Collision of two action potentials in a single excitable cell

Fillafer, Christian; Paeger, Anne; Schneider, Mat­thias

doi:10.1016/j.bbagen.2017.09.020

Cited by 14 publications

(15 citation statements)

References 36 publications

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“…For example, the collisions of two impulses propagating in orthodromic and antidromic directions in the giant axons of earthworms and lobsters did not result in the annihilation of the two signals, contrary to the notion on the refractory period in the Hodgkin – Huxley model 5 . This contradiction has been repeatedly found later by other researchers 6 . Heimberg and Jackson et al .…”

Section: Introductionmentioning

confidence: 62%

“…This model has supporting evidences from previous experiments and computational simulations that there were changes of local heat and membrane displacement along with the action potential process 9 – 13 . The model could explain the non-annihilation condition of the two signals in collision 5 , 6 , by describing the nerve signals as waves for the first time. Nevertheless, it encounters problems in explaining the “ saltatory conduction ” in myelinated axons and the neural transmission in poikilotherm 14 .…”

Section: Introductionmentioning

confidence: 99%

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Experimental and Computational Studies on the Basic Transmission Properties of Electromagnetic Waves in Softmaterial Waveguides

Sun

et al. 2018

Sci Rep

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Conventional waveguides are usually made of metallic materials, and they are effective pathways for the transmission of electromagnetic waves. A “Softmaterial waveguide”, by contrast, is supposed to be made of dielectric material and ionic fluids. In this work, by means of both experiment and computational simulation we examined one kind of softmaterial waveguide, which has the configuration of ionic fluids filled in and out of a dielectric tube. We investigated configurations with varied parameters, i.e., tube thickness from 0.2 mm to 5.0 mm, tube length of 2.0–12.0 cm, ionic concentration covering 4 orders of magnitude from 0.0002–2.0 mol/L, frequency of 10 Hz to 100 MHz for sine wave excitations, pulse duration of 5 ns to 100 ms for excitation pulses. We also mimicked the myelin sheath structure in myelinated axons in simulation. Both experimental and simulation results consistently showed a clear confinement effect for the energy flux of transmitting electromagnetic waves inside the dielectric tube, strongly supporting the model of softmaterail waveguide. The results revealed that the softmaterial waveguide had a low-pass nature, where the intensity of transmitted signals saturated at a duration of 10–100 μs for pulses, or cut off at frequency of 10–100 kHz for sine waves. And, the transmission efficiency increased with the thickness of the dielectric layer, as well as ion concentration of the solution. The results may help for a better understanding various electrical communication behaviors observed in biosystems, where a natural lipid membrane with bilateral fluids was suggested as the efficient pathway for pulsed neural impulses in a way similar to soliton-like electromagnetic pulses transmitting in a softmaterial waveguide.

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Section: Introductionmentioning

confidence: 62%

Section: Introductionmentioning

confidence: 99%

Experimental and Computational Studies on the Basic Transmission Properties of Electromagnetic Waves in Softmaterial Waveguides

Sun

et al. 2018

Sci Rep

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“…With respect to collisions in particular, the predictions of the theoretical analysis of colliding pulses reveals no annihilation (less than 4%) in soliton models [32,33], which is in clear contrast to our results that demonstrate significant (up to 80%) decrease in amplitude upon collision. In fact we observe annihilation of colliding pulses both in lipid monolayers as well as Algae [34]. In addition to correctly accounting for nonlinearity and dispersion, internal heat transfer in the colliding pulses is also central to an understanding of the annihilation phenomenon, which requires incorporating the nonlinear viscosity resulting from relaxation of phase change in the hydrodynamic equations as well [22,31].…”

Section: Discussionmentioning

confidence: 93%

Collision and annihilation of nonlinear sound waves and action potentials in interfaces

Shrivastava

Kang

Schneider

2018

J. R. Soc. Interface.

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Nerve impulses, previously proposed as manifestations of nonlinear acoustic pulses localized at the plasma membrane, can annihilate upon collision. However, whether annihilation of acoustic waves at interfaces takes place is unclear. We previously showed the propagation of nonlinear sound waves that propagate as solitary waves above a threshold (super-threshold) excitation in a lipid monolayer near a phase transition. Here we investigate the interaction of these waves. Sound waves were excited mechanically via a piezo cantilever in a lipid monolayer at the air–water interface and their amplitude is reported before and after a collision. The compression amplitude was observed via Förster resonance energy transfer between donor and acceptor dyes, measured at fixed points along the propagation path in the lipid monolayer. We provide direct experimental evidence for the annihilation of two super-threshold interfacial pulses upon head-on collision in a lipid monolayer and conclude that sound waves propagating in a lipid interface can interact linearly, nonlinearly, or annihilate upon collision depending on the state of the system. Thus we show that the main characteristics of nerve impulses, i.e. solitary character, velocity, couplings, all-or-none behaviour, threshold and even annihilation are also demonstrated by nonlinear sound waves in a lipid monolayer, where they follow directly from the thermodynamic principles applied to an interface. As these principles are equally unavoidable in a nerve membrane, our observations strongly suggest that the underlying physical basis of action potentials and the observed nonlinear-pules is identical.

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“…In the literature, several experimental studies were conducted in various nerve fibers or cells to examine whether annihilation can occur or not on AP collision [66][67][68][69][70]. It has been frequently witnessed that colliding APs are reciprocally annihilated instead of penetrating each other.…”

Section: Discussionmentioning

confidence: 99%

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

2019

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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 ≈1 nm, 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.

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Collision of two action potentials in a single excitable cell

Cited by 14 publications

References 36 publications

Experimental and Computational Studies on the Basic Transmission Properties of Electromagnetic Waves in Softmaterial Waveguides

Experimental and Computational Studies on the Basic Transmission Properties of Electromagnetic Waves in Softmaterial Waveguides

Collision and annihilation of nonlinear sound waves and action potentials in interfaces

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

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