1. Type I vestibular hair cells were isolated from the cristae ampullares of the semicircular canals of the Mongolian gerbil (Meriones unguiculatus) and the white king pigeon(Columba livia). Dissociated type I cells were distinguished from type II hair cells by their neck to plate ratio (NPR) and their characteristic amphora shape. 2. The membrane properties of gerbil and pigeon type I hair cells were studied in whole-cell voltage- and current-clamp using the perforated patch technique with amphotericin B as the perforating agent. 3. In whole-cell current-clamp, the average zero-current potential, V-z, measured for pigeon type I hair cells, was -70 +/- 7 (SD) mV (n = 18) and -71 +/- 11 mV (n = 83) for gerbil type I hair cells. 4. At V-z, for both gerbil and pigeon type I hair cells, a potassium current (I-KI) was greater than or equal to 50% activated. This current deactivated rapidly when the membrane potential was hyperpolarized below -90 mV. 5. I-KI was blocked by externally applied 4-aminopyridine (4-AP) (5 mM) and by internally applied 20 mM tetraethylammonium (TEA). It was also reduced when 4 mM barium was present in the external solution. The degree of block by barium increased as the membrane potential became more positive. External cesium (5 mM) blocked the inward component of I-KI. When I-KI was pharmacologically blocked, V-z depolarized by similar to 40 mV. Therefore I-KI appears to be a delayed rectifier and to set the more negative V-z noted for isolated type I hair cells when compared to isolated type II hair cells, which do not have I-KI. 6. A second, smaller potassium current was present at membrane potential depolarizations above -40 mV. This current was blocked by 30-50 mM, externally applied TEA, 100 mu M quinidine, 100 nM apamin, but not 100 nM charybdotoxin, indicating that this is a calcium-activated potassium current, I-K(Ca), different from the maxi-K calcium-activated potassium current found in most other hair cells.