Mechanical surface waves accompany action potential propagation.

Ahmed El Hady,Benjamin B Machta

doi:10.1038/ncomms7697

Ahmed El Hady, Benjamin B Machta

Open Access

https://doi.org/10.1038/ncomms7697

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Abstract

Many diverse studies have shown that a mechanical displacement of the axonal membrane accompanies the electrical pulse defining the action potential (AP). We present a model for these mechanical displacements as arising from the driving of surface wave modes in which potential energy is stored in elastic properties of the neuronal membrane and cytoskeleton while kinetic energy is carried by the axoplasmic fluid. In our model, these surface waves are driven by the travelling wave of electrical depolarization characterizing the AP, altering compressive electrostatic forces across the membrane. This driving leads to co-propagating mechanical displacements, which we term Action Waves (AWs). Our model allows us to estimate the shape of the AW that accompanies any travelling wave of voltage, making predictions that are in agreement with results from several experimental systems. Our model can serve as a framework for understanding the physical origins and possible functional roles of these AWs.

Highlights

Many diverse studies have shown that a mechanical displacement of the axonal membrane accompanies the electrical pulse defining the action potential (AP)
We expect that the surface waves we predict would accompany the AP predicted by Hodgkin and Huxley (HH) and the cable theory, even if they do not contribute to neuronal function
We estimate the driving force on these modes that accompanies the passing of an AP

Summary

Introduction

Many diverse studies have shown that a mechanical displacement of the axonal membrane accompanies the electrical pulse defining the action potential (AP). We present a model for these mechanical displacements as arising from the driving of surface wave modes in which potential energy is stored in elastic properties of the neuronal membrane and cytoskeleton while kinetic energy is carried by the axoplasmic fluid In our model, these surface waves are driven by the travelling wave of electrical depolarization characterizing the AP, altering compressive electrostatic forces across the membrane. While measuring and understanding the electrical component of the AP has been the focus of most experimental and theoretical efforts, a large number of experimental studies have shown that the AP is accompanied by fast and temporary mechanical changes These include changes in axonal radius[2,3,4,5,6,7,8,9,10], pressure[4,11], optical properties[12], the release and subsequent absorption of a small amount of heat[7] and shortening of the axon at its terminus when the AP arrives[13]. Our results allow for the possibility that the mechanical changes that accompany these surface waves feed back and influence the electrical AP, giving them functional importance

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