Modelling the effect of ephaptic coupling on spike propagation in peripheral nerve fibres
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
35538379
PubMed Central
PMC9287264
DOI
10.1007/s00422-022-00934-9
PII: 10.1007/s00422-022-00934-9
Knihovny.cz E-zdroje
- Klíčová slova
- Ephaptic coupling, Peripheral nerves, Spike propagation, Synchronisation,
- MeSH
- akční potenciály fyziologie MeSH
- axony * fyziologie MeSH
- membránové potenciály MeSH
- nervová vlákna * MeSH
- periferní nervy MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Experimental and theoretical studies have shown that ephaptic coupling leads to the synchronisation and slowing down of spikes propagating along the axons within peripheral nerve bundles. However, the main focus thus far has been on a small number of identical axons, whereas realistic peripheral nerve bundles contain numerous axons with different diameters. Here, we present a computationally efficient spike propagation model, which captures the essential features of propagating spikes and their ephaptic interaction, and facilitates the theoretical investigation of spike volleys in large, heterogeneous fibre bundles. We first lay out the theoretical basis to describe how the spike in an active axon changes the membrane potential of a passive axon. These insights are then incorporated into the spike propagation model, which is calibrated with a biophysically realistic model based on Hodgkin-Huxley dynamics. The fully calibrated model is then applied to fibre bundles with a large number of axons and different types of axon diameter distributions. One key insight of this study is that the heterogeneity of the axonal diameters has a dispersive effect, and that a higher level of heterogeneity requires stronger ephaptic coupling to achieve full synchronisation between spikes.
Zobrazit více v PubMed
Anastassiou C, Koch C. Ephaptic coupling to endogenous electric field activity: why bother? Curr Opin Neurobiol. 2015;31:95–103. doi: 10.1016/j.conb.2014.09.002. PubMed DOI
Anastassiou C, Perin R, Markram H, Koch C. Ephaptic coupling of cortical neurons. Nat Neurosci. 2011;14:217–223. doi: 10.1038/nn.2727. PubMed DOI
Arvanitaki A. Effects evoked in an axon by the activity of a contiguous one. J Neurophysiol. 1942;5:89–108. doi: 10.1152/jn.1942.5.2.89. DOI
Assaf Y, Blumenfeld-Katzir T, Yovel Y, Basser P. AxCaliber: a method for measuring axon diameter distribution from diffusion MRI. Magn Reson Med. 2008;59:1347–1354. doi: 10.1002/mrm.21577. PubMed DOI PMC
Barr R, Plonsey R. Electrophysiological interaction through the interstitial space between adjacent unmyelinated fibers. Biophys J . 1992;61:1164–1175. doi: 10.1016/S0006-3495(92)81925-2. PubMed DOI PMC
Basser P. Cable equation for a myelinated axon derived from its microstructure. Med Biol Eng Comput. 1993;31:S87–S92. doi: 10.1007/BF02446655. PubMed DOI
Bell J. Modelling parallel, unmyelinated axons: pulse trapping and ephaptic transmission. SIAM J Appl Math. 1981;41:168–180. doi: 10.1137/0141012. DOI
Binczak S, Eilbeck J, Scott A. Ephaptic coupling of myelinated nerve fibers. Physica D. 2001;148:159–174. doi: 10.1016/S0167-2789(00)00173-1. DOI
Bokil H, Laaris N, Blinder K, Ennis M, Keller A. Ephaptic interactions in the mammalian olfactory system. J Neurosci. 2001;21:173. doi: 10.1523/jneurosci.21-20-j0004.2001. PubMed DOI PMC
Brill M, Waxman S, Moore J, Joyner R. Conduction velocity and spike configuration in myelinated fibres: computed dependence on internode distance. J Neurol Neurosurg Psychiatry. 1977;40:769–774. doi: 10.1136/jnnp.40.8.769. PubMed DOI PMC
Buzsáki G, Anastassiou C, Koch C. The origin of extracellular fields and currents—EEG, ECoG, LFP and spikes. Nat Rev Neurosci. 2012;13:407–420. doi: 10.1038/nrn3241. PubMed DOI PMC
Capllonch-Juan M, Sepulveda F. Modelling the effects of ephaptic coupling on selectivity and response patterns during artificial stimulation of peripheral nerves. PLoS Comput Biol. 2020;16:e1007826. doi: 10.1371/journal.pcbi.1007826. PubMed DOI PMC
Clark J, Plonsey R. A mathematical study of nerve interaction. Biophys J . 1970;10:937–957. doi: 10.1016/S0006-3495(70)86344-5. PubMed DOI PMC
Eichel M, Gargareta VI, D’Este E, Fledrich R, Kungl T, Buscham T, Lüders K, Miracle C, Jung R, Distler U, Kusch K, Möbius W, Hülsmann S, Tenzer S, Nave KA, Werner H. CMTM6 expressed on the Adaxonal Schwann cell surface restricts axonal diameters in peripheral nerves. Nat Commun. 2020;11:4514. doi: 10.1038/s41467-020-18172-7. PubMed DOI PMC
Eilbeck J, Luzader S, Scott A. Pulse evolution on coupled nerve fibres. Bull Math Biol. 1981;43:389–400. doi: 10.1007/BF02459429. PubMed DOI
Goldman L, Albus J. Computation of impulse conduction in myelinated fibers; theoretical basis of the velocity-diameter relation. Biophys J . 1968;8:596–607. doi: 10.1016/S0006-3495(68)86510-5. PubMed DOI PMC
Goldwyn J, Rinzel J. Neuronal coupling by endogenous electric fields: cable theory and applications to coincidence detector neurons in the auditory brain stem. J Neurophysiol. 2016;115:2033–2051. doi: 10.1152/jn.00780.2015. PubMed DOI PMC
Hodgkin A, Huxley A. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol. 1952;117:500–544. doi: 10.1113/jphysiol.1952.sp004764. PubMed DOI PMC
Holt G, Koch C. Electrical interactions via the extracellular potential near cell bodies. J Comput Neurosci. 1999;6:169–184. doi: 10.1023/a:1008832702585. PubMed DOI
Hursh J. Conduction velocity and diameter of nerve fibers. Am J Physiol. 1939;127:131–139. doi: 10.1152/ajplegacy.1939.127.1.131. DOI
Ikeda M, Oka Y. The relationship between nerve conduction velocity and fiber morphology during peripheral nerve regeneration. Brain Behav. 2012;2:382–390. doi: 10.1002/brb3.61. PubMed DOI PMC
Katz B, Schmitt O. Electric interaction between two adjacent nerve fibres. J Physiol. 1940;97:471–488. doi: 10.1113/jphysiol.1940.sp003823. PubMed DOI PMC
Kuramoto Y. Chemical oscillations, waves, and turbulence. New York: Springer; 1984.
Maïna I, Tabi C, Fouda HE, Mohamadou A, Kofané T (2015) Discrete impulses in ephaptically coupled nerve fibers. Chaos 25:043118. 10.1063/1.4919077 PubMed
Marrazzi A, Lorente de Nó R. Interaction of neighbouring fibres in myelinated nerve. J Neurophysiol. 1944;7:83. doi: 10.1152/jn.1944.7.2.83. DOI
McColgan T, Liu J, Kuokkanen P, Carr C, Wagner H, Kempter R (2017) Dipolar extracellular potentials generated by axonal projections. eLife 6:e26106. 10.7554/eLife.26106 PubMed PMC
Parker J, Shariati N, Karantonis D. Electrically evoked compound action potential recording in peripheral nerves. Bioelectron Med. 2018;1:71–83. doi: 10.2217/bem-2017-0005. DOI
Pikovsky A, Rosenblum M, Kurths J (2001) Synchronization: a universal concept in nonlinear science. Cambridge University Press
Rall W (1977) Core conductor theory and cable properties of neurons. In: Poeter R (ed) Handbook of physiology: the nervous system, vol 3. American Physiological Society, Bethesda, pp 39–97
Reutskiy S, Rossoni E, Tirozzi B. Conduction in bundles of demyelinated nerve fibers: computer simulation. Biol Cybern. 2003;89:439–448. doi: 10.1007/s00422-003-0430-x. PubMed DOI
Rosenblueth A. The stimulation of myelinated axons by nerve impulses in adjacent myelinated axons. Am J Physiol. 1941;132:119–128. doi: 10.1152/ajplegacy.1941.132.1.119. DOI
Sanders F. The thickness of the myelin sheaths of normal and regenerating peripheral nerve fibres. Proc Roy Soc Lond Ser B. 1947;135:323–357. doi: 10.1098/rspb.1948.0015. DOI
Schmidt H, Knösche T. Action potential propagation and synchronisation in myelinated axons. PLoS Comput Biol. 2019;15:e1007004. doi: 10.1371/journal.pcbi.1007004. PubMed DOI PMC
Schmidt H, Hahn G, Deco G, Knosche TR. Ephaptic coupling in white matter fibre bundles modulates axonal transmission delays. PLOS Comput Biol. 2021;17:e1007858. doi: 10.1371/journal.pcbi.1007858. PubMed DOI PMC
Sheheitli H, Jirsa V. A mathematical model of ephaptic interactions in neuronal fiber pathways: could there be more than transmission along the tracts? Network Neurosci. 2020;4:595–610. doi: 10.1162/netn_a_00134. PubMed DOI PMC
Shneider M, Pekker M. Correlation of action potentials in adjacent neurons. Phys Biol. 2015;12:066009. doi: 10.1088/1478-3975/12/6/066009. PubMed DOI
Trayanova N, Henriquez C, Plonsey R. Limitations of approximate solutions for computing the extracellular potential of single fibers and bundle equivalents. IEEE Trans Biomed Eng. 1990;37:22–35. doi: 10.1109/10.43608. PubMed DOI
Tveit A, Jaeger K, Lines G, Paszkowski L, Edwards A, Maki-Marttunen T, Halnes G, Einevoll G. An evaluation of the accuracy of classical models for computing the membrane potential and extracellular potential for neurons. Front Comput Neurosci. 2017;11:27. doi: 10.3389/fncom.2017.00027. PubMed DOI PMC