Comparative Transduction Mechanisms of Hair Cells in Utriculus. I. Responses to Intracellular Current

1. Hair cells in whole-mount in vitro preparations of the utricular macula of the bullfrog (Rana catesbeiana) were selected ac= cording to their macular location and hair bundle morphology. The voltage responses of selected hair cells to intracellular current steps and sinnsoids in the frequency range of 0.5-200 Hz were studied with conventional intracellularecordings. 2. The utricularmacula isdivided intomedial and lateralparts by the striola, a 75to l()O-um zone thatruns fornearlythe entire lengthof the sensory macula near itslateralborder.The striolais distinguishedfrom flanking cxtrastriolaregionsby the elevated heightof itsapicalsurfaceand the wider spacing of itshaircells. A linedividing hair cellsof opposing polarities,located near the lateralborder of the striola,separatesitinto medial and lateral parts.On average,the striolaconsistsof fiveto seven medial and two to threelateralrows of hair cells. 3. Utricular hair cellswere classifiedinto four types on the basisof hair bundle morphology. Type B cells,the predominant hair celltype in the utriculaxmacula, are small cellswith short stereociliand kinocilia2-6 times as long as theirlongeststereocilia.These haircellswere found throughout the extrastrioland, more rarely,in the striolaregion.Three otherhaircelltypeswere restrictedto the striolarregion.Type C cells,found primarily in the outer striolarows, resemble enlarged versionsof Type B hair cells.Type F ceilshave kinociliaapproximately equal inlength to theirlongest stcreociliand arc restrictedto the rniddlcstriolar rows.Type E cells,found only in the inncrrnoststriolarows, have short kinociliawith prominent kinociliaxybulbs. 4. The restingpotentialof 99 haircellswas -58.0 _ 7.6 (SD) mV and did not vary significantly forhaircellsin differingmaculaxlocationsor with differinghairbundle morphology. The Rr_ of hair cells,measured from the voltage response to current steps, varied from 200 to >2,000 Mi2 and was not well correlatedwith cellsize.On average,Type B ceilshad the highestRN, followed by Type F, Type E, and Type C cells.When normalized to their surface area,the membrane resistanceof haircellsranged from < 1,000 to > l0,000 kfl.cm 2. The input capacitance of hair cells ranged from <3 to > 15 pA, corresponding on average to a mereblanc 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 IV relations that saturated for larger depolaxizing 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 -I00 mY. 6. The voltage responses ofType B cells to intracelIular 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 cellswere fast,peaking in 10-15 ms, and did not vary with current amplitude. Type F cellshad slower responses,peaking in 25-50 ms. Most Type E ceils, unlikeotherutricularhairceils,were electricallyresonant, exhibiting one to three cycles of highly damped oscillationsatthe onset of depolarizingand the terminationof hyperpolaxizingcurrent steps.A few T.vpc E cellsdisplayed spikclikeresponses. 7. To simulate thein vivo situationduring hairbundle stimulation I examined the voltage responses of utricularhair cellsto sinusoidalcurrents in the frequency range of 0.5-200 Hz. Type B and Type C ceilshad nearly linearresponses for a wide range of stimulus amplitudes. Type E and, to a lesserextent,Type F ceils displayed largenonlinear deviationsduring the depolarizing portion of theirresponse.These deviationswere most evident at low stimulus frequencies and theirpeak shiftedwith increasing frequency in individualcells. 8. My resultssuggestthatutricularhairceilsdifferin theircomplements of basolatcralmembrane conductances. These conductances modify the sensitivity and response dynamics of haircells to naturalstimulation.Type B and T.vpcF cells,forexample, have highRN and are dominated by slow potassium currents,suggesting thatthey encode tonichead movement. Type C cells,on the other hand, have low RN and fastermembrane currents,enabling them to encode phasic head movements over a wide range ofamplitudes and frequencies.Type E cellsare electrically resonating and presumably enable the bullfrogutriculus.toencode substratc-borne vibration. 9. The utriculaxmacula isorganized to encode both tonic and dynamic displacement. Hair cellsin extrastriolaxregions possess only low-frequency sensitivity and presumably encode staticgravityand tonic head movements. Hair celltypes restrictedto the striola,on the other hand, arc adapted to encode high-frequency information. Within thisdynamic zone there isa segregation of function,with Type C ceilsin the outer striolarrows providing dynamic gravitysensitivity and Type E cellsin theinnermost rows supplying vibratorysensitivity.