1. Hair cells in whole-mount in vitro preparations of the utricular macula of the bullfrog (Rana catesbeiana) were selected according to their macular location and hair bundle morphology. The voltage responses of selected hair cells to intracellular current steps and sinusoids in the frequency range of 0.5-200 Hz were studied with conventional intracellular recordings. 2. The utricular macula is divided into medial and lateral parts by the striola, a 75- to 100-mu m zone that runs for nearly the entire length of the sensory macula near its lateral border. The striola is distinguished from flanking extrastriolar regions by the elevated height of its apical surface and the wider spacing of its hair cells. A line dividing hair cells of opposing polarities, located near the lateral border of the striola, separates it into medial and lateral parts. On average, the striola consists of five to seven medial and two to three lateral rows of hair cells. 3. Utricular hair cells were classified into four types on the basis of hair bundle morphology. Type B cells, the predominant hair cell type in the utricular macula are small cells with short stereocilia and kinocilia 2-6 times as long as their longest stereocilia. These hair cells were found throughout the extrastriola and, more rarely, in the striolar region. Three other hair cell types were restricted to the striolar region. Type C cells, found primarily in the outer striolar rows, resemble enlarged versions of Type B hair cells. Type F cells have kinocilia approximately equal in length to their longest stereocilia and are restricted to the middle striolar rows. Type E cells, found only in the innermost striolar rows, have short kinocilia with prominent kinociliary bulbs. 4. The resting potential of 99 hair cells was -58.0 +/- 7.6 (SD) mV and did not vary significantly for hair cells in differing macular locations or with differing hair bundle morphology. The R(N) of hair cells, measured from the voltage response to current steps, varied from 200 to >2,000 M Omega and was not well correlated with cell size. On average, Type B cells had the highest R(N), followed by Type F, Type E, and Type C cells. When normalized to their surface area, the membrane resistance of hair cells ranged from <1,000 to >10,000 k Omega cm(2). The input capacitance of hair cells ranged from <3 to >15 pA, corresponding on average to a membrane capacitance of 0.8 + 0.2 pA/cm(2). 5. The current-voltage (I-V) relations of utricular hair cells were correlated with their hair bundle morphology. Type B cells, in both the striolar (n = 4) and extrastriolar (n = 3) regions, had slightly outwardly rectifying I-V relations. The I-V relations of Type C cells (n = 15) were nearly linear for both depolarizing and hyperpolarizing currents. Type F cells (n = 19) had sigmoidal I-V relations that saturated for larger depolarizing and hyperpolarizing currents. Type E cells (n = 14),in addition to being outwardly rectifying at depolarizing currents, had a pronounced inward (anomalous) rectification for voltages more negative than - 100 mV. 6. The voltage responses of Type B cells to intracellular current were largely passive. Hair cells restricted to the striolar region, on the other hand, exhibited active voltage responses at the onset and termination of depolarizing currents. The voltage responses of Type C cells were fast, peaking in 10-15 ms, and did not vary with current amplitude. Type F cells had slower responses, peaking in 25-50 ms. Most Type E cells, unlike other utricular hair cells, were electrically resonant, exhibiting one to three cycles of highly damped oscillations at the onset of depolarizing and the termination of hyperpolar
