Reduced order models of myelinated axonal compartments

The paper presents a hierarchical series of computational models for myelinated axonal compartments. Three classes of models are considered, either with distributed parameters (2.5D EQS–ElectroQuasi Static, 1D TL-Transmission Lines) or with lumped parameters (0D). They are systematically analyzed with both analytical and numerical approaches, the main goal being to identify the best procedure for order reduction of each case. An appropriate error estimator is proposed in order to assess the accuracy of the models. This is the foundation of a procedure able to find the simplest reduced model having an imposed precision. The most computationally efficient model from the three geometries proved to be the analytical 1D one, which is able to have accuracy less than 0.1%. By order reduction with vector fitting, a finite model is generated with a relative difference of 10− 4 for order 5. The dynamical models thus extracted allow an efficient simulation of neurons and, consequently, of neuronal circuits. In such situations, the linear models of the myelinated compartments coupled with the dynamical, non-linear models of the Ranvier nodes, neuronal body (soma) and dendritic tree give global reduced models. In order to ease the simulation of large-scale neuronal systems, the sub-models at each level, including those of myelinated compartments should have the lowest possible order. The presented procedure is a first step in achieving simulations of neural systems with accuracy control.

[1]  Wha Wil Schilders,et al.  Parameterized model order reduction , 2015 .

[2]  D. Sorensen,et al.  A Survey of Model Reduction Methods for Large-Scale Systems , 2000 .

[3]  J W Moore,et al.  Axon voltage-clamp simulations. I. Methods and tests. , 1975, Biophysical journal.

[4]  Paula T. Kuokkanen,et al.  On the origin of the extracellular potential in the nucleus laminaris of the barn owl , 2012 .

[5]  Eugene M. Izhikevich,et al.  Simple model of spiking neurons , 2003, IEEE Trans. Neural Networks.

[6]  Daniel Ioan,et al.  Modeling the Saltatory Conduction in Myelinated Axons by Order Reduction , 2018 .

[7]  Laura M. Roa,et al.  Internodal myelinated segments: delay and RGC time-domain Green function model , 2004, IEEE Transactions on Biomedical Engineering.

[8]  R. Plonsey,et al.  A mathematical evaluation of the core conductor model. , 1966, Biophysical journal.

[9]  Daniel Ioan,et al.  Simple 1D models for neuro-signals transmission along axons , 2016, 2016 International Conference and Exposition on Electrical and Power Engineering (EPE).

[10]  Inder K. Rana Singular value decomposition of a matrix , 2002 .

[11]  M. Abramowitz,et al.  Handbook of Mathematical Functions With Formulas, Graphs and Mathematical Tables (National Bureau of Standards Applied Mathematics Series No. 55) , 1965 .

[12]  Nicholas T. Carnevale,et al.  The NEURON Book: Epilogue , 2006 .

[13]  PJ Pieter Heres,et al.  Robust and Efficient Krylov Subspace Methods for Model Order Reduction , 2005 .

[14]  Sander M. Bohte,et al.  Computing with Spiking Neuron Networks , 2012, Handbook of Natural Computing.

[15]  Patrick van der Smagt,et al.  Introduction to neural networks , 1995, The Lancet.

[16]  Boris Lohmann,et al.  Krylov Subspace Methods in Linear Model Order Reduction : Introduction and Invariance Properties , 2002 .

[17]  David M. Halliday,et al.  An Introduction to the Principles of Neuronal Modelling , 1999 .

[18]  Alexander Gow,et al.  A model of tight junction function in central nervous system myelinated axons. , 2008, Neuron glia biology.

[19]  Michael Günther,et al.  Coupled multiscale simulation and optimization in nanoelectronics , 2015 .

[20]  Alain Glière,et al.  Current approaches to model extracellular electrical neural microstimulation , 2014, Front. Comput. Neurosci..

[21]  A. Semlyen,et al.  Rational approximation of frequency domain responses by vector fitting , 1999 .

[22]  Francesca Rapetti,et al.  On quasi-static models hidden in Maxwell's equations , 2014 .

[23]  R. FitzHugh,et al.  Computation of impulse initiation and saltatory conduction in a myelinated nerve fiber. , 1962, Biophysical journal.

[24]  A. Huxley,et al.  Evidence for saltatory conduction in peripheral myelinated nerve fibres , 1949, The Journal of physiology.

[25]  James M. Bower,et al.  The Book of GENESIS , 1994, Springer New York.

[26]  W. C. Elmore The Transient Response of Damped Linear Networks with Particular Regard to Wideband Amplifiers , 1948 .

[27]  R. Romer,et al.  Tables of functions with formulae and curves , 1934 .

[28]  James P. Keener,et al.  Comprar Mathematical Physiology · I: Cellular Physiology | Keener, James | 9780387758466 | Springer , 2009 .

[29]  Erik De Schutter,et al.  Automated neuron model optimization techniques: a review , 2008, Biological Cybernetics.

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

[31]  P. Robinson,et al.  Multiscale brain modelling , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[32]  J. Clark,et al.  Extracellular currents and potentials of the active myelinated nerve fiber. , 1987, Biophysical journal.

[33]  John Robert Burger Human Memory Modeled with Standard Analog and Digital Circuits , 2009 .

[34]  Carretera de Valencia,et al.  The finite element method in electromagnetics , 2000 .

[35]  A. Huxley,et al.  The action potential in the myelinated nerve fibre of Xenopus laevis as computed on the basis of voltage clamp data , 1964, The Journal of physiology.

[36]  Andrew K. Wise,et al.  Impact of Morphometry, Myelinization and Synaptic Current Strength on Spike Conduction in Human and Cat Spiral Ganglion Neurons , 2013, PloS one.

[37]  J. Halter,et al.  A distributed-parameter model of the myelinated nerve fiber , 1988, Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[38]  Vollständiger Abdruck,et al.  Model Order Reduction by Krylov Subspace Methods with Global Error Bounds and Automatic Choice of Parameters , 2014 .

[39]  E. Seebacher,et al.  Compact modeling and fast simulation of on-chip interconnect lines , 2006, IEEE Transactions on Magnetics.

[40]  L. Goldman,et al.  Computation of impulse conduction in myelinated fibers; theoretical basis of the velocity-diameter relation. , 1968, Biophysical journal.

[41]  J. Holsheimer,et al.  Recruitment of dorsal column fibers in spinal cord stimulation: influence of collateral branching , 1992, IEEE Transactions on Biomedical Engineering.

[42]  Haza Nuzly Abdul Hamed,et al.  Computing with Spiking Neuron Networks A Review , 2014, SOCO 2014.

[43]  Egidio D'Angelo,et al.  Computational Modeling of Single Neuron Extracellular Electric Potentials and Network Local Field Potentials using LFPsim , 2016, Front. Comput. Neurosci..

[44]  Daniel W. Lozier,et al.  NIST Digital Library of Mathematical Functions , 2003, Annals of Mathematics and Artificial Intelligence.

[45]  John B. Moore,et al.  Singular Value Decomposition , 1994 .

[46]  Nicolas Brunel,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[47]  Simon Haykin,et al.  Neural Networks: A Comprehensive Foundation , 1998 .

[48]  Wofgang Maas,et al.  Networks of spiking neurons: the third generation of neural network models , 1997 .

[49]  Ernst Niebur,et al.  Neuronal cable theory , 2008, Scholarpedia.

[50]  D. I. Stephanova Myelin as longitudinal conductor: a multi-layered model of the myelinated human motor nerve fibre , 2001, Biological Cybernetics.

[51]  J W Moore,et al.  Axon voltage-clamp simulations. II. Double sucrose-gap method. , 1975, Biophysical journal.

[52]  Angus M. Brown,et al.  Computational modeling of the effects of auditory nerve dysmyelination , 2014, Front. Neuroanat..

[53]  J W Moore,et al.  Simulations of conduction in uniform myelinated fibers. Relative sensitivity to changes in nodal and internodal parameters. , 1978, Biophysical journal.

[54]  Alexandru Timotin,et al.  LA STRUCTURE DE LA FIBRE NERVEUSE: UN PROJET OPTIMAL , 2004 .

[55]  Wulfram Gerstner,et al.  Phenomenological models of synaptic plasticity based on spike timing , 2008, Biological Cybernetics.

[56]  Stefan Güttel,et al.  A Rational Krylov Toolbox for MATLAB , 2014 .

[57]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1990 .