Rhythmic control of oscillatory sequential dynamics in heteroclinic motifs

Abstract Cognitive/behavioral brain functions are implemented through temporary correlated sequential activity of many brain elements that form universal anatomical and functional motifs, i.e., characteristic functional interactions among brain nodes, at different levels of the neural hierarchy. Such motif dynamics is determined by both the interconnections among nodes and their intrinsic oscillations. This paper focuses on heteroclinic motifs, i.e., those built in networks of oscillatory nodes that interact through asymmetric inhibitory coupling in a winnerless competitive way. We introduce a basic rate-phase motif model – based on a generalization of the well-known ecological Lotka–Volterra model – for the analysis and prediction of control processes that emerge in interacting heteroclinic motifs under periodic stimulation. This approach describes both intensity and phase in each node. We study how a rhythmic signal, which can be linked to internal or external sources, can functionally change the heteroclinic network and produce a rich gallery of motifs in the form of coordinated sequential activations. In computer simulations of the model in a “master-slave” approximation, we report phenomena such as dynamical filtering, encoding enhancement and transition to chaos. Our results are relevant in the context of several experimental protocols related to the role of brain rhythms and/or the use of external rhythmic stimulation, in particular in the context of transcranial control and evoked potentials, to assess cognitive functions and their associated pathologies.

[1]  M. Nitsche,et al.  Exploring prefrontal cortex functions in healthy humans by transcranial electrical stimulation , 2015, Neuroscience Bulletin.

[2]  J. A. Scott Kelso,et al.  Brain coordination dynamics: True and false faces of phase synchrony and metastability , 2009, Progress in Neurobiology.

[3]  Christian Bick,et al.  Dynamical origin of the effective storage capacity in the brain's working memory. , 2009, Physical review letters.

[4]  Brendon O. Watson,et al.  Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease. , 2012, Dialogues in clinical neuroscience.

[5]  A. Selverston,et al.  Dynamical principles in neuroscience , 2006 .

[6]  Andrew A Fingelkurts,et al.  Natural world physical, brain operational, and mind phenomenal space-time. , 2010, Physics of life reviews.

[7]  Xavier Bresson,et al.  Transient networks of spatio-temporal connectivity map communication pathways in brain functional systems , 2017, NeuroImage.

[8]  Kenji Doya,et al.  Near-Saddle-Node Bifurcation Behavior as Dynamics in Working Memory for Goal-Directed Behavior , 1998, Neural Computation.

[9]  N. Matsuki,et al.  Metastability of Active CA3 Networks , 2007, The Journal of Neuroscience.

[10]  Karl J. Friston,et al.  A Hierarchy of Time-Scales and the Brain , 2008, PLoS Comput. Biol..

[11]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[12]  C. Koch,et al.  Ephaptic coupling to endogenous electric field activity: why bother? , 2015, Current Opinion in Neurobiology.

[13]  Christof Koch,et al.  Ephaptic coupling of cortical neurons , 2011, Nature Neuroscience.

[14]  Ramón Huerta,et al.  Dynamical encoding by networks of competing neuron groups: winnerless competition. , 2001 .

[15]  Thomas Nowotny,et al.  Criteria for robustness of heteroclinic cycles in neural microcircuits , 2011, Journal of mathematical neuroscience.

[16]  Michael M. Plichta,et al.  Sequential inhibitory control processes assessed through simultaneous EEG–fMRI , 2014, NeuroImage.

[17]  Gary F. Egan,et al.  Complex spatio-temporal dynamics of fMRI BOLD: A study of motor learning , 2007, NeuroImage.

[18]  Ramón Huerta,et al.  Transient Cognitive Dynamics, Metastability, and Decision Making , 2008, PLoS Comput. Biol..

[19]  M. Murray,et al.  Shaping Intrinsic Neural Oscillations with Periodic Stimulation , 2016, The Journal of Neuroscience.

[20]  J. Kelso,et al.  The Metastable Brain , 2014, Neuron.

[21]  Pablo Varona,et al.  Consciousness as Sequential Dynamics, Robustness, and Mental Disorders. , 2017, JAMA psychiatry.

[22]  Pablo Varona,et al.  Synchronization and coordination of sequences in two neural ensembles. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[23]  Stephen Maren,et al.  Prefrontal-Hippocampal Interactions in Memory and Emotion , 2015, Front. Syst. Neurosci..

[24]  Thomas Nowotny,et al.  Dynamical origin of independent spiking and bursting activity in neural microcircuits. , 2007, Physical review letters.

[25]  C. Miniussi,et al.  New insights into rhythmic brain activity from TMS–EEG studies , 2009, Trends in Cognitive Sciences.

[26]  G. Sperling,et al.  Attentional modulation of SSVEP power depends on the network tagged by the flicker frequency. , 2006, Cerebral cortex.

[27]  Peter J Hellyer,et al.  Cognitive Flexibility through Metastable Neural Dynamics Is Disrupted by Damage to the Structural Connectome , 2015, The Journal of Neuroscience.

[28]  Michael Field,et al.  Patterns of desynchronization and resynchronization in heteroclinic networks , 2017 .

[29]  Søren K. Andersen,et al.  Sustained Multifocal Attentional Enhancement of Stimulus Processing in Early Visual Areas Predicts Tracking Performance , 2013, The Journal of Neuroscience.

[30]  Ruoshi Yuan,et al.  Dynamical behaviors determined by the Lyapunov function in competitive Lotka-Volterra systems. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[32]  Pablo Varona,et al.  Discrete Sequential Information Coding: Heteroclinic Cognitive Dynamics , 2018, Front. Comput. Neurosci..

[33]  Jérémie Lefebvre,et al.  Modulation of Cortical Oscillations by Low-Frequency Direct Cortical Stimulation Is State-Dependent , 2016, PLoS biology.

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

[35]  Thilo Womelsdorf,et al.  A Role of Phase-Resetting in Coordinating Large Scale Neural Networks During Attention and Goal-Directed Behavior , 2016, Front. Syst. Neurosci..

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

[37]  F. Castellanos,et al.  Entrainment of neural oscillations as a modifiable substrate of attention , 2014, Trends in Cognitive Sciences.

[38]  Mariano Sigman,et al.  Parsing a sequence of brain activations at psychological times using fMRI , 2007, NeuroImage.

[39]  C. Herrmann,et al.  Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes , 2013, Front. Hum. Neurosci..

[40]  Gilles Laurent,et al.  Transient Dynamics for Neural Processing , 2008, Science.

[41]  J. Gordon,et al.  Long-range neural synchrony in behavior. , 2015, Annual review of neuroscience.

[42]  Pablo Varona,et al.  Robust Transient Dynamics and Brain Functions , 2011, Front. Comput. Neurosci..

[43]  T. Nowotny,et al.  Dynamics of Odor-Evoked Activity Patterns in the Olfactory System , 2017 .

[44]  C. Herrmann Human EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena , 2001, Experimental Brain Research.

[45]  Karl J. Friston Book Review: Brain Function, Nonlinear Coupling, and Neuronal Transients , 2001 .

[46]  Margaret Wilson,et al.  Rhythmic entrainment: Why humans want to, fireflies can’t help it, pet birds try, and sea lions have to be bribed , 2016, Psychonomic bulletin & review.

[47]  G. Winocur,et al.  Episodic Memory and Beyond: The Hippocampus and Neocortex in Transformation. , 2016, Annual review of psychology.

[48]  Björn Herrmann,et al.  Low-Frequency Neural Oscillations Support Dynamic Attending in Temporal Context , 2014 .

[49]  R. Huerta,et al.  Heteroclinic synchronization: ultrasubharmonic locking. , 2006, Physical review letters.

[50]  Pablo Varona,et al.  Information flow dynamics in the brain. , 2012, Physics of life reviews.

[51]  James P. Crutchfield,et al.  Chaos Forgets and Remembers: Measuring Information Creation, Destruction, and Storage , 2013, ArXiv.

[52]  V. Zhigulin,et al.  On the origin of reproducible sequential activity in neural circuits. , 2004, Chaos.

[53]  Pablo Varona,et al.  Heteroclinic Contours in Neural Ensembles and the Winnerless Competition Principle , 2004, Int. J. Bifurc. Chaos.

[54]  A. Engel,et al.  Antiphasic 40 Hz Oscillatory Current Stimulation Affects Bistable Motion Perception , 2013, Brain Topography.

[55]  Pablo Varona,et al.  Chunking dynamics: heteroclinics in mind , 2014, Front. Comput. Neurosci..

[56]  Aurélia Bugaiska,et al.  The Influence of Music on Prefrontal Cortex during Episodic Encoding and Retrieval of Verbal Information: A Multichannel fNIRS Study , 2015, Behavioural neurology.

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

[58]  Gustavo Deco,et al.  The dynamics of resting fluctuations in the brain: metastability and its dynamical cortical core , 2016, bioRxiv.

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

[60]  A. Engel,et al.  Entrainment of Brain Oscillations by Transcranial Alternating Current Stimulation , 2014, Current Biology.

[61]  P. Schyns,et al.  Entrainment of Perceptually Relevant Brain Oscillations by Non-Invasive Rhythmic Stimulation of the Human Brain , 2011, Front. Psychology.

[62]  P. Varona,et al.  Assisted closed-loop optimization of SSVEP-BCI efficiency , 2012, Front. Neural Circuits.

[63]  Pablo Varona,et al.  Hierarchical nonlinear dynamics of human attention , 2015, Neuroscience & Biobehavioral Reviews.

[64]  C. Miniussi,et al.  The Functional Importance of Rhythmic Activity in the Brain , 2012, Current Biology.

[65]  G. Rauchs,et al.  When Music and Long-Term Memory Interact: Effects of Musical Expertise on Functional and Structural Plasticity in the Hippocampus , 2010, PloS one.

[66]  Rufin VanRullen,et al.  Transcranial Magnetic Stimulation Reveals Intrinsic Perceptual and Attentional Rhythms , 2017, Front. Neurosci..

[67]  Ramón Huerta,et al.  Generation and reshaping of sequences in neural systems , 2006, Biological Cybernetics.

[68]  Pablo Varona,et al.  Dynamical bridge between brain and mind , 2015, Trends in Cognitive Sciences.

[69]  Ramón Huerta,et al.  Reproducible sequence generation in random neural ensembles. , 2004, Physical review letters.

[70]  William D. Penny,et al.  Causal evidence that intrinsic beta-frequency is relevant for enhanced signal propagation in the motor system as shown through rhythmic TMS , 2016, NeuroImage.

[71]  Ned T. Sahin,et al.  Dynamic circuit motifs underlying rhythmic gain control, gating and integration , 2014, Nature Neuroscience.

[72]  M. Lavidor,et al.  Transcranial Alternating Current Stimulation Increases Risk-Taking Behavior in the Balloon Analog Risk Task , 2011, Front. Neurosci..

[73]  Alessandro Barardi,et al.  Probing scale interaction in brain dynamics through synchronization , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[74]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[75]  Karl J. Friston The Variational Principles of Cognition , 2017 .

[76]  Pablo Varona,et al.  Hierarchical dynamics of informational patterns and decision-making , 2016, Proceedings of the Royal Society B: Biological Sciences.

[77]  Walter Paulus,et al.  Spatial Working Memory in Humans Depends on Theta and High Gamma Synchronization in the Prefrontal Cortex , 2016, Current Biology.

[78]  Alexa B. Roggeveen,et al.  Large-scale gamma-band phase synchronization and selective attention. , 2008, Cerebral cortex.

[79]  Torfi Sigurdsson,et al.  Hippocampal-Prefrontal Interactions in Cognition, Behavior and Psychiatric Disease , 2016, Front. Syst. Neurosci..

[80]  Valentin Afraimovich,et al.  Sequential memory: Binding dynamics. , 2015, Chaos.

[81]  Zhengyi Lu,et al.  Three limit cycles for a three-dimensional Lotka-Volterra competitive system with a heteroclinic cycle☆ , 2003 .

[82]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[83]  Timothy Edward John Behrens,et al.  Unmasking Latent Inhibitory Connections in Human Cortex to Reveal Dormant Cortical Memories , 2016, Neuron.

[84]  Danielle S Bassett,et al.  Dynamic network structure of interhemispheric coordination , 2012, Proceedings of the National Academy of Sciences.

[85]  Leonardo L. Gollo,et al.  The frustrated brain: from dynamics on motifs to communities and networks , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[86]  Pablo Varona,et al.  Neural Dynamics of Attentional Cross-Modality Control , 2013, PloS one.

[87]  M. Kringelbach,et al.  Metastability and Coherence: Extending the Communication through Coherence Hypothesis Using A Whole-Brain Computational Perspective , 2016, Trends in Neurosciences.

[88]  G. Buzsáki Rhythms of the brain , 2006 .

[89]  Viktor K. Jirsa,et al.  Transcranial direct current stimulation changes resting state functional connectivity: A large-scale brain network modeling study , 2016, NeuroImage.

[90]  P. Uhlhaas,et al.  Working memory and neural oscillations: alpha–gamma versus theta–gamma codes for distinct WM information? , 2014, Trends in Cognitive Sciences.

[91]  Robert Kozma,et al.  Robust sequential working memory recall in heterogeneous cognitive networks , 2014, Front. Syst. Neurosci..

[92]  Jochen Triesch,et al.  Ongoing brain rhythms shape I-wave properties in a computational model , 2017, Brain Stimulation.

[93]  Peter beim Graben,et al.  Sequences by Metastable Attractors: Interweaving Dynamical Systems and Experimental Data , 2017, Front. Appl. Math. Stat..