Membrane Electromechanics in Biology, with a Focus on Hearing

Abstract

Cells are ion conductive gels surrounded by a ~5-nm-thick insulating membrane, and molecular ionic pumps in the membrane establish an internal potential of approximately -90 mV. This electrical energy store is used for high-speed communication in nerve and muscle and other cells. Nature also has used this electric field for high-speed motor activity, most notably in the ear, where transduction and detection can function as high as 120 kHz. In the ear, there are two sets of sensory cells: the "inner hair cells" that generate an electrical output to the nervous system and the more numerous "outer hair cells" that use electromotility to counteract viscosity and thus sharpen resonance to improve frequency resolution. Nature, in a remarkable exhibition of nanomechanics, has made out of soft, aqueous materials a microphone and high-speed decoder capable of functioning at 120 kHz, limited only by thermal noise. Both physics and biology are only now becoming aware of the material properties of biomembranes and their ability to perform work and sense the environment. We anticipate new examples of this biopiezoelectricity will be forthcoming.

Figure 1

Cartoon of a biomembrane after Singer & Nicolson from Dowhan et al. A variety of proteins, including ion channels, receptors, and enzymes, are in or near the membrane. Glycosylphosphatidylinositol (GPI)-anchored proteins are those anchored to the membrane by the glycolipid GPI.

Figure 2

The parameters of flexoelectricity (taken from the logo of the 1st and 2nd Flexoelectric Congresses, SUNY-Buffalo, 2001 and Rice-Houston, 2003). On the right, flexoelectric (curvature-induced) polarization of the membrane P_s and sign convention about the flexocoefficient f. For the case shown, f is positive. R₁ and R₂ are the principal radii of membrane curvature.

Figure 3

Distribution of electric potential across a flat (solid line) and a curved (broken line) bilayer lipid membrane. The membrane is composed of lipids carrying surface charge and permanent dipoles. The potential distribution of a curved membrane corresponds to the open circuit condition. Δ V = Ф_d + Ф_s is the total surface potential of a monolayer (measurable by a vibrating electrode on the same lipid monolayer spread over the air-water interface of a classical Langmuir trough); Ф_d is the dipolar potential of the monolayer; Ф_s is the surface charge potential of the monolayer; the superscripts i and o stand for the inner and outer lipid monolayer, respectively. U_f is the curvature-generated (flexoelectric) potential difference. Reprinted with permission from Reference .

Figure 4

Movement of a human embryonic kidney cell as the voltage is stepped. (a) Stimulus voltage; (b) cell current; (c) membrane movement at a set point of 0.7 nN. The inset is a scaled cesium atom (5.2 Å diameter). Adapted with permission from Reference .

Figure 5

Sensory hair cell anatomy. Stereocilia are arranged in rows of different length and collectively make up the stereocilia bundle. Reprinted with permission from Reference .

Figure 6

The organ of Corti and outer hair cell. (a) The central axis of the spiraling cochlea is to the left of the drawing. Adapted from Reference . (b) Adapted from Reference .

Figure 7

Postulated nanoscale rippling of the outer hair cell (OHC) lateral wall plasma membrane. OHC is shown at low magnification when hyperpolarized (a) and depolarized (c). A portion of the lateral wall is shown at higher magnification in (b) and (d). These cartoons portray flexoelectric alterations in membrane curvature associated with electromotile length changes. The plasma membrane is attached to cortical lattice pillars (tan), which, in turn, are attached to actin filaments (purple). These are cross linked with the elastic spectrin (thin red) filaments. Reprinted with permission from Reference .