Complete Classification of the Macroscopic Behavior of a Heterogeneous Network of Theta Neurons

We design and analyze the dynamics of a large network of theta neurons, which are idealized type I neurons. The network is heterogeneous in that it includes both inherently spiking and excitable neurons. The coupling is global, via pulselike synapses of adjustable sharpness. Using recently developed analytical methods, we identify all possible asymptotic states that can be exhibited by a mean field variable that captures the network's macroscopic state. These consist of two equilibrium states that reflect partial synchronization in the network and a limit cycle state in which the degree of network synchronization oscillates in time. Our approach also permits a complete bifurcation analysis, which we carry out with respect to parameters that capture the degree of excitability of the neurons, the heterogeneity in the population, and the coupling strength (which can be excitatory or inhibitory). We find that the network typically tends toward the two macroscopic equilibrium states when the neuron's intrinsic dynamics and the network interactions reinforce one another. In contrast, the limit cycle state, bifurcations, and multistability tend to occur when there is competition among these network features. Finally, we show that our results are exhibited by finite network realizations of reasonable size.

[1]  Eugene M. Izhikevich,et al.  Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting , 2006 .

[2]  Germán Mato,et al.  Asynchronous States and the Emergence of Synchrony in Large Networks of Interacting Excitatory and Inhibitory Neurons , 2003, Neural Computation.

[3]  P. Peretto,et al.  Collective properties of neural networks: A statistical physics approach , 2004, Biological Cybernetics.

[4]  Yi Zeng,et al.  Synchrony and Periodicity in Excitable Neural Networks with Multiple Subpopulations , 2014, SIAM J. Appl. Dyn. Syst..

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

[6]  F. Attneave,et al.  The Organization of Behavior: A Neuropsychological Theory , 1949 .

[7]  Frances K Skinner,et al.  Inhibitory Networks of Fast-Spiking Interneurons Generate Slow Population Activities due to Excitatory Fluctuations and Network Multistability , 2012, The Journal of Neuroscience.

[8]  H. Robinson,et al.  Threshold firing frequency-current relationships of neurons in rat somatosensory cortex: type 1 and type 2 dynamics. , 2004, Journal of neurophysiology.

[9]  K. Harris Neural signatures of cell assembly organization , 2005, Nature Reviews Neuroscience.

[10]  Haim Sompolinsky,et al.  STATISTICAL MECHANICS OF NEURAL NETWORKS , 1988 .

[11]  D. Paz'o,et al.  Low-dimensional dynamics of populations of pulse-coupled oscillators , 2013, 1305.4044.

[12]  P. Bressloff SYNAPTICALLY GENERATED WAVE PROPAGATION IN EXCITABLE NEURAL MEDIA , 1999 .

[13]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[14]  E. Montbrió,et al.  Shear diversity prevents collective synchronization. , 2011, Physical review letters.

[15]  M. Wolfrum,et al.  Nonuniversal transitions to synchrony in the Sakaguchi-Kuramoto model. , 2012, Physical review letters.

[16]  Carlo R Laing,et al.  Derivation of a neural field model from a network of theta neurons. , 2014, Physical review. E, Statistical, nonlinear, and soft matter physics.

[17]  Abbott,et al.  Asynchronous states in networks of pulse-coupled oscillators. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[18]  Cheng Ly,et al.  Dynamics of Coupled Noisy Neural Oscillators with Heterogeneous Phase Resetting Curves , 2014, SIAM J. Appl. Dyn. Syst..

[19]  J. Brobeck The Integrative Action of the Nervous System , 1948, The Yale Journal of Biology and Medicine.

[20]  Edward Ott,et al.  Low dimensional description of pedestrian-induced oscillation of the Millennium Bridge. , 2009, Chaos.

[21]  Remus Osan,et al.  Regular Traveling Waves in a One-Dimensional Network of Theta Neurons , 2002, SIAM J. Appl. Math..

[22]  H. Daido Onset of cooperative entrainment in limit-cycle oscillators with uniform all-to-all interactions: bifurcation of the order function , 1996 .

[23]  Carlo R. Laing,et al.  Taking the Pulse , 2014 .

[24]  J. Crawford,et al.  Amplitude expansions for instabilities in populations of globally-coupled oscillators , 1993, patt-sol/9310005.

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

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

[27]  Maria V. Sanchez-Vives,et al.  Electrophysiological classes of cat primary visual cortical neurons in vivo as revealed by quantitative analyses. , 2003, Journal of neurophysiology.

[28]  Frances K Skinner,et al.  Moving beyond Type I and Type II neuron types , 2013, F1000Research.

[29]  Alexandre Wagemakers,et al.  Control of collective network chaos. , 2014, Chaos.

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

[31]  G. Ermentrout,et al.  Parabolic bursting in an excitable system coupled with a slow oscillation , 1986 .

[32]  E. Ott,et al.  Low dimensional behavior of large systems of globally coupled oscillators. , 2008, Chaos.

[33]  Bard Ermentrout,et al.  The Analysis of Synaptically Generated Traveling Waves , 1998, Journal of Computational Neuroscience.

[34]  Leandro M Alonso,et al.  Average dynamics of a driven set of globally coupled excitable units. , 2011, Chaos.

[35]  Ernest Barreto,et al.  Macroscopic complexity from an autonomous network of networks of theta neurons , 2014, Front. Comput. Neurosci..

[36]  D. Hansel,et al.  Existence and stability of persistent states in large neuronal networks. , 2001, Physical review letters.

[37]  Yoshiki Kuramoto,et al.  Chemical Oscillations, Waves, and Turbulence , 1984, Springer Series in Synergetics.

[38]  Ernest Barreto,et al.  Generating macroscopic chaos in a network of globally coupled phase oscillators. , 2011, Chaos.

[39]  E. Ott,et al.  Exact results for the Kuramoto model with a bimodal frequency distribution. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[40]  Y. Kuznetsov Elements of Applied Bifurcation Theory , 2023, Applied Mathematical Sciences.

[41]  E. Ott,et al.  Long time evolution of phase oscillator systems. , 2009, Chaos.

[42]  Ronald A. J. van Elburg,et al.  External Drive to Inhibitory Cells Induces Alternating Episodes of High- and Low-Amplitude Oscillations , 2012, PLoS Comput. Biol..

[43]  Alan Peters,et al.  Cellular components of the cerebral cortex , 1984 .

[44]  A. Hodgkin The local electric changes associated with repetitive action in a non‐medullated axon , 1948, The Journal of physiology.

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

[46]  S. Strogatz,et al.  Identical phase oscillators with global sinusoidal coupling evolve by Mobius group action. , 2009, Chaos.

[47]  Yoshiki Kuramoto,et al.  Self-entrainment of a population of coupled non-linear oscillators , 1975 .

[48]  Arkady Pikovsky,et al.  Dynamics of heterogeneous oscillator ensembles in terms of collective variables , 2011 .

[49]  Masatoshi Sekine,et al.  Analysis of globally connected active rotators with excitatory and inhibitory connections using the Fokker-Planck equation. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[50]  W. Beiglböck,et al.  Lecture Notes in Physics 1969–1985 , 1985 .

[51]  Huzihiro Araki,et al.  International Symposium on Mathematical Problems in Theoretical Physics , 1975 .

[52]  Tanushree B. Luke,et al.  Networks of theta neurons with time-varying excitability: Macroscopic chaos, multistability, and final-state uncertainty , 2014 .

[53]  Steven H Strogatz,et al.  Invariant submanifold for series arrays of Josephson junctions. , 2008, Chaos.

[54]  Rhonda Dzakpasu,et al.  Observed network dynamics from altering the balance between excitatory and inhibitory neurons in cultured networks. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.