Informative and misinformative interactions in a school of fish

Quantifying distributed information processing is crucial to understanding collective motion in animal groups. Recent studies have begun to apply rigorous methods based on information theory to quantify such distributed computation. Following this perspective, we use transfer entropy to quantify dynamic information flows locally in space and time across a school of fish during directional changes around a circular tank, i.e., U-turns. This analysis reveals peaks in information flows during collective U-turns and identifies two different flows: an informative flow (positive transfer entropy) from fish that have already turned to fish that are turning, and a misinformative flow (negative transfer entropy) from fish that have not turned yet to fish that are turning. We also reveal that the information flows are related to relative position and alignment between fish and identify spatial patterns of information and misinformation cascades. This study offers several methodological contributions and we expect further application of these methodologies to reveal intricacies of self-organisation in other animal groups and active matter in general.

[1]  Matthias Bethge,et al.  Beyond GLMs: A Generative Mixture Modeling Approach to Neural System Identification , 2012, PLoS Comput. Biol..

[2]  Claudio J. Tessone,et al.  Dynamical coupling during collective animal motion , 2013, 1311.1417.

[3]  T. Bossomaier,et al.  Transfer entropy as a log-likelihood ratio. , 2012, Physical review letters.

[4]  X. R. Wang,et al.  Quantifying and Tracing Information Cascades in Swarms , 2012, PloS one.

[5]  J. Geweke,et al.  Measurement of Linear Dependence and Feedback between Multiple Time Series , 1982 .

[6]  D. Sumpter,et al.  Inferring the rules of interaction of shoaling fish , 2011, Proceedings of the National Academy of Sciences.

[7]  Sachit Butail,et al.  Information Flow in Animal-Robot Interactions , 2014, Entropy.

[8]  Christopher G. Langton,et al.  Computation at the edge of chaos: Phase transitions and emergent computation , 1990 .

[9]  Guy Theraulaz,et al.  Stigmergic construction and topochemical information shape ant nest architecture , 2016, Proceedings of the National Academy of Sciences.

[10]  Gholam-Ali Hossein-Zadeh,et al.  Long-Range Reduced Predictive Information Transfers of Autistic Youths in EEG Sensor-Space During Face Processing , 2015, Brain Topography.

[11]  Mikhail Prokopenko,et al.  Measuring Information Dynamics in Swarms , 2014 .

[12]  James P. Crutchfield,et al.  Information Flows? A Critique of Transfer Entropies , 2015, Physical review letters.

[13]  P. Kostyrko,et al.  On the symmetric derivative , 1972 .

[14]  Schreiber,et al.  Measuring information transfer , 2000, Physical review letters.

[15]  Joseph T. Lizier,et al.  Measuring the Dynamics of Information Processing on a Local Scale in Time and Space , 2014 .

[16]  Guy Theraulaz,et al.  Task partitioning in a ponerine ant. , 2002, Journal of theoretical biology.

[17]  Larissa Albantakis,et al.  From the Phenomenology to the Mechanisms of Consciousness: Integrated Information Theory 3.0 , 2014, PLoS Comput. Biol..

[18]  F. Ginelli,et al.  Boundary information inflow enhances correlation in flocking. , 2012, Physical review letters.

[19]  P. Lissaman,et al.  Formation Flight of Birds , 1970, Science.

[20]  Randall D. Beer,et al.  Generalized Measures of Information Transfer , 2011, ArXiv.

[21]  Fabrizio Ladu,et al.  Acute caffeine administration affects zebrafish response to a robotic stimulus , 2015, Behavioural Brain Research.

[22]  Mark A. Girolami,et al.  Bat detective—Deep learning tools for bat acoustic signal detection , 2017, bioRxiv.

[23]  X. R. Wang,et al.  Relating Fisher information to order parameters. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[24]  H. Chaté,et al.  Intermittent collective dynamics emerge from conflicting imperatives in sheep herds , 2015, Proceedings of the National Academy of Sciences.

[25]  Albert Y. Zomaya,et al.  Local information transfer as a spatiotemporal filter for complex systems. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[26]  Colin R. Twomey,et al.  Revealing the hidden networks of interaction in mobile animal groups allows prediction of complex behavioral contagion , 2015, Proceedings of the National Academy of Sciences.

[27]  Joseph T. Lizier,et al.  Multivariate construction of effective computational networks from observational data , 2012 .

[28]  Massimo Materassi,et al.  Information Theory Analysis of Cascading Process in a Synthetic Model of Fluid Turbulence , 2014, Entropy.

[29]  Luca Faes,et al.  Lag-Specific Transfer Entropy as a Tool to Assess Cardiovascular and Cardiorespiratory Information Transfer , 2014, IEEE Transactions on Biomedical Engineering.

[30]  Andrea Cavagna,et al.  Collective Behaviour without Collective Order in Wild Swarms of Midges , 2013, PLoS Comput. Biol..

[31]  J. Deneubourg,et al.  Discrete dragline attachment induces aggregation in spiderlings of a solitary species , 2004, Animal Behaviour.

[32]  G. A. Barnard,et al.  Transmission of Information: A Statistical Theory of Communications. , 1961 .

[33]  Nicole Abaid,et al.  A transfer entropy analysis of leader-follower interactions in flying bats , 2015 .

[34]  Guy Theraulaz,et al.  Domino-like propagation of collective U-turns in fish schools , 2017, bioRxiv.

[35]  J. Deneubourg,et al.  Self-organized aggregation in cockroaches , 2005, Animal Behaviour.

[36]  Marco Dorigo,et al.  Swarm intelligence: from natural to artificial systems , 1999 .

[37]  Robert M. May,et al.  Flight formations in geese and other birds , 1979, Nature.

[38]  Guy Theraulaz,et al.  Identifying influential neighbors in animal flocking , 2017, PLoS Comput. Biol..

[39]  Jie Sun,et al.  Inference of Causal Information Flow in Collective Animal Behavior , 2016, IEEE Transactions on Molecular, Biological and Multi-Scale Communications.

[40]  Joseph T. Lizier,et al.  Reduced predictable information in brain signals in autism spectrum disorder , 2014, Front. Neuroinform..

[41]  Guy Theraulaz,et al.  Modeling Collective Animal Behavior with a Cognitive Perspective: A Methodological Framework , 2012, PloS one.

[42]  A. Cavagna,et al.  Diffusion of individual birds in starling flocks , 2012, Proceedings of the Royal Society B: Biological Sciences.

[43]  Arend Hintze,et al.  Evolution of Integrated Causal Structures in Animats Exposed to Environments of Increasing Complexity , 2014, PLoS Comput. Biol..

[44]  Irene Giardina,et al.  Collective behavior in animal groups: Theoretical models and empirical studies , 2008, HFSP journal.

[45]  David J. T. Sumpter,et al.  Initiation and spread of escape waves within animal groups , 2014, Royal Society Open Science.

[47]  A. Ledberg,et al.  When two become one: the limits of causality analysis of brain dynamics. , 2012, PloS one.

[48]  Ruth E. Baker,et al.  Modelling Hair Follicle Growth Dynamics as an Excitable Medium , 2012, PLoS Comput. Biol..

[49]  Albert Y. Zomaya,et al.  Information modification and particle collisions in distributed computation. , 2010, Chaos.

[50]  T. Vicsek,et al.  Context-dependent hierarchies in pigeons , 2013, Proceedings of the National Academy of Sciences.

[51]  I. Couzin,et al.  Inferring the structure and dynamics of interactions in schooling fish , 2011, Proceedings of the National Academy of Sciences.

[52]  Luca Faes,et al.  Conditional Entropy-Based Evaluation of Information Dynamics in Physiological Systems , 2014 .

[53]  G. Parisi,et al.  Interaction ruling animal collective behavior depends on topological rather than metric distance: Evidence from a field study , 2007, Proceedings of the National Academy of Sciences.

[54]  Andrea Cavagna,et al.  Emergence of collective changes in travel direction of starling flocks from individual birds' fluctuations , 2014, Journal of The Royal Society Interface.

[55]  David J. T. Sumpter,et al.  Information transfer in moving animal groups , 2008, Theory in Biosciences.

[56]  Raul Vicente,et al.  Transfer Entropy in Neuroscience , 2014 .

[57]  Yukio-Pegio Gunji,et al.  Information transfer in a swarm of soldier crabs , 2016, Artificial Life and Robotics.

[58]  Oliver Obst,et al.  Quantifying Long-Range Interactions and Coherent Structure in Multi-Agent Dynamics , 2017, Artificial Life.

[59]  Xiaoyi Jiang,et al.  FIMTrack: An open source tracking and locomotion analysis software for small animals , 2017, PLoS Comput. Biol..

[60]  Joseph T. Lizier,et al.  JIDT: An Information-Theoretic Toolkit for Studying the Dynamics of Complex Systems , 2014, Front. Robot. AI.

[61]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[62]  Vasily A. Vakorin,et al.  Confounding effects of indirect connections on causality estimation , 2009, Journal of Neuroscience Methods.

[63]  Viola Priesemann,et al.  Bits from Brains for Biologically Inspired Computing , 2014, Front. Robot. AI.

[64]  Guy Theraulaz,et al.  Deciphering Interactions in Moving Animal Groups , 2012, PLoS Comput. Biol..

[65]  Gordon Pipa,et al.  Transfer entropy—a model-free measure of effective connectivity for the neurosciences , 2010, Journal of Computational Neuroscience.

[66]  Jakob Heinzle,et al.  Multivariate information-theoretic measures reveal directed information structure and task relevant changes in fMRI connectivity , 2010, Journal of Computational Neuroscience.

[67]  Albert Y. Zomaya,et al.  A framework for the local information dynamics of distributed computation in complex systems , 2008, ArXiv.

[68]  Guy Theraulaz,et al.  Disentangling and modeling interactions in fish with burst-and-coast swimming reveal distinct alignment and attraction behaviors , 2017, PLoS Comput. Biol..

[69]  Roman Garnett,et al.  Multi-scale Inference of Interaction Rules in Animal Groups Using Bayesian Model Selection , 2012, PLoS Comput. Biol..

[70]  Guy Theraulaz,et al.  Collective response to perturbations in a data-driven fish school model , 2014, Journal of The Royal Society Interface.

[71]  Yu Sun,et al.  Information Transfer in Swarms with Leaders , 2014, ArXiv.

[72]  Henrik Jeldtoft Jensen,et al.  Quantifying ‘Causality’ in Complex Systems: Understanding Transfer Entropy , 2013, PloS one.

[73]  A. Pérez-Escudero,et al.  idTracker: tracking individuals in a group by automatic identification of unmarked animals , 2014, Nature Methods.

[74]  Mikhail Prokopenko,et al.  Thermodynamics and computation during collective motion near criticality. , 2018, Physical review. E.

[75]  Mikhail Prokopenko,et al.  Information Dynamics in Small-World Boolean Networks , 2011, Artificial Life.

[76]  Nitish Thakor,et al.  Revealing Cross-Frequency Causal Interactions During a Mental Arithmetic Task Through Symbolic Transfer Entropy: A Novel Vector-Quantization Approach , 2016, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[77]  E. Bonabeau,et al.  Spatial patterns in ant colonies , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[78]  Albert Y. Zomaya,et al.  Local measures of information storage in complex distributed computation , 2012, Inf. Sci..

[79]  I. Couzin Collective cognition in animal groups , 2009, Trends in Cognitive Sciences.

[80]  L. Faes,et al.  Information-based detection of nonlinear Granger causality in multivariate processes via a nonuniform embedding technique. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[81]  Carl S. McTague,et al.  The organization of intrinsic computation: complexity-entropy diagrams and the diversity of natural information processing. , 2008, Chaos.

[82]  Mario Ragwitz,et al.  Markov models from data by simple nonlinear time series predictors in delay embedding spaces. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[83]  W. Potts The chorus-line hypothesis of manoeuvre coordination in avian flocks , 1984, Nature.

[84]  Minoru Asada,et al.  Information processing in echo state networks at the edge of chaos , 2011, Theory in Biosciences.

[85]  Dirk Helbing,et al.  Experimental study of the behavioural mechanisms underlying self-organization in human crowds , 2009, Proceedings of the Royal Society B: Biological Sciences.

[86]  Stephen J. Simpson,et al.  Group structure in locust migratory bands , 2011, Behavioral Ecology and Sociobiology.

[87]  A. Seth,et al.  Granger causality and transfer entropy are equivalent for Gaussian variables. , 2009, Physical review letters.

[88]  B. Partridge,et al.  The effect of school size on the structure and dynamics of minnow schools , 1980, Animal Behaviour.

[89]  Craig W. Reynolds Flocks, herds, and schools: a distributed behavioral model , 1987, SIGGRAPH.

[90]  Jean-Louis Deneubourg,et al.  Ant traffic rules , 2010, Journal of Experimental Biology.

[91]  Viola Priesemann,et al.  Measuring Information-Transfer Delays , 2013, PloS one.

[92]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[93]  Giorgio Parisi,et al.  Propagating waves in starling, Sturnus vulgaris, flocks under predation , 2011, Animal Behaviour.

[94]  D. A. Riley,et al.  Multidimensional psychophysics and selective attention in animals. , 1976 .

[95]  Daniel Polani,et al.  Information Flows in Causal Networks , 2008, Adv. Complex Syst..

[96]  T. Bossomaier,et al.  Information flow in a kinetic Ising model peaks in the disordered phase. , 2013, Physical review letters.

[97]  Daniele Marinazzo,et al.  Causal Information Approach to Partial Conditioning in Multivariate Data Sets , 2011, Comput. Math. Methods Medicine.

[98]  Albert Y. Zomaya,et al.  The local information dynamics of distributed computation in complex systems , 2012 .

[99]  Joseph J. Hale,et al.  From Disorder to Order in Marching Locusts , 2006, Science.

[100]  Steven V. Viscido,et al.  Self-Organized Fish Schools: An Examination of Emergent Properties , 2002, The Biological Bulletin.

[101]  Andrea Cavagna,et al.  Information transfer and behavioural inertia in starling flocks , 2013, Nature Physics.

[102]  Jerome Buhl,et al.  Mechanisms underpinning aggregation and collective movement by insect groups. , 2016, Current opinion in insect science.

[103]  Dmitry A Smirnov,et al.  Spurious causalities with transfer entropy. , 2013, Physical review. E, Statistical, nonlinear, and soft matter physics.

[104]  Mikhail Prokopenko,et al.  Differentiating information transfer and causal effect , 2008, 0812.4373.

[105]  T. Vicsek,et al.  Hierarchical group dynamics in pigeon flocks , 2010, Nature.

[106]  W. Bialek,et al.  Statistical mechanics for natural flocks of birds , 2011, Proceedings of the National Academy of Sciences.

[107]  Sachit Butail,et al.  Model-free information-theoretic approach to infer leadership in pairs of zebrafish. , 2016, Physical review. E.

[108]  Iain D. Couzin,et al.  Collective States, Multistability and Transitional Behavior in Schooling Fish , 2013, PLoS Comput. Biol..

[109]  Dirk Helbing,et al.  How simple rules determine pedestrian behavior and crowd disasters , 2011, Proceedings of the National Academy of Sciences.

[110]  Jonathan M. Mudge,et al.  Evidence for Transcript Networks Composed of Chimeric RNAs in Human Cells , 2012, PloS one.