Several types of cells' skeletal, muscle, nerve, epithelia, and heart have been shown to contain ion channels which are sensitive to membrane tension. In chick skeletal muscle, the transduction persists in excised patches and involves no chemical messengers. Quantitative analysis of single channel records reveals that the sensitivity to stretch can be described by a linear four state model with three closed (C) and one open (O) state: (Formula: see text). Only the rate constant k12 is sensitive to tension (and membrane potential) following the law: k12 = kO12 exp/(theta T2 + alpha V) where theta is a constant describing the sensitivity to tension, T, and alpha is a constant describing the sensitivity to voltage, V, and kO12 is a constant. The form of the tension sensitivity can be accounted for by a model in which strain energy is used to gate the channel. Analysis of strain sensitivity, theta, indicates that the channel must concentrate energy from a large (ca. 500-nm diameter) area of membrane which suggests that the channel is in series with a component of the cytoskeleton. Treatment with cytochalasins suggests that actin is mechanically in parallel with the channel. When a channel with the above properties is incorporated into a simple model of mechanical transduction in hair cells, the resulting model is capable of explaining the kinetic features and the sensitivity found in the cochlear-vestibular system. The proposed gating mechanism of mechanical transduction appears to be general and can account for existing data on a variety of systems.