Transmission delays and frequency detuning can regulate information flow between brain regions

Brain networks exhibit very variable and dynamical functional connectivity and flexible configurations of information exchange despite their overall fixed structure (connectome). Brain oscillations are hypothesized to underlie time-dependent functional connectivity by periodically changing the excitability of neural populations. In this paper, we investigate the role that the connection delay and the frequency detuning between different neural populations play in the transmission of signals. Based on numerical simulations and analytical arguments, we show that the amount of information transfer between two oscillating neural populations can be determined solely by their connection delay and the mismatch in their oscillation frequencies. Our results highlight the role of the collective phase response curve of the oscillating neural populations for the efficacy of signal transmission and the quality of the information transfer in brain networks. Author summary Collective dynamics in brain networks is characterized by a coordinated activity of their constituent neurons that lead to brain oscillations. Many evidences highlight the role that brain oscillations play in signal transmission, the control of the effective communication between brain areas and the integration of information processed by different specialized regions. Oscillations periodically modulate the excitability of neurons and determine the response those areas receiving the signals. Based on the communication trough coherence (CTC) theory, the adjustment of the phase difference between local oscillations of connected areas can specify the timing of exchanged signals and therefore, the efficacy of the communication channels. An important factor is the delay in the transmission of signals from one region to another that affects the phase difference and timing, and consequently the impact of the signals. Despite this delay plays an essential role in CTC theory, its role has been mostly overlooked in previous studies. In this manuscript, we concentrate on the role that the connection delay and the oscillation frequency of the populations play in the signal transmission, and consequently in the effective connectivity, between two brain areas. Through extensive numerical simulations, as well as analytical results with reduced models, we show that these parameters have two essential impacts on the effective connectivity of the neural networks: First, that the populations advancing in phase to others do not necessarily play the role of the information source; and second, that the amount and direction of information transfer dependents on the oscillation frequency of the populations.

[1]  P. Fries,et al.  Both ongoing alpha and visually induced gamma oscillations show reliable diversity in their across-site phase-relations. , 2015, Journal of neurophysiology.

[2]  C. Felser,et al.  Negative magnetoresistance without well-defined chirality in the Weyl semimetal TaP , 2015, Nature Communications.

[3]  Nicolas Brunel,et al.  Dynamics of Sparsely Connected Networks of Excitatory and Inhibitory Spiking Neurons , 2000, Journal of Computational Neuroscience.

[4]  Leonardo L. Gollo,et al.  Modeling positive Granger causality and negative phase lag between cortical areas , 2014, NeuroImage.

[5]  Olaf Sporns,et al.  THE HUMAN CONNECTOME: A COMPLEX NETWORK , 2011, Schizophrenia Research.

[6]  Robert J. Butera,et al.  Comprar Phase Response Curves In Neuroscience. Theory, Experiment And Analysis (Springer Series In Computational Neuroscience, Vol. 6) | Robert J. Butera | 9781461407386 | Springer , 2012 .

[7]  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.

[8]  Claudio R Mirasso,et al.  Anticipated and zero-lag synchronization in motifs of delay-coupled systems. , 2017, Chaos.

[9]  Wulfram Gerstner,et al.  Spike-timing dependent plasticity , 2010, Scholarpedia.

[10]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[11]  Robert J. Butera,et al.  Phase Response Curves in Neuroscience , 2012, Springer Series in Computational Neuroscience.

[12]  G Bard Ermentrout,et al.  Phase-response curves and synchronized neural networks , 2010, Philosophical Transactions of the Royal Society B: Biological Sciences.

[13]  Terrence J. Sejnowski,et al.  Mechanisms for Phase Shifting in Cortical Networks and their Role in Communication through Coherence , 2010, Front. Hum. Neurosci..

[14]  Alessandro Barardi,et al.  Phase-Coherence Transitions and Communication in the Gamma Range between Delay-Coupled Neuronal Populations , 2014, PLoS Comput. Biol..

[15]  H. Jörntell Cerebellar Neuronal Codes-Perspectives from Intracellular Analysis In Vivo , 2015 .

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

[17]  I. Peretz,et al.  Individual Differences in Rhythmic Cortical Entrainment Correlate with Predictive Behavior in Sensorimotor Synchronization , 2016, Scientific Reports.

[18]  Alexandre Hyafil,et al.  Speech encoding by coupled cortical theta and gamma oscillations , 2015, eLife.

[19]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[20]  V. Booth,et al.  Collective phase response curves for heterogeneous coupled oscillators. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[21]  A. Pikovsky,et al.  Phase resetting of collective rhythm in ensembles of oscillators. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  E. Miller,et al.  Gamma and Beta Bursts Underlie Working Memory , 2016, Neuron.

[23]  E. Miller,et al.  Goal-direction and top-down control , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[24]  Alireza Valizadeh,et al.  Zero-Lag Synchronization Despite Inhomogeneities in a Relay System , 2014, PloS one.

[25]  E. Moser,et al.  Gamma oscillations in the hippocampus. , 2010, Physiology.

[26]  T. Womelsdorf,et al.  The role of neuronal synchronization in selective attention , 2007, Current Opinion in Neurobiology.

[27]  Michael N. Economo,et al.  Membrane potential‐dependent integration of synaptic inputs in entorhinal stellate neurons , 2014, Hippocampus.

[28]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[29]  O. Sporns Discovering the Human Connectome , 2012 .

[30]  E. Miller,et al.  Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices , 2007, Science.

[31]  T. Curran,et al.  Functional role of gamma and theta oscillations in episodic memory , 2010, Neuroscience & Biobehavioral Reviews.

[32]  Bryan C. Souza,et al.  Theta-associated high-frequency oscillations (110–160Hz) in the hippocampus and neocortex , 2013, Progress in Neurobiology.

[33]  Andrea Brovelli,et al.  Functional connectivity and neuronal dynamics: insights from computational methods , 2020 .

[34]  Miles A. Whittington,et al.  Neurosystems: brain rhythms and cognitive processing , 2013, The European journal of neuroscience.

[35]  P. Brown,et al.  New insights into the relationship between dopamine, beta oscillations and motor function , 2011, Trends in Neurosciences.

[36]  S. Sadeghi,et al.  Synchronization of delayed coupled neurons in presence of inhomogeneity , 2012, Journal of Computational Neuroscience.

[37]  Ayan S. Waite,et al.  Layer and rhythm specificity for predictive routing , 2020, Proceedings of the National Academy of Sciences.

[38]  Raul Vicente,et al.  Zero-lag long-range synchronization via dynamical relaying. , 2006, Physical review letters.

[39]  Marc Timme,et al.  Dynamic information routing in complex networks , 2015, Nature Communications.

[40]  Jordi García-Ojalvo,et al.  Role of frequency mismatch in neuronal communication through coherence , 2014, Journal of Computational Neuroscience.

[41]  Olaf Sporns,et al.  Neurobiologically Realistic Determinants of Self-Organized Criticality in Networks of Spiking Neurons , 2011, PLoS Comput. Biol..

[42]  Andreas K. Engel,et al.  Temporal Binding, Binocular Rivalry, and Consciousness , 1999, Consciousness and Cognition.

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

[44]  H. Kennedy,et al.  Visual Areas Exert Feedforward and Feedback Influences through Distinct Frequency Channels , 2014, Neuron.

[45]  Leonardo L. Gollo,et al.  Stimulus-dependent synchronization in delayed-coupled neuronal networks , 2016, Scientific Reports.

[46]  Annette Witt,et al.  Dynamic Effective Connectivity of Inter-Areal Brain Circuits , 2011, PLoS Comput. Biol..

[47]  Claudio R. Mirasso,et al.  Anticipated synchronization in neuronal circuits unveiled by a phase-response-curve analysis. , 2017, Physical review. E.

[48]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[49]  Ad Aertsen,et al.  Facilitating the propagation of spiking activity in feedforward networks by including feedback , 2019, bioRxiv.

[50]  Gordon Pipa,et al.  Effect of the Topology and Delayed Interactions in Neuronal Networks Synchronization , 2011, PloS one.

[51]  Nicolas Brunel,et al.  Contributions of intrinsic membrane dynamics to fast network oscillations with irregular neuronal discharges. , 2005, Journal of neurophysiology.

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

[53]  P. Fries,et al.  Diverse Phase Relations among Neuronal Rhythms and Their Potential Function , 2016, Trends in Neurosciences.

[54]  Simon Hanslmayr,et al.  The role of alpha oscillations in temporal attention , 2011, Brain Research Reviews.

[55]  W. Klimesch,et al.  What does phase information of oscillatory brain activity tell us about cognitive processes? , 2008, Neuroscience & Biobehavioral Reviews.

[56]  Yoji Kawamura,et al.  Collective phase dynamics of globally coupled oscillators: Noise-induced anti-phase synchronization ✩ , 2013, 1312.7054.

[57]  Michael N. Shadlen,et al.  Noise, neural codes and cortical organization , 1994, Current Opinion in Neurobiology.

[58]  H. Kennedy,et al.  Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas , 2016, Neuron.

[59]  T. Womelsdorf,et al.  Neuronal coherence during selective attentional processing and sensory–motor integration , 2006, Journal of Physiology-Paris.

[60]  E. P. Lowet,et al.  On the operation of visual cortical gamma in the light of frequency variation , 2016 .

[61]  P. Fries A mechanism for cognitive dynamics: neuronal communication through neuronal coherence , 2005, Trends in Cognitive Sciences.

[62]  Harvey Swadlow,et al.  Axonal conduction delays , 2012, Scholarpedia.

[63]  P. Dayan,et al.  Supporting Online Material Materials and Methods Som Text Figs. S1 to S9 References the Asynchronous State in Cortical Circuits , 2022 .

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

[65]  J. Palva,et al.  Phase Synchrony among Neuronal Oscillations in the Human Cortex , 2005, The Journal of Neuroscience.

[66]  R. Quian Quiroga Principles of neural coding. , 2011, Current biology : CB.

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

[68]  Arne D. Ekstrom,et al.  Brain Oscillations Control Timing of Single-Neuron Activity in Humans , 2007, The Journal of Neuroscience.

[69]  Olaf Sporns,et al.  Mechanisms of Zero-Lag Synchronization in Cortical Motifs , 2013, PLoS Comput. Biol..

[70]  Nicolas Brunel,et al.  Sparsely synchronized neuronal oscillations. , 2008, Chaos.

[71]  G B Ermentrout,et al.  Fine structure of neural spiking and synchronization in the presence of conduction delays. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[72]  W. Singer,et al.  The gamma cycle , 2007, Trends in Neurosciences.

[73]  J. Fell,et al.  The role of phase synchronization in memory processes , 2011, Nature Reviews Neuroscience.

[74]  Ad Aertsen,et al.  Portraits of communication in neuronal networks , 2018, Nature Reviews Neuroscience.

[75]  Alireza Valizadeh,et al.  High frequency neurons determine effective connectivity in neuronal networks , 2018, NeuroImage.

[76]  Ingo Fischer,et al.  Simultaneous bidirectional message transmission in a chaos-based communication scheme. , 2007, Optics letters.

[77]  Arvind Kumar,et al.  Communication through Resonance in Spiking Neuronal Networks , 2014, PLoS Comput. Biol..

[78]  Fred Wolf,et al.  Flexible information routing by transient synchrony , 2017, Nature Neuroscience.

[79]  Leonardo L. Gollo,et al.  Dynamical relaying can yield zero time lag neuronal synchrony despite long conduction delays , 2008, Proceedings of the National Academy of Sciences.

[80]  Yoji Kawamura,et al.  Collective-phase description of coupled oscillators with general network structure. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[81]  Roger D. Traub,et al.  Dual Gamma Rhythm Generators Control Interlaminar Synchrony in Auditory Cortex , 2011, The Journal of Neuroscience.

[82]  Fiona E. N. LeBeau,et al.  GABA-enhanced collective behavior in neuronal axons underlies persistent gamma-frequency oscillations , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[83]  R. Spigler,et al.  The Kuramoto model: A simple paradigm for synchronization phenomena , 2005 .