Synchronization by uncorrelated noise: interacting rhythms in interconnected oscillator networks

Oscillators coupled in a network can synchronize with each other to yield a coherent population rhythm. How do multiple such rhythms interact with each other? Do these collective oscillations synchronize like individual oscillators? We show that this is not the case: for strong, inhibitory coupling rhythms can become synchronized by noise. In contrast to stochastic synchronization, this new mechanism synchronizes the rhythms even if the noisy inputs to different oscillators are completely uncorrelated. Key for the synchrony across networks is the reduced synchrony within the networks: it substantially increases the frequency range across which the networks can be entrained by other networks or by periodic pacemaker-like inputs. We demonstrate this type of robust synchronization for different classes of oscillators and network connectivities. The synchronization of different population rhythms is expected to be relevant for brain rhythms.

[1]  Wiesenfeld,et al.  Synchronization transitions in a disordered Josephson series array. , 1996, Physical review letters.

[2]  M. Elowitz,et al.  Modeling a synthetic multicellular clock: repressilators coupled by quorum sensing. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Yoji Kawamura,et al.  Phase synchronization between collective rhythms of globally coupled oscillator groups: noisy identical case. , 2010, Chaos.

[4]  Gerald J. Sun,et al.  Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb , 2016, Neuron.

[5]  Jurgen Kurths,et al.  Synchronization in complex networks , 2008, 0805.2976.

[6]  Fiona E. N. LeBeau,et al.  Multiple origins of the cortical gamma rhythm , 2011, Developmental neurobiology.

[7]  A. Barabasi,et al.  Hierarchical Organization of Modularity in Metabolic Networks , 2002, Science.

[8]  Xiao-Jing Wang Neurophysiological and computational principles of cortical rhythms in cognition. , 2010, Physiological reviews.

[9]  Bard Ermentrout,et al.  Type I Membranes, Phase Resetting Curves, and Synchrony , 1996, Neural Computation.

[10]  A. F. Adams,et al.  The Survey , 2021, Dyslexia in Higher Education.

[11]  Michael J Rust,et al.  The cyanobacterial clock and metabolism. , 2014, Current opinion in microbiology.

[12]  Eric Shea-Brown,et al.  Correlation and synchrony transfer in integrate-and-fire neurons: basic properties and consequences for coding. , 2008, Physical review letters.

[13]  B. Bassler,et al.  Quorum sensing in bacteria. , 2001, Annual review of microbiology.

[14]  T. Sejnowski,et al.  Cortical Enlightenment: Are Attentional Gamma Oscillations Driven by ING or PING? , 2009, Neuron.

[15]  R. C. Compton,et al.  Quasi-optical power combining using mutually synchronized oscillator arrays , 1991 .

[16]  György Buzsáki,et al.  What does gamma coherence tell us about inter-regional neural communication? , 2015, Nature Neuroscience.

[17]  Xuchen Han,et al.  Top-down inputs drive neuronal network rewiring and context-enhanced sensory processing in olfaction , 2018, bioRxiv.

[18]  Xiao-Jing Wang,et al.  What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. , 2003, Journal of neurophysiology.

[19]  P. Fries Rhythms for Cognition: Communication through Coherence , 2015, Neuron.

[20]  P H Tiesinga,et al.  Robust gamma oscillations in networks of inhibitory hippocampal interneurons , 1999, Network.

[21]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[22]  Nicolas Brunel,et al.  Fast Global Oscillations in Networks of Integrate-and-Fire Neurons with Low Firing Rates , 1999, Neural Computation.

[23]  L. Haberly,et al.  Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. , 2003, Journal of neurophysiology.

[24]  Hiroyuki Kitajima,et al.  Bifurcations in Morris-Lecar neuron model , 2006, Neurocomputing.

[25]  Florian Dörfler,et al.  Synchronization in complex networks of phase oscillators: A survey , 2014, Autom..

[26]  E Oh,et al.  Modular synchronization in complex networks. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  J. Teramae,et al.  Robustness of the noise-induced phase synchronization in a general class of limit cycle oscillators. , 2004, Physical review letters.

[28]  Kenneth Showalter,et al.  Chimera and chimera-like states in populations of nonlocally coupled homogeneous and heterogeneous chemical oscillators. , 2016, Chaos.

[29]  Richard E. Harang,et al.  A neuropeptide speeds circadian entrainment by reducing intercellular synchrony , 2013, Proceedings of the National Academy of Sciences.

[30]  Jürgen Kurths,et al.  Noise-induced phase synchronization and synchronization transitions in chaotic oscillators. , 2002, Physical review letters.

[31]  I. Mihalcescu,et al.  Cyanobacterial clock, a stable phase oscillator with negligible intercellular coupling , 2007, Proceedings of the National Academy of Sciences.

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

[33]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[34]  T. Sejnowski,et al.  Reliability of spike timing in neocortical neurons. , 1995, Science.

[35]  G. Buzsáki,et al.  Mechanisms of gamma oscillations. , 2012, Annual review of neuroscience.

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

[37]  Gilmore J. Dunning,et al.  Self-organized coherence in fiber laser arrays , 2004, SPIE LASE.

[38]  A. Goldbeter,et al.  Systems biology of cellular rhythms , 2012, FEBS letters.

[39]  Nancy Kopell,et al.  Gamma Oscillations and Stimulus Selection , 2008, Neural Computation.

[40]  Steven H. Strogatz,et al.  Nonlinear Dynamics and Chaos , 2024 .

[41]  Ying-Cheng Lai,et al.  Synchronization in complex networks with a modular structure. , 2006, Chaos.

[42]  P. Jonas,et al.  Shunting Inhibition Improves Robustness of Gamma Oscillations in Hippocampal Interneuron Networks by Homogenizing Firing Rates , 2006, Neuron.

[43]  Bernd Blasius,et al.  Complex dynamics and phase synchronization in spatially extended ecological systems , 1999, Nature.

[44]  Hermann Riecke,et al.  Neurogenesis Drives Stimulus Decorrelation in a Model of the Olfactory Bulb , 2012, PLoS Comput. Biol..

[45]  Steven H. Strogatz,et al.  Cellular Construction of a Circadian Clock: Period Determination in the Suprachiasmatic Nuclei , 1997, Cell.

[46]  J. Jalife,et al.  Mechanisms of Sinoatrial Pacemaker Synchronization: A New Hypothesis , 1987, Circulation research.

[47]  Bard Ermentrout,et al.  Correlation transfer in stochastically driven neural oscillators over long and short time scales. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[48]  Bard Ermentrout,et al.  Complex dynamics in winner-take-all neural nets with slow inhibition , 1992, Neural Networks.

[49]  P. McEuen,et al.  Synchronization of micromechanical oscillators using light , 2011, IEEE Photonic Society 24th Annual Meeting.

[50]  P. Fries,et al.  Robust Gamma Coherence between Macaque V1 and V2 by Dynamic Frequency Matching , 2013, Neuron.

[51]  J. Hasty,et al.  Synchronizing genetic relaxation oscillators by intercell signaling , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Leslie M Kay,et al.  How global are olfactory bulb oscillations? , 2010, Journal of neurophysiology.

[53]  B. Ermentrout,et al.  An adaptive model for synchrony in the firefly Pteroptyx malaccae , 1991 .

[54]  Hermann Riecke,et al.  Independent Noise Synchronizing Networks of Oscillator Networks , 2016, 1612.06881.

[55]  R. Desimone,et al.  Gamma-band synchronization in visual cortex predicts speed of change detection , 2006, Nature.

[56]  Ying-Cheng Lai,et al.  Transition to global synchronization in clustered networks. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[57]  R. Traub,et al.  Inhibition-based rhythms: experimental and mathematical observations on network dynamics. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[58]  T. Womelsdorf,et al.  Attentional Stimulus Selection through Selective Synchronization between Monkey Visual Areas , 2012, Neuron.

[59]  Nancy Kopell,et al.  Synchronization in Networks of Excitatory and Inhibitory Neurons with Sparse, Random Connectivity , 2003, Neural Computation.

[60]  Thomas K. D. M. Peron,et al.  The Kuramoto model in complex networks , 2015, 1511.07139.

[61]  T. Kondo,et al.  Autonomous synchronization of the circadian KaiC phosphorylation rhythm , 2007, Nature Structural &Molecular Biology.

[62]  J. Tyson,et al.  A simple model of circadian rhythms based on dimerization and proteolysis of PER and TIM. , 1999, Biophysical journal.