The living state: How cellular excitability is controlled by the thermodynamic state of the membrane

Fillafer, Christian; Paeger, Anne; Schneider, Mat­thias

doi:10.1016/j.pbiomolbio.2020.10.003

Cited by 18 publications

(21 citation statements)

References 90 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Within this frame, cell membranes are excitable if the resting state is in the vicinity of an ordered-disordered transition. Any variable that influences the position of the transition relative to physiological conditions potentially affects the excitability of the membrane, as shown in Figure 4 A,B, and clearly explained by Fillafer et al [ 164 ]. In line with this, the Meyer-Overton correlation, known for a long time, states that the potency of general anesthetics is proportional to their solubility in the lipid membrane [ 165 ].…”

Section: Potentials Across Membranesmentioning

confidence: 97%

See 1 more Smart Citation

On the Coupling between Mechanical Properties and Electrostatics in Biological Membranes

Galassi

Wilke

2021

Membranes

View full text Add to dashboard Cite

Cell membrane structure is proposed as a lipid matrix with embedded proteins, and thus, their emerging mechanical and electrostatic properties are commanded by lipid behavior and their interconnection with the included and absorbed proteins, cytoskeleton, extracellular matrix and ionic media. Structures formed by lipids are soft, dynamic and viscoelastic, and their properties depend on the lipid composition and on the general conditions, such as temperature, pH, ionic strength and electrostatic potentials. The dielectric constant of the apolar region of the lipid bilayer contrasts with that of the polar region, which also differs from the aqueous milieu, and these changes happen in the nanometer scale. Besides, an important percentage of the lipids are anionic, and the rest are dipoles or higher multipoles, and the polar regions are highly hydrated, with these water molecules forming an active part of the membrane. Therefore, electric fields (both, internal and external) affects membrane thickness, density, tension and curvature, and conversely, mechanical deformations modify membrane electrostatics. As a consequence, interfacial electrostatics appears as a highly important parameter, affecting the membrane properties in general and mechanical features in particular. In this review we focus on the electromechanical behavior of lipid and cell membranes, the physicochemical origin and the biological implications, with emphasis in signal propagation in nerve cells.

show abstract

Section: Potentials Across Membranesmentioning

confidence: 97%

“…(C) According to the melting point depression theory[162,166], anesthetics leave the resting state in the disordered phase, but increase its distance to the transition. This figure is reproduced from ref [164]. with permission from Elsevier.…”

mentioning

confidence: 99%

On the Coupling between Mechanical Properties and Electrostatics in Biological Membranes

Galassi

Wilke

2021

Membranes

View full text Add to dashboard Cite

show abstract

“…The random opening and closing of ion channels in resting-state results in electrical currents, inducing membrane potential fluctuations without presynaptic inputs (White et al, 2000 ). Although little is known about the thermodynamic properties of neurons, it has been suggested that the action potential forces the membrane through the transition from fluid to gel state, leading to the membrane potential change (Aizawa et al, 1975 ; Heimburg and Jackson, 2005 ; Andersen et al, 2009 ; Fillafer et al, 2021 ).…”

Section: Discussionmentioning

confidence: 99%

Numerical Simulation: Fluctuation in Background Synaptic Activity Regulates Synaptic Plasticity

Takeda

Hata

Yamazaki

et al. 2021

Front. Syst. Neurosci.

View full text Add to dashboard Cite

Synaptic plasticity is vital for learning and memory in the brain. It consists of long-term potentiation (LTP) and long-term depression (LTD). Spike frequency is one of the major components of synaptic plasticity in the brain, a noisy environment. Recently, we mathematically analyzed the frequency-dependent synaptic plasticity (FDP) in vivo and found that LTP is more likely to occur with an increase in the frequency of background synaptic activity. Meanwhile, previous studies suggest statistical fluctuation in the amplitude of background synaptic activity. Little is understood, however, about its contribution to synaptic plasticity. To address this issue, we performed numerical simulations of a calcium-based synapse model. Then, we found attenuation of the tendency to become LTD due to an increase in the fluctuation of background synaptic activity, leading to an enhancement of synaptic weight. Our result suggests that the fluctuation affects synaptic plasticity in the brain.

show abstract

“…Finally, going back to the burning fuse analogy of action potential, the material in general expands during such a process where as this study shows a reversible compression (and a thermotropic condensation), making it highly unlikely that wave front propagation does not involve momentum transfer(75). However, answering that question completely will require systematic investigation of the entire phenomenon as a function of thermodynamic state (76). Most important would be to show the dependence of conduction velocity on a thermodynamic susceptibility.…”

Section: Challenges and Limitationsmentioning

confidence: 99%

A Thermodynamic Interpretation of the Stimulated Raman Spectroscopic Signature of an Action Potential in a Single Neuron

Shrivastava

Lee

Cheng

2020

Preprint

View full text Add to dashboard Cite

It has previously been suggested that the plasma membrane condenses and melts reversibly during an action potential in a neuron. If true it has fundamental consequences for our understanding of the regulation of biological functions during an action potential. It has long been known that the electrical dipoles in the neuronal membrane reorient during an action potential, observed through a variety of optical methods. However, this information has been insufficient to confirm if and how the collective thermodynamic state of the neuronal membrane changes during an action potential. Here, we show that hyperspectral stimulated Raman spectroscopy can resolve the thermodynamic state of the neuronal membranes in a single neuron during an action potential. Based on these measurements we provide the first evidence that the system condenses during the de-polarisation phase and melts during the polarisation phase. Statement of SignificanceWhile action-potentials can be measured using a variety of methods, none of these methods have been able to provide sufficient information to characterise the collective thermodynamic state of the membrane during an action-potential. Therefore, new tools are required to satisfactorily resolve the fundamental nature of the phenomenon, i.e. does the wave-front propagates irreversibly/diffusively as in the burning of a fuse, or reversibly/elastically as in the propagation of sound. It has been postulated that if action-potentials indeed propagate elastically, then the membrane must undergo a localised condensation during the actionpotential. This article confirms and quantifies the condensation of the membrane during an action-potential based on time-resolved changes in the Raman band at 2930 cm -1 , also known as the "melting-marker".

show abstract

The living state: How cellular excitability is controlled by the thermodynamic state of the membrane

Cited by 18 publications

References 90 publications

On the Coupling between Mechanical Properties and Electrostatics in Biological Membranes

On the Coupling between Mechanical Properties and Electrostatics in Biological Membranes

Numerical Simulation: Fluctuation in Background Synaptic Activity Regulates Synaptic Plasticity

A Thermodynamic Interpretation of the Stimulated Raman Spectroscopic Signature of an Action Potential in a Single Neuron

Contact Info

Product

Resources

About