A neural mass model of phase–amplitude coupling

Brain activity shows phase–amplitude coupling between its slow and fast oscillatory components. We study phase–amplitude coupling as recorded at individual sites, using a modified version of the well-known Wendling neural mass model. To the population of fast inhibitory interneurons of this model, we added external modulatory input and dynamic self-feedback. These two modifications together are sufficient to let the inhibitory population serve as a limit-cycle oscillator, with frequency characteristics comparable to the beta and gamma bands. The frequency and power of these oscillations can be tuned through the time constant of the dynamic and modulatory input. Alpha band activity is generated, as is usual in such models, as a result of interactions of pyramidal neurons and a population of slow inhibitory interneurons. The slow inhibitory population activity directly influences the fast oscillations via the synaptic gain between slow and fast inhibitory populations. As a result, the amplitude envelope of the fast oscillation is coupled to the phase of the slow activity; this result is consistent with the notion that phase–amplitude coupling is effectuated by interactions between inhibitory interneurons.

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

[2]  G. Alarcón,et al.  Power spectrum and intracranial EEG patterns at seizure onset in partial epilepsy. , 1995, Electroencephalography and clinical neurophysiology.

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

[4]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[5]  Leonidas D. Iasemidis,et al.  Controlling epileptic seizures in a neural mass model , 2009, J. Comb. Optim..

[6]  Karl J. Friston,et al.  Evaluation of different measures of functional connectivity using a neural mass model , 2004, NeuroImage.

[7]  L. Finkel,et al.  Ketamine Disrupts Theta Modulation of Gamma in a Computer Model of Hippocampus , 2011, The Journal of Neuroscience.

[8]  W. Freeman Mass action in the nervous system : examination of the neurophysiological basis of adaptive behavior through the EEG , 1975 .

[9]  Michael X. Cohen,et al.  Sustained Neural Activity Patterns during Working Memory in the Human Medial Temporal Lobe , 2007, The Journal of Neuroscience.

[10]  F. H. Lopes da Silva,et al.  Model of brain rhythmic activity , 1974, Kybernetik.

[11]  F. H. Lopes da Silva,et al.  Models of neuronal populations: the basic mechanisms of rhythmicity. , 1976, Progress in brain research.

[12]  Pablo Fuentealba,et al.  Cell Type-Specific Tuning of Hippocampal Interneuron Firing during Gamma Oscillations In Vivo , 2007, The Journal of Neuroscience.

[13]  Damien Coyle,et al.  A thalamo-cortico-thalamic neural mass model to study alpha rhythms in Alzheimer's disease , 2011, Neural Networks.

[14]  Olivier D. Faugeras,et al.  Bifurcation Analysis of Jansen's Neural Mass Model , 2006, Neural Computation.

[15]  J. Bellanger,et al.  Epileptic fast activity can be explained by a model of impaired GABAergic dendritic inhibition , 2002, The European journal of neuroscience.

[16]  Stephen Coombes,et al.  Large-scale neural dynamics: Simple and complex , 2010, NeuroImage.

[17]  Gordon Pipa,et al.  Untangling cross-frequency coupling in neuroscience , 2014 .

[18]  M. Scanziani,et al.  It's about time for thalamocortical circuits , 2007, Nature Neuroscience.

[19]  R. Schmidt,et al.  Cross-Frequency Phase–Phase Coupling between Theta and Gamma Oscillations in the Hippocampus , 2012, The Journal of Neuroscience.

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

[21]  M. Kahana,et al.  Reset of human neocortical oscillations during a working memory task , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[22]  F. Skinner THE EFFECT OF SYNAPTIC DEPRESSION ON MODEL INHIBITORY NETWORKS , 2022 .

[23]  R. Eckhorn,et al.  Task-related coupling from high- to low-frequency signals among visual cortical areas in human subdural recordings. , 2004, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[24]  G Buzsáki,et al.  The hippocampo-neocortical dialogue. , 1996, Cerebral cortex.

[25]  K. Miller,et al.  Exaggerated phase–amplitude coupling in the primary motor cortex in Parkinson disease , 2013, Proceedings of the National Academy of Sciences.

[26]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[27]  György Buzsáki,et al.  Oscillatory and Intermittent Synchrony in the Hippocampus: Relevance to Memory Trace Formation , 1994 .

[28]  J. Touboul,et al.  Codimension Two Bifurcations and Rythms in Neural Mass Models , 2009, 0907.2718.

[29]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Karl J. Friston,et al.  Behavioral / Systems / Cognitive Connectivity Changes Underlying Spectral EEG Changes during Propofol-Induced Loss of Consciousness , 2012 .

[31]  R. Knight,et al.  Shifts in Gamma Phase–Amplitude Coupling Frequency from Theta to Alpha Over Posterior Cortex During Visual Tasks , 2010, Front. Hum. Neurosci..

[32]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[33]  Y. Kamitani,et al.  Regulation of Motor Representation by Phase–Amplitude Coupling in the Sensorimotor Cortex , 2012, The Journal of Neuroscience.

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

[35]  Karl J. Friston,et al.  a K.E. Stephan, a R.B. Reilly, , 2007 .

[36]  H. Eichenbaum,et al.  Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. , 2010, Journal of neurophysiology.

[37]  R. Meddis,et al.  A computer model of amplitude-modulation sensitivity of single units in the inferior colliculus. , 1994, The Journal of the Acoustical Society of America.

[38]  Wolfgang Klimesch,et al.  A short review of slow phase synchronization and memory: Evidence for control processes in different memory systems? , 2008, Brain Research.

[39]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[40]  Carson C. Chow,et al.  Synchronization and Oscillatory Dynamics in Heterogeneous, Mutually Inhibited Neurons , 1998, Journal of Computational Neuroscience.

[41]  Miles A Whittington,et al.  Interneuron Diversity series: Inhibitory interneurons and network oscillations in vitro , 2003, Trends in Neurosciences.

[42]  Michael X. Cohen,et al.  Oscillatory Activity and Phase–Amplitude Coupling in the Human Medial Frontal Cortex during Decision Making , 2009, Journal of Cognitive Neuroscience.

[43]  J. Lisman The theta/gamma discrete phase code occuring during the hippocampal phase precession may be a more general brain coding scheme , 2005, Hippocampus.

[44]  Correction: Ih Tunes Theta/Gamma Oscillations and Cross-Frequency Coupling In an In Silico CA3 Model , 2013, PLoS ONE.

[45]  T. Hafting,et al.  Frequency of gamma oscillations routes flow of information in the hippocampus , 2009, Nature.

[46]  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.

[47]  Ben H. Jansen,et al.  Electroencephalogram and visual evoked potential generation in a mathematical model of coupled cortical columns , 1995, Biological Cybernetics.

[48]  Theiler,et al.  Generating surrogate data for time series with several simultaneously measured variables. , 1994, Physical review letters.

[49]  Karl J. Friston,et al.  Modelling event-related responses in the brain , 2005, NeuroImage.

[50]  Karl J. Friston,et al.  The Dynamic Brain: From Spiking Neurons to Neural Masses and Cortical Fields , 2008, PLoS Comput. Biol..

[51]  A. Thomson,et al.  Interlaminar connections in the neocortex. , 2003, Cerebral cortex.

[52]  Mauro Ursino,et al.  A thalamo-cortical neural mass model for the simulation of brain rhythms during sleep , 2013, Journal of Computational Neuroscience.

[53]  Andreas Spiegler,et al.  Bifurcation Analysis of Neural Mass Models , 2010 .

[54]  H. Markram,et al.  Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. , 2000, Science.

[55]  Weidong Zhou,et al.  Bifurcation and oscillation in a time-delay neural mass model , 2014, Biological Cybernetics.

[56]  G. Buzsáki,et al.  Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[57]  O. Paulsen,et al.  Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro , 1998, Nature.

[58]  E. Callaway,et al.  Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons , 2000, Nature Neuroscience.

[59]  G. Buzsáki,et al.  Hippocampal CA1 interneurons: an in vivo intracellular labeling study , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  W. Lytton,et al.  Ih Tunes Theta/Gamma Oscillations and Cross-Frequency Coupling In an In Silico CA3 Model , 2013, PloS one.

[61]  Ben H. Jansen,et al.  A neurophysiologically-based mathematical model of flash visual evoked potentials , 2004, Biological Cybernetics.

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

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

[64]  Cees van Leeuwen,et al.  Efficiency of Conscious Access Improves with Coupling of Slow and Fast Neural Oscillations , 2014, Journal of Cognitive Neuroscience.

[65]  Adriano B. L. Tort,et al.  Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons , 2009, Proceedings of the National Academy of Sciences.

[66]  A. Agmon,et al.  Short-Term Plasticity of Unitary Inhibitory-to-Inhibitory Synapses Depends on the Presynaptic Interneuron Subtype , 2012, The Journal of Neuroscience.

[67]  Song Liu,et al.  Variable Bandwidth Filtering for Improved Sensitivity of Cross-Frequency Coupling Metrics , 2012, Brain Connect..

[68]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[69]  Jarmo A. Hämäläinen,et al.  Reduced phase locking to slow amplitude modulation in adults with dyslexia: An MEG study , 2012, NeuroImage.

[70]  I. Toni,et al.  Oscillations , 2018, Physics to a Degree.

[71]  Adriano B. L. Tort,et al.  Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task , 2008, Proceedings of the National Academy of Sciences.

[72]  Cees van Leeuwen,et al.  Robust emergence of small-world structure in networks of spiking neurons , 2007, Cognitive Neurodynamics.

[73]  György Buzsáki,et al.  Gamma frequency oscillation in the hippocampus of the rat: intracellular analysis in vivo , 1998, The European journal of neuroscience.

[74]  R. Traub,et al.  Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation , 1995, Nature.

[75]  T. Sejnowski,et al.  Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. , 1991, Journal of neurophysiology.

[76]  György Buzsáki,et al.  Alteration of Theta Timescale Dynamics of Hippocampal Place Cells by a Cannabinoid Is Associated with Memory Impairment , 2009, The Journal of Neuroscience.

[77]  William W. Lytton,et al.  Emergence of Physiological Oscillation Frequencies in a Computer Model of Neocortex , 2011, Front. Comput. Neurosci..

[78]  J. Bellanger,et al.  Epileptic fast intracerebral EEG activity: evidence for spatial decorrelation at seizure onset. , 2003, Brain : a journal of neurology.

[79]  G. Tamás,et al.  Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro , 1998, The Journal of physiology.

[80]  J. O’Neill,et al.  Gamma Oscillatory Firing Reveals Distinct Populations of Pyramidal Cells in the CA1 Region of the Hippocampus , 2008, The Journal of Neuroscience.

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

[82]  R. Traub,et al.  Neuronal networks for induced ‘40 Hz’ rhythms , 1996, Trends in Neurosciences.

[83]  Adriano B. L. Tort,et al.  Theta–gamma coupling increases during the learning of item–context associations , 2009, Proceedings of the National Academy of Sciences.

[84]  J. Csicsvari,et al.  Oscillatory Coupling of Hippocampal Pyramidal Cells and Interneurons in the Behaving Rat , 1999, The Journal of Neuroscience.

[85]  S. Hestrin,et al.  Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex , 1998, Nature Neuroscience.

[86]  Sean M Montgomery,et al.  Entrainment of Neocortical Neurons and Gamma Oscillations by the Hippocampal Theta Rhythm , 2008, Neuron.

[87]  L. Astolfi,et al.  A neural mass model for the simulation of cortical activity estimated from high resolution EEG during cognitive or motor tasks , 2006, Journal of Neuroscience Methods.

[88]  J. Glowinski,et al.  Influence of the hippocampus on interneurons of the rat prefrontal cortex , 2004, The European journal of neuroscience.

[89]  R. Traub,et al.  A mechanism for generation of long-range synchronous fast oscillations in the cortex , 1996, Nature.

[90]  Hamid Soltanian-Zadeh,et al.  Integrated MEG/EEG and fMRI model based on neural masses , 2006, IEEE Transactions on Biomedical Engineering.

[91]  W. Klimesch,et al.  Control mechanisms in working memory: A possible function of EEG theta oscillations , 2010, Neuroscience & Biobehavioral Reviews.

[92]  Mauro Ursino,et al.  The generation of rhythms within a cortical region: Analysis of a neural mass model , 2010, NeuroImage.

[93]  R. Fisher,et al.  High-frequency EEG activity at the start of seizures. , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[94]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[95]  O. Jensen,et al.  Gamma Power Is Phase-Locked to Posterior Alpha Activity , 2008, PloS one.

[96]  Donald L Rowe,et al.  Estimation of neurophysiological parameters from the waking EEG using a biophysical model of brain dynamics. , 2004, Journal of theoretical biology.

[97]  J. R. Hughes,et al.  Gamma, fast, and ultrafast waves of the brain: Their relationships with epilepsy and behavior , 2008, Epilepsy & Behavior.

[98]  S. Hestrin,et al.  Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[99]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[100]  A. J. Hermans,et al.  A model of the spatial-temporal characteristics of the alpha rhythm. , 1982, Bulletin of mathematical biology.

[101]  W. Freeman Simulation of chaotic EEG patterns with a dynamic model of the olfactory system , 1987, Biological Cybernetics.

[102]  N. Busch,et al.  Gamma amplitudes are coupled to theta phase in human EEG during visual perception. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[103]  G. Buzsáki,et al.  Phase relations of hippocampal projection cells and interneurons to theta activity in the anesthetized rat , 1983, Brain Research.

[104]  Mauro Ursino,et al.  A neural mass model of interconnected regions simulates rhythm propagation observed via TMS-EEG , 2011, NeuroImage.

[105]  S. Cruikshank,et al.  Electrical and chemical synapses between relay neurons in developing thalamus , 2010, The Journal of physiology.

[106]  Michael X Cohen,et al.  Assessing transient cross-frequency coupling in EEG data , 2008, Journal of Neuroscience Methods.

[107]  Karl J. Friston,et al.  A neural mass model for MEG/EEG: coupling and neuronal dynamics , 2003, NeuroImage.

[108]  Nelson J. Trujillo-Barreto,et al.  Successful memory encoding is associated with increased cross-frequency coupling between frontal theta and posterior gamma oscillations in human scalp-recorded EEG , 2013, NeuroImage.

[109]  J. Csicsvari,et al.  Mechanisms of Gamma Oscillations in the Hippocampus of the Behaving Rat , 2003, Neuron.

[110]  Henry J. Alitto,et al.  Corticothalamic feedback and sensory processing , 2003, Current Opinion in Neurobiology.

[111]  W. Singer,et al.  The Phase of Thalamic Alpha Activity Modulates Cortical Gamma-Band Activity: Evidence from Resting-State MEG Recordings , 2013, The Journal of Neuroscience.

[112]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[113]  I. Tyukin,et al.  Leaders do not look back, or do they? , 2015, 1505.01440.

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

[115]  Michael Recce,et al.  A model of hippocampal function , 1994, Neural Networks.

[116]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[117]  M. Kahana,et al.  Phase–Amplitude Coupling in Human Electrocorticography Is Spatially Distributed and Phase Diverse , 2012, The Journal of Neuroscience.