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

2019

J. R. Soc. Interface.

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In an ongoing debate on the physical nature of the action potential (AP), one group adheres to the electrical model of Hodgkin and Huxley, while the other describes the AP as a nonlinear acoustic pulse propagating within an interface near a transition. However, despite remarkable similarities, acoustics remains a non-intuitive mechanism for APs for the following reason. While acoustic pulses are typically associated with the propagation of density, pressure and temperature variation, APs are most commonly measured electrically. Here, we show that this discrepancy is lifted upon considering the electrical and chemical aspects of the interface, in addition to its mechanical properties. Specifically, we demonstrate how electrical and pH aspects of acoustic pulses emerge from an idealized description of the lipid interface, which is based on classical physical principles and contains no fit parameters. The pulses that emerge from the model show similarities to APs not only in qualitative shape and scales (time, velocity and voltage), but also demonstrate saturation of amplitude and annihilation upon collision.

Section: Discussionmentioning

confidence: 99%

It sounds like an action potential: unification of electrical, chemical and mechanical aspects of acoustic pulses in lipids

Mussel

2019

J. R. Soc. Interface.

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“…(5) Even the less intuitive properties of APs, namely threshold behavior (a sigmoidal response, the so called all-or-none) [32] and annihilation upon collision [33,34], can be demonstrated as acoustic behavior near phase transition. Specifically, stimulation was shown to prompt a sigmoidal response of density pulses in lipid interfaces near phase transition [26], and these pulses were demonstrated to annihilate upon collision [35].…”

Section: Introductionmentioning

confidence: 99%

Similarities between action potentials and acoustic pulses in a van der Waals fluid

Mussel

2019

Sci Rep

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An action potential is typically described as a purely electrical change that propagates along the membrane of excitable cells. However, recent experiments have demonstrated that non-linear acoustic pulses that propagate along lipid interfaces and traverse the melting transition, share many similar properties with action potentials. Despite the striking experimental similarities, a comprehensive theoretical study of acoustic pulses in lipid systems is still lacking. Here we demonstrate that an idealized description of an interface near phase transition captures many properties of acoustic pulses in lipid monolayers, as well as action potentials in living cells. The possibility that action potentials may better be described as acoustic pulses in soft interfaces near phase transition is illustrated by the following similar properties: correspondence of time and velocity scales, qualitative pulse shape, sigmoidal response to stimulation amplitude (an ‘all-or-none’ behavior), appearance in multiple observables (particularly, an adiabatic change of temperature), excitation by many types of stimulations, as well as annihilation upon collision. An implication of this work is that crucial functional information of the cell may be overlooked by focusing only on electrical measurements.

“…The relation between temperature and nonlinear sound pulses was then investigated. As demonstrated previously, when the membrane set slightly outside the transition state is perturbed locally with sufficient power, a finite, nonlinear change in the local density relative to the undisturbed state is generated, and this disturbance propagates as a solitary pulse [15,21]. Because excitable systems typically exhibit nonlinear behavior (i.e., all-or-none), we studied nonlinear pulses here to compare the pulse characteristics in parallel.…”

Section: Resultsmentioning

confidence: 95%

“…Preparation and excitation of monolayer were performed in similar fashion as described previously [15,21]. Briefly, 1,2-dipalmitoyl-sn-glycero-3-phosphocholine (DPPC) was mixed with FRET-pair fluorophores at 98:1:1 w/v% (lipid : DPPC, Avanti Polar; Alabaster, AL, USA; donor/acceptor dye: NBD-PE/Texas Red DHPE, Thermo Fischer Scientific; Waltham, MA, USA).…”

Section: Methodsmentioning

confidence: 99%

Nonlinear pulses at the interface and its relation to state and temperature

Kang

2020

Eur. Phys. J. E

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Environmental temperature has a well-conserved effect on the pulse velocity and excitability of excitable biological systems. The consistency suggests that the cause originates from a fundamental principle. A physical (hydrodynamic) approach has proposed that the thermodynamic state of the hydrated interface (e.g., plasma membrane) determines the pulse behavior. This implies that the temperature effect happens because the environmental temperature affects the state of the interface in any given system. To test the hypothesis, we measured temperature-dependent phase diagrams of a lipid monolayer and studied the properties of nonlinear acoustic pulses excited along the membrane. We observed that the membrane in the fluid-gel transition regime exhibited lower compressibility (i.e., stiffer) overall with increasing temperature. Nonlinear pulses excited near the transition state propagated with greater velocity with increasing temperature, and these observations were consistent with the compressibility profiles. Excitability was suppressed significantly or ceased completely when the state departed too far from the transition regime either by cooling or by heating. The overall correlation between the pulses in the membrane and in living systems as a function of temperature supports the view that the thermodynamic state of the interface and phase transition are the key to understanding pulse propagation in excitable systems.