordings , 2014, Front. Neural Circuits.

[46]  Scott W. Linderman,et al.  The Striatum Organizes 3D Behavior via Moment-to-Moment Action Selection , 2018, Cell.

[47]  Adam J. Calhoun,et al.  Quantifying behavior to solve sensorimotor transformations: advances from worms and flies , 2017, Current Opinion in Neurobiology.

[48]  A. Gomez-Marin,et al.  Hierarchical compression of Caenorhabditis elegans locomotion reveals phenotypic differences in the organization of behaviour , 2015, Journal of The Royal Society Interface.

[49]  L. Abbott,et al.  Beyond the edge of chaos: amplification and temporal integration by recurrent networks in the chaotic regime. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  Yoshinobu Kawahara,et al.  Change-Point Detection in Time-Series Data Based on Subspace Identification , 2007, Seventh IEEE International Conference on Data Mining (ICDM 2007).

[51]  M. Magnasco,et al.  Self-Regulated Dynamical Criticality in Human ECoG , 2012, Front. Integr. Neurosci..

[52]  J. Sulston,et al.  The DNA of Caenorhabditis elegans. , 1974, Genetics.

[53]  E. Ott Chaos in Dynamical Systems: Contents , 2002 .

[54]  Scott W. Linderman,et al.  Bayesian Learning and Inference in Recurrent Switching Linear Dynamical Systems , 2017, AISTATS.

[55]  André E. X. Brown,et al.  Changes in Postural Syntax Characterize Sensory Modulation and Natural Variation of C. elegans Locomotion , 2015, bioRxiv.

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

[57]  Toru Yanagawa,et al.  Untangling Brain-Wide Dynamics in Consciousness by Cross-Embedding , 2015, PLoS Comput. Biol..

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

[59]  Matthew T. Kaufman,et al.  Neural population dynamics during reaching , 2012, Nature.

[60]  Laura J. Grundy,et al.  A dictionary of behavioral motifs reveals clusters of genes affecting Caenorhabditis elegans locomotion , 2012, Proceedings of the National Academy of Sciences.

[61]  S. Olivares,et al.  Full characterization of bipartite entangled states by means of a single homodyne detector , 2009, CLEO/Europe - EQEC 2009 - European Conference on Lasers and Electro-Optics and the European Quantum Electronics Conference.

[62]  J. H. Ward Hierarchical Grouping to Optimize an Objective Function , 1963 .

[63]  James M. Rehg,et al.  Learning and Inferring Motion Patterns using Parametric Segmental Switching Linear Dynamic Systems , 2008, International Journal of Computer Vision.

[64]  Zoran Nikoloski,et al.  Segmentation of biological multivariate time-series data , 2015, Scientific Reports.

[65]  Mark D Humphries,et al.  A spiral attractor network drives rhythmic locomotion , 2017, bioRxiv.

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

[67]  Maxim Volgushev,et al.  Properties of Slow Oscillation during Slow-Wave Sleep and Anesthesia in Cats , 2011, The Journal of Neuroscience.

[68]  Zenas C. Chao,et al.  Large-Scale Information Flow in Conscious and Unconscious States: an ECoG Study in Monkeys , 2013, PloS one.

[69]  Ugne Klibaite,et al.  An unsupervised method for quantifying the behavior of paired animals , 2016, Physical biology.

[70]  Khellil Sefiane,et al.  Experimental investigation of self-induced thermocapillary convection for an evaporating meniscus in capillary tubes using micro-PIV , 2005 .

[71]  Guido Rossum,et al.  Python Reference Manual , 2000 .

[72]  William S Ryu,et al.  Resolving coiled shapes reveals new reorientation behaviors in C. elegans , 2016, eLife.

[73]  Jeremy G Todd,et al.  Systematic exploration of unsupervised methods for mapping behavior , 2016, bioRxiv.

[74]  R. Prevedel,et al.  Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light , 2013, Nature Methods.

[75]  I. Jolliffe A Note on the Use of Principal Components in Regression , 1982 .

[76]  Kenji Yamanishi,et al.  A unifying framework for detecting outliers and change points from time series , 2006, IEEE Transactions on Knowledge and Data Engineering.

[77]  Jack W. Tsao,et al.  Observed brain dynamics, P.P. Mitra, H. Bokil. Oxford University Press (2008), ISBN-13: 978-0-19-517808-1, 381 pages, $65.00 , 2009 .

[78]  Joao Pinheiro Neto,et al.  Operating in a Reverberating Regime Enables Rapid Tuning of Network States to Task Requirements , 2018, Front. Syst. Neurosci..

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

[80]  Yasuo Nagasaka,et al.  Multidimensional Recording (MDR) and Data Sharing: An Ecological Open Research and Educational Platform for Neuroscience , 2011, PloS one.

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

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

[83]  Michael I. Jordan,et al.  Nonparametric Bayesian Learning of Switching Linear Dynamical Systems , 2008, NIPS.

[84]  H. Dette,et al.  Detection of Multiple Structural Breaks in Multivariate Time Series , 2013, 1309.1309.

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

[86]  William Bialek,et al.  Mapping the stereotyped behaviour of freely moving fruit flies , 2013, Journal of The Royal Society Interface.

[87]  Anders Lansner,et al.  Computing the Local Field Potential (LFP) from Integrate-and-Fire Network Models , 2015, PLoS Comput. Biol..

[88]  David J. Freedman,et al.  A hierarchy of intrinsic timescales across primate cortex , 2014, Nature Neuroscience.

[89]  Burak Alakent,et al.  Time series analysis of collective motions in proteins. , 2004, The Journal of chemical physics.

[90]  Theodore H. Lindsay,et al.  Global Brain Dynamics Embed the Motor Command Sequence of Caenorhabditis elegans , 2015, Cell.

[91]  W. Bialek,et al.  Emergence of long timescales and stereotyped behaviors in Caenorhabditis elegans , 2011, Proceedings of the National Academy of Sciences.

[92]  Paulo E. Arratia,et al.  Stretching and mixing of non-Newtonian fluids in time-periodic flows , 2005 .

[93]  J. Guckenheimer,et al.  Finding the dimension of slow dynamics in a rhythmic system , 2012, Journal of The Royal Society Interface.