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      Mechanical surface waves accompany action potential propagation

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      Nature Communications
      Springer Science and Business Media LLC

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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.

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          Most cited references43

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          Fluorogenic probes for live-cell imaging of the cytoskeleton.

          We introduce far-red, fluorogenic probes that combine minimal cytotoxicity with excellent brightness and photostability for fluorescence imaging of actin and tubulin in living cells. Applied in stimulated emission depletion (STED) microscopy, they reveal the ninefold symmetry of the centrosome and the spatial organization of actin in the axon of cultured rat neurons with a resolution unprecedented for imaging cytoskeletal structures in living cells.
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            Critical fluctuations in plasma membrane vesicles.

            We demonstrate critical behavior in giant plasma membrane vesicles (GPMVs) that are isolated directly from living cells. GPMVs contain two liquid phases at low temperatures and one liquid phase at high temperatures and exhibit transition temperatures in the range of 15 to 25 degrees C. In the two-phase region, line tensions linearly approach zero as temperature is increased to the transition. In the one-phase region, micrometer-scale composition fluctuations occur and become increasingly large and long-lived as temperature is decreased to the transition. These results indicate proximity to a critical point and are quantitatively consistent with established theory. Our observations of robust critical fluctuations suggest that the compositions of mammalian plasma membranes are tuned to reside near a miscibility critical point and that heterogeneity corresponding to < 50 nm-sized compositional fluctuations are present in GPMV membranes at physiological temperatures. Our results provide new insights for plasma membrane heterogeneity that may be related to functional lipid raft domains in live cells.
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              On soliton propagation in biomembranes and nerves.

              The lipids of biological membranes and intact biomembranes display chain melting transitions close to temperatures of physiological interest. During this transition the heat capacity, volume and area compressibilities, and relaxation times all reach maxima. Compressibilities are thus nonlinear functions of temperature and pressure in the vicinity of the melting transition, and we show that this feature leads to the possibility of soliton propagation in such membranes. In particular, if the membrane state is above the melting transition solitons will involve changes in lipid state. We discuss solitons in the context of several striking properties of nerve membranes under the influence of the action potential, including mechanical dislocations and temperature changes.
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                Author and article information

                Journal
                Nature Communications
                Nat Commun
                Springer Science and Business Media LLC
                2041-1723
                November 2015
                March 30 2015
                November 2015
                : 6
                : 1
                Article
                10.1038/ncomms7697
                25819404
                bc4136e7-21f2-458a-b36d-8169d313fe83
                © 2015

                http://www.springer.com/tdm

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