• Open Access

Computational model of the mechanoelectrophysiological coupling in axons with application to neuromodulation

Haoyu Chen, Daniel Garcia-Gonzalez, and Antoine Jérusalem
Phys. Rev. E 99, 032406 – Published 5 March 2019
PDFHTMLExport Citation

Abstract

For more than half a century, the action potential (AP) has been considered a purely electrical phenomenon. However, experimental observations of membrane deformations occurring during APs have revealed that this process also involves mechanical features. This discovery has recently fuelled a controversy on the real nature of APs: whether they are mechanical or electrical. In order to examine some of the modern hypotheses regarding APs, we propose here a coupled mechanoelectrophysiological membrane finite-element model for neuronal axons. The axon is modeled as an axisymmetric thin-wall cylindrical tube. The electrophysiology of the membrane is modeled using the classic Hodgkin-Huxley (H-H) equations for the Nodes of Ranvier or unmyelinated axons and the cable theory for the internodal regions, whereas the axonal mechanics is modeled by means of viscoelasticity theory. Membrane potential changes induce a strain gradient field via reverse flexoelectricity, whereas mechanical pulses result in an electrical self-polarization field following the direct flexoelectric effect, in turn influencing the membrane potential. Moreover, membrane deformation also alters the values of membrane capacitance and resistance in the H-H equation. These three effects serve as the fundamental coupling mechanisms between the APs and mechanical pulses in the model. A series of numerical studies was systematically conducted to investigate the consequences of interaction between the APs and mechanical waves on both myelinated and unmyelinated axons. Simulation results illustrate that the AP is always accompanied by an in-phase propagating membrane displacement of 1nm, whereas mechanical pulses with enough magnitude can also trigger APs. The model demonstrates that mechanical vibrations, such as the ones arising from ultrasound stimulations, can either annihilate or enhance axonal electrophysiology depending on their respective directionality and frequency. It also shows that frequency of pulse repetition can also enhance signal propagation independently of the amplitude of the signal. This result not only reconciles the mechanical and electrical natures of the APs but also provides an explanation for the experimentally observed mechanoelectrophysiological phenomena in axons, especially in the context of ultrasound neuromodulation.

  • Figure
  • Figure
  • Figure
  • Figure
  • Figure
  • Figure
  • Figure
5 More
  • Received 5 July 2018
  • Revised 4 December 2018

DOI:https://doi.org/10.1103/PhysRevE.99.032406

Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article's title, journal citation, and DOI.

Published by the American Physical Society

Physics Subject Headings (PhySH)

Interdisciplinary PhysicsPhysics of Living Systems

Authors & Affiliations

Haoyu Chen, Daniel Garcia-Gonzalez, and Antoine Jérusalem*

  • Department of Engineering Science, University of Oxford, Oxford OX1 3PJ, United Kingdom

  • *antoine.jerusalem@eng.ox.ac.uk

Article Text

Click to Expand

Supplemental Material

Click to Expand

References

Click to Expand
Issue

Vol. 99, Iss. 3 — March 2019

Reuse & Permissions
Author publication services for translation and copyediting assistance advertisement

Authorization Required


×
×

Images

×

Sign up to receive regular email alerts from Physical Review E

Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

×

Log In

Cancel
×

Search


Article Lookup

Paste a citation or DOI

Enter a citation
×