How effective delays shape oscillatory dynamics in neuronal networks

Abstract Synaptic, dendritic and single-cell kinetics generate significant time delays that shape the dynamics of large networks of spiking neurons. Previous work has shown that such effective delays can be taken into account with a rate model through the addition of an explicit, fixed delay (Roxin et al. (2005,2006) [29] , [30] ). Here we extend this work to account for arbitrary symmetric patterns of synaptic connectivity and generic nonlinear transfer functions. Specifically, we conduct a weakly nonlinear analysis of the dynamical states arising via primary instabilities of the asynchronous state. In this way we determine analytically how the nature and stability of these states depend on the choice of transfer function and connectivity. We arrive at two general observations of physiological relevance that could not be explained in previous work. These are: 1 — fast oscillations are always supercritical for realistic transfer functions and 2 — traveling waves are preferred over standing waves given plausible patterns of local connectivity. We finally demonstrate that these results show good agreement with those obtained performing numerical simulations of a network of Hodgkin–Huxley neurons.

[1]  A. Thomson,et al.  Functional Maps of Neocortical Local Circuitry , 2007, Front. Neurosci..

[2]  A. Hutt Effects of nonlocal feedback on traveling fronts in neural fields subject to transmission delay. , 2004, Physical review. E, Statistical, nonlinear, and soft matter physics.

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

[4]  K. Miller,et al.  Neural noise can explain expansive, power-law nonlinearities in neural response functions. , 2002, Journal of neurophysiology.

[5]  S. Amari Dynamics of pattern formation in lateral-inhibition type neural fields , 1977, Biological Cybernetics.

[6]  D. Hansel,et al.  How Noise Contributes to Contrast Invariance of Orientation Tuning in Cat Visual Cortex , 2002, The Journal of Neuroscience.

[7]  Stephen Coombes,et al.  Waves, bumps, and patterns in neural field theories , 2005, Biological Cybernetics.

[8]  D. Hansel,et al.  Role of delays in shaping spatiotemporal dynamics of neuronal activity in large networks. , 2005, Physical review letters.

[9]  H. Sompolinsky,et al.  Theory of orientation tuning in visual cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[10]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[11]  Bernhard Hellwig,et al.  A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex , 2000, Biological Cybernetics.

[12]  P. Matthews,et al.  Dynamic instabilities in scalar neural field equations with space-dependent delays , 2007 .

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

[14]  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.

[15]  Nicolas Brunel,et al.  Rate Models with Delays and the Dynamics of Large Networks of Spiking Neurons(Oscillation, Chaos and Network Dynamics in Nonlinear Science) , 2006 .

[16]  Stephen Coombes,et al.  The importance of different timings of excitatory and inhibitory pathways in neural field models , 2006, Network.

[17]  S. Coombes,et al.  Delays in activity-based neural networks , 2009, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[18]  W. J. Nowack Methods in Neuronal Modeling , 1991, Neurology.

[19]  P. C. Murphy,et al.  Cerebral Cortex , 2017, Cerebral Cortex.

[20]  T. Maung on in C , 2010 .

[21]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[22]  Bard Ermentrout,et al.  Pattern Formation in a Network of Excitatory and Inhibitory Cells with Adaptation , 2004, SIAM J. Appl. Dyn. Syst..

[23]  Axel Hutt,et al.  Effects of distributed transmission speeds on propagating activity in neural populations. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[24]  M. Cross,et al.  Pattern formation outside of equilibrium , 1993 .

[25]  G. Lord,et al.  Waves and bumps in neuronal networks with axo-dendritic synaptic interactions , 2003 .

[26]  M. Holmes Introduction to Perturbation Methods , 1995 .

[27]  M. V. Rossum,et al.  In Neural Computation , 2022 .

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

[29]  J. Bullier,et al.  Feedforward and feedback connections between areas V1 and V2 of the monkey have similar rapid conduction velocities. , 2001, Journal of neurophysiology.

[30]  J. Cowan,et al.  Large Scale Spatially Organized Activity in Neural Nets , 1980 .

[31]  D. Amit,et al.  Model of global spontaneous activity and local structured activity during delay periods in the cerebral cortex. , 1997, Cerebral cortex.

[32]  Axel Hutt,et al.  Stability and Bifurcations in Neural Fields with Finite Propagation Speed and General Connectivity , 2004, SIAM J. Appl. Math..

[33]  J. A. Roberts,et al.  Modeling distributed axonal delays in mean-field brain dynamics. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[34]  B. Ermentrout Neural networks as spatio-temporal pattern-forming systems , 1998 .

[35]  Axel Hutt,et al.  Neural Fields with Distributed Transmission Speeds and Long-Range Feedback Delays , 2006, SIAM J. Appl. Dyn. Syst..

[36]  Bard Ermentrout,et al.  Spatially Structured Activity in Synaptically Coupled Neuronal Networks: I. Traveling Fronts and Pulses , 2001, SIAM J. Appl. Math..

[37]  B. M. Fulk MATH , 1992 .

[38]  D. Liley,et al.  Modeling electrocortical activity through improved local approximations of integral neural field equations. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[39]  André Longtin,et al.  Driving neural oscillations with correlated spatial input and topographic feedback. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[40]  T. Harkany,et al.  Pyramidal cell communication within local networks in layer 2/3 of rat neocortex , 2003, The Journal of physiology.

[41]  Bard Ermentrout,et al.  Spatially Structured Activity in Synaptically Coupled Neuronal Networks: II. Lateral Inhibition and Standing Pulses , 2001, SIAM J. Appl. Math..

[42]  Oren Shriki,et al.  Rate Models for Conductance-Based Cortical Neuronal Networks , 2003, Neural Computation.

[43]  Bard Ermentrout,et al.  Reduction of Conductance-Based Models with Slow Synapses to Neural Nets , 1994, Neural Computation.

[44]  G. Ermentrout,et al.  Existence and uniqueness of travelling waves for a neural network , 1993, Proceedings of the Royal Society of Edinburgh: Section A Mathematics.

[45]  D. Hansel,et al.  Temporal decorrelation of collective oscillations in neural networks with local inhibition and long-range excitation. , 2007, Physical review letters.

[46]  H. Haken,et al.  Field Theory of Electromagnetic Brain Activity. , 1996, Physical review letters.

[47]  Idan Segev,et al.  Methods in Neuronal Modeling , 1988 .

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

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

[50]  D. Koshland Frontiers in neuroscience. , 1988, Science.