A two-layered brain network model and its chimera state

Based on the data of cerebral cortex, we present a two-layered brain network model of coupled neurons where the two layers represent the left and right hemispheres of cerebral cortex, respectively, and the links between the two layers represent the inter-couplings through the corpus callosum. By this model we show that abundant patterns of synchronization can be observed, especially the chimera state, depending on the parameters of system such as the coupling strengths and coupling phase. Further, we extend the model to a more general two-layered network to better understand the mechanism of the observed patterns, where each hemisphere of cerebral cortex is replaced by a highly clustered subnetwork. We find that the number of inter-couplings is another key parameter for the emergence of chimera states. Thus, the chimera states come from a matching between the structure parameters such as the number of inter-couplings and clustering coefficient etc and the dynamics parameters such as the intra-, inter-coupling strengths and coupling phase etc. A brief theoretical analysis is provided to explain the borderline of synchronization. These findings may provide helpful clues to understand the mechanism of brain functions.

[1]  D. R. Euston,et al.  Fast-Forward Playback of Recent Memory Sequences in Prefrontal Cortex During Sleep , 2007, Science.

[2]  S Yanchuk,et al.  Spectral properties of chimera states. , 2011, Chaos.

[3]  Doru Georg Margineanu,et al.  Epileptic hypersynchrony revisited , 2010, Neuroreport.

[4]  C. Bick,et al.  Controlling chimeras , 2014, 1402.6363.

[5]  O Sporns,et al.  Predicting human resting-state functional connectivity from structural connectivity , 2009, Proceedings of the National Academy of Sciences.

[6]  H. Sakaguchi Instability of synchronized motion in nonlocally coupled neural oscillators. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[7]  J. Cowan,et al.  A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue , 1973, Kybernetik.

[8]  Eckehard Schöll,et al.  Chimera states in complex networks: interplay of fractal topology and delay , 2017, The European Physical Journal Special Topics.

[9]  Francesco Sorrentino,et al.  Complete characterization of the stability of cluster synchronization in complex dynamical networks , 2015, Science Advances.

[10]  Philipp Hövel,et al.  Transition from spatial coherence to incoherence in coupled chaotic systems. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[11]  Hansel,et al.  Clustering and slow switching in globally coupled phase oscillators. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[12]  Joseph D. Hart,et al.  Experimental observation of chimera and cluster states in a minimal globally coupled network. , 2015, Chaos.

[13]  A. Schnitzler,et al.  Normal and pathological oscillatory communication in the brain , 2005, Nature Reviews Neuroscience.

[14]  Guillaume Huyet,et al.  Coherence and incoherence in an optical comb. , 2014, Physical review letters.

[15]  H. Gastaut,et al.  Epilepsy and the functional anatomy of the human brain , 1954 .

[16]  F. S. Borges,et al.  Chimera-like states in a neuronal network model of the cat brain , 2016, 1609.01534.

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

[18]  Arnaud Delorme,et al.  Frontal midline EEG dynamics during working memory , 2005, NeuroImage.

[19]  A. McIntosh,et al.  Mapping cognition to the brain through neural interactions. , 1999, Memory.

[20]  D. Abrams,et al.  Chimera states: coexistence of coherence and incoherence in networks of coupled oscillators , 2014, 1403.6204.

[21]  Chris G. Antonopoulos,et al.  Chimera-like States in Modular Neural Networks , 2015, Scientific Reports.

[22]  M. Wilson,et al.  Coordinated memory replay in the visual cortex and hippocampus during sleep , 2007, Nature Neuroscience.

[23]  Adilson E Motter,et al.  Stable Chimeras and Independently Synchronizable Clusters. , 2017, Physical review letters.

[24]  Philipp Hövel,et al.  Controlling chimera states: The influence of excitable units. , 2016, Physical review. E.

[25]  Changhai Tian,et al.  Asymmetric couplings enhance the transition from chimera state to synchronization. , 2017, Physical review. E.

[26]  Simona Olmi,et al.  Collective chaos in pulse-coupled neural networks , 2010, 1010.2957.

[27]  Eckehard Schöll,et al.  Tweezers for Chimeras in Small Networks. , 2016, Physical review letters.

[28]  Carlo R. Laing,et al.  Fronts and bumps in spatially extended Kuramoto networks , 2011 .

[29]  O. Hallatschek,et al.  Chimera states in mechanical oscillator networks , 2013, Proceedings of the National Academy of Sciences.

[30]  Fatihcan M Atay,et al.  Clustered chimera states in delay-coupled oscillator systems. , 2008, Physical review letters.

[31]  Mattia Frasca,et al.  Pinning control of chimera states. , 2016, Physical review. E.

[32]  Mingzhou Ding,et al.  Enhancement of neural synchrony by time delay. , 2004, Physical review letters.

[33]  M. Balconi,et al.  Consciousness and arousal effects on emotional face processing as revealed by brain oscillations. A gamma band analysis. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[34]  Yuri Maistrenko,et al.  Chimera states in three dimensions , 2015 .

[35]  Eckehard Schöll,et al.  Experimental observations of group synchrony in a system of chaotic optoelectronic oscillators. , 2013, Physical review letters.

[36]  L. Mukhametov,et al.  Interhemispheric asymmetry of the electroencephalographic sleep patterns in dolphins , 1977, Brain Research.

[37]  Junzhong Yang,et al.  The oscillating two-cluster chimera state in non-locally coupled phase oscillators , 2012 .

[38]  Katharina Krischer,et al.  A classification scheme for chimera states. , 2016, Chaos.

[39]  A. Pereda,et al.  Electrical synapses and their functional interactions with chemical synapses , 2014, Nature Reviews Neuroscience.

[40]  Erik A Martens,et al.  Solvable model of spiral wave chimeras. , 2009, Physical review letters.

[41]  Soumen Majhi,et al.  Chimera states in neuronal networks: A review. , 2019, Physics of life reviews.

[42]  Philipp Hövel,et al.  When nonlocal coupling between oscillators becomes stronger: patched synchrony or multichimera states. , 2012, Physical review letters.

[43]  Paolo Massobrio,et al.  Criticality as a signature of healthy neural systems , 2015, Front. Syst. Neurosci..

[44]  Carlo R Laing,et al.  Chimeras in random non-complete networks of phase oscillators. , 2012, Chaos.

[45]  S. L. Lima,et al.  Behavioral, neurophysiological and evolutionary perspectives on unihemispheric sleep , 2000, Neuroscience & Biobehavioral Reviews.

[46]  D. L. Schomer,et al.  Niedermeyer's Electroencephalography: Basic Principles, Clinical Applications, and Related Fields , 2012 .

[47]  T. Sejnowski,et al.  Estimating alertness from the EEG power spectrum , 1997, IEEE Transactions on Biomedical Engineering.

[48]  Peter A Tass,et al.  Chimera states: the natural link between coherence and incoherence. , 2008, Physical review letters.

[49]  Iryna Omelchenko,et al.  Delay controls chimera relay synchronization in multiplex networks , 2018, Physical Review E.

[50]  Liang Wang,et al.  Cluster synchronization in complex network of coupled chaotic circuits: An experimental study , 2018, 1804.00881.

[51]  Louis Pecora,et al.  Symmetry- and input-cluster synchronization in networks. , 2018, Physical review. E.

[52]  R. Miles,et al.  Glutamatergic pre-ictal discharges emerge at the transition to seizure in human epilepsy , 2011, Nature Neuroscience.

[53]  O. Sporns,et al.  From regions to connections and networks: new bridges between brain and behavior , 2016, Current Opinion in Neurobiology.

[54]  E Kopelowitz,et al.  Sensitivity of global network dynamics to local parameters versus motif structure in a cortexlike neuronal model. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[55]  Awadhesh Prasad,et al.  Time-delay-induced phase-transition to synchrony in coupled bursting neurons. , 2011, Chaos.

[56]  Y. Kuramoto,et al.  Coexistence of Coherence and Incoherence in Nonlocally Coupled Phase Oscillators , 2002, cond-mat/0210694.

[57]  Eugene M. Izhikevich,et al.  Polychronization: Computation with Spikes , 2006, Neural Computation.

[58]  N. Lazarides,et al.  Chimeras in SQUID metamaterials , 2014, 1408.6072.

[59]  S. Strogatz,et al.  Chimera states for coupled oscillators. , 2004, Physical review letters.

[60]  Grant M. Fiddyment,et al.  Human seizures couple across spatial scales through travelling wave dynamics , 2017, Nature Communications.

[61]  Edgar Knobloch,et al.  Twisted chimera states and multicore spiral chimera states on a two-dimensional torus. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[62]  R. Miledi,et al.  Miniature Synaptic Potentials in Squid Nerve Cells , 1966, Nature.

[63]  Takeo Watanabe,et al.  Night Watch in One Brain Hemisphere during Sleep Associated with the First-Night Effect in Humans , 2016, Current Biology.

[64]  Tomasz Kapitaniak,et al.  Different types of chimera states: an interplay between spatial and dynamical chaos. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[65]  Zonghua Liu,et al.  A simplified memory network model based on pattern formations , 2014, Scientific Reports.

[66]  B T Thomas Yeo,et al.  The modular and integrative functional architecture of the human brain , 2015, Proceedings of the National Academy of Sciences.

[67]  Fabrice Wendling,et al.  Relevance of nonlinear lumped-parameter models in the analysis of depth-EEG epileptic signals , 2000, Biological Cybernetics.

[68]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[69]  Manuel Schabus,et al.  Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[70]  Anastasios Bezerianos,et al.  Chimera States in Networks of Nonlocally Coupled Hindmarsh-Rose Neuron Models , 2013, Int. J. Bifurc. Chaos.

[71]  Mark J Panaggio,et al.  Chimera states on the surface of a sphere. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[73]  M. Rosenblum,et al.  Partially integrable dynamics of hierarchical populations of coupled oscillators. , 2008, Physical review letters.

[74]  Alain Destexhe,et al.  Ions in the Brain, Normal Function, Seizures, and Stroke, G.G. Somjen. Oxford University Press, Oxford, UK (2004), 432 pages, ISBN: 0195151712 , 2005 .

[75]  R. Roy,et al.  Experimental observation of chimeras in coupled-map lattices , 2012, Nature Physics.

[76]  H. Jasper,et al.  Book Reviews: Epilepsy and the Functional Anatomy of the Human Brain , 1954 .

[77]  Changhai Tian,et al.  Diversity of chimera-like patterns from a model of 2D arrays of neurons with nonlocal coupling , 2017 .

[78]  Katharina Krischer,et al.  Clustering as a prerequisite for chimera states in globally coupled systems. , 2015, Physical review letters.

[79]  O. Omel'chenko,et al.  Coherence–incoherence patterns in a ring of non-locally coupled phase oscillators , 2013 .

[80]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[81]  Markus Siegel,et al.  Phase-dependent neuronal coding of objects in short-term memory , 2009, Proceedings of the National Academy of Sciences.

[82]  J. Kurths,et al.  Structure–function relationship in complex brain networks expressed by hierarchical synchronization , 2007 .

[83]  Ning-Han Liu,et al.  Recognizing the Degree of Human Attention Using EEG Signals from Mobile Sensors , 2013, Sensors.

[84]  L. L. Bologna,et al.  Self-organization and neuronal avalanches in networks of dissociated cortical neurons , 2008, Neuroscience.

[85]  Jan Sieber,et al.  Controlling unstable chaos: stabilizing chimera states by feedback. , 2014, Physical review letters.

[86]  Francesco Sorrentino,et al.  Cluster synchronization and isolated desynchronization in complex networks with symmetries , 2013, Nature Communications.

[87]  Zhigang Zheng,et al.  Chimera states on complex networks. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[88]  K. Showalter,et al.  Chimera and phase-cluster states in populations of coupled chemical oscillators , 2012, Nature Physics.

[89]  Jean M. Vettel,et al.  Controllability of structural brain networks , 2014, Nature Communications.

[90]  Arkady Pikovsky,et al.  Self-emerging and turbulent chimeras in oscillator chains. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[91]  Erik De Schutter,et al.  Computational Modeling Methods for Neuroscientists , 2009 .

[92]  Philipp Hövel,et al.  Robustness of chimera states for coupled FitzHugh-Nagumo oscillators. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[93]  Eckehard Schöll,et al.  Chimera states in brain networks: Empirical neural vs. modular fractal connectivity. , 2017, Chaos.

[94]  Mark J Panaggio,et al.  Chimera states on a flat torus. , 2012, Physical review letters.

[95]  Beom Jun Kim Performance of networks of artificial neurons: the role of clustering. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

[96]  Jean M Vettel,et al.  Cognitive chimera states in human brain networks , 2018, Science Advances.

[97]  Eckehard Schöll,et al.  Amplitude-phase coupling drives chimera states in globally coupled laser networks. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[98]  P. Hövel,et al.  Loss of coherence in dynamical networks: spatial chaos and chimera states. , 2011, Physical review letters.

[99]  Soumen Majhi,et al.  Chimera states in a multilayer network of coupled and uncoupled neurons. , 2017, Chaos.

[100]  John A. Lesku,et al.  Asynchronous Eye Closure as an Anti‐Predator Behavior in the Western Fence Lizard (Sceloporus occidentalis) , 2006 .

[101]  Eckehard Schöll,et al.  Coherence-Resonance Chimeras in a Network of Excitable Elements. , 2015, Physical review letters.

[102]  A. Pikovsky,et al.  Resolving clusters in chaotic ensembles of globally coupled identical oscillators. , 2001, Physical review letters.

[103]  S Yanchuk,et al.  Stationary patterns of coherence and incoherence in two-dimensional arrays of non-locally-coupled phase oscillators. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[104]  Danielle S Bassett,et al.  Data-driven brain network models differentiate variability across language tasks , 2018, PLoS Comput. Biol..

[105]  V N Belykh,et al.  Cluster synchronization modes in an ensemble of coupled chaotic oscillators. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[106]  R. Miledi,et al.  Spontaneous synaptic potentials and quantal release of transmitter in the stellate ganglion of the squid , 1967, The Journal of physiology.

[107]  Danielle Smith Bassett,et al.  Small-World Brain Networks , 2006, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[108]  Tomasz Kapitaniak,et al.  Chimera states on the route from coherence to rotating waves. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[109]  Zonghua Liu,et al.  Robust features of chimera states and the implementation of alternating chimera states , 2010 .

[110]  W. Singer,et al.  Neural Synchrony in Brain Disorders: Relevance for Cognitive Dysfunctions and Pathophysiology , 2006, Neuron.

[111]  E. Ott,et al.  Network synchronization of groups. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[112]  S. Strogatz,et al.  Solvable model for chimera states of coupled oscillators. , 2008, Physical review letters.