Carhart Memorial Lecture

5:00 - 6:15, March 7th

Piezoelectric Membrane-based Motors in the Outer Hair Cell

William E. Brownell, Ph.D.
Baylor College of Medicine Houston, Texas

The cylindrical outer hair cell appeared with mammals over 200 million years ago is the most exotically specialized hair cell. Morphological and molecular features of its lateral wall endow it with the ability to generate mechanical force at high (> 50 kHz) frequencies. The force alters the vibrations of the organ of Corti enhancing the perception and discrimination of high frequency sounds. The lateral wall is an elegant, nanoscale (~100 nm thick), piezomotor that is self-assembling and self repairing. It consists of three layers, two are membranes and sandwiched between them is a layer of cytoskeletal proteins with preferential orientations. The force generating mechanism is based on a direct conversion of the transmembrane electrical potential into mechanical energy. The mechanism would be functionally useless if the membrane behaved like the membranes of other cells and was unable to sustain transmembrane receptor potentials at high frequencies. Providentially, a strong coupling of electrical and mechanical energy sustains high frequency charge movements. Stretching or compressing an outer hair cell alters its membrane potential and, conversely, changing the electrical potential alters its length. The bi-directional energy conversion resembles piezoelectricity both qualitatively and quantitatively. Piezoelectricity was discovered in the early 1880s by Jacques and Pierre Curie. They found that mechanically deforming one of a variety of crystalline materials produced electricity and coined the term piezoelectricity (from the Greek, piezein--to press). A few years later they discovered the same crystals changed their shape in response to electrical stimulation. Piezoelectric materials have been used in applications that range from marine sonar and medical ultrasound devices to laptop microphones. Biological piezoelectricity has been observed in bone and ligaments. Prestin, an integral membrane protein belonging to the Slc26A family of anion transporters, has been isolated, cloned and shown to endow transfected test cells with piezoelectric properties resembling those of OHCs. An equivalent circuit for the outer hair cell that includes piezoelectricity shows a greater admittance at high frequencies than one containing only membrane resistance and capacitance. The model also predicts resonance at ultrasonic frequencies that is inversely proportional to cell length. These features suggest all mammals use outer hair cell piezoelectricity to support the high frequency receptor potentials that drive electromotility. It is also possible that bats, whales and dolphins use outer hair cell piezoelectric resonance in detecting the species-specific vocalizations they use in echolocation.