In amniotes, there are two types of hair cells, designated I and II, that differ in their morphology, innervation pattern, and ionic membrane properties. Type I cells are unique among hair cells in that their basolateral surfaces are almost completely enclosed by an afferent calyceal nerve terminal. Recently, several lines of evidence have ascribed a motile function to type I hair cells. To investigate this, elevated external K⁺, which had been used previously to induce hair cell shortening, was used to induce shape changes in dissociated mammalian type I vestibular hair cells. Morphologically identified type I cells shortened and widened when the external K⁺ concentration was raised isotonically from 2 to 125 mM. The shortening did not require external Ca²⁺ but was abolished when external Cl was replaced with gluconate or sulfate and when external Na⁺ was replaced with N-methyl-D-glucamine. Bumetanide (10-100 µM), a specific blocker of the Na⁺-K⁺-Cl cotransporter, significantly reduced K⁺-induced shortening. Hyposmotic solution resulted in type I cell shape changes similar to those seen with high K⁺, i.e., shortening and widening. Type I cells became more spherical in hyposmotic solution, presumably as a result of a volume increase due to water influx. In hypertonic solution, cells became narrower and increased in length. These results suggest that shape changes in type I hair cells induced by high K⁺ are due, at least in part, to ion and solute entry via an Na⁺-K⁺-Cl cotransporter, which results in cell swelling. A scheme is proposed whereby the type I hair cell depolarizes and K⁺ leaves the cell via voltage-dependent K⁺ channels and accumulates in the synaptic space between the type I hair cell and calyx. Excess K⁺ could then be removed from the intercellular space by uptake via the cotransporter.