potentials
Peter Dallos and Mary Ann Cheatham
AuditoryPhysiology
Laboratory(HughKnowlesCenter)andDepartmentofNeurobiology
andPhysiology,
NorthwesternUniversity,
Evanston,Illinois60208
Ac and dc receptorpotentialcomponents
in responseto tone-burststimuliweremeasured
from innerhair cellsin the third cochlearturn of the guineapig. Comparisons
weresought
betweenconditionswhenconstantpolarizingcurrentwasinjectedinto the cell throughthe
recordingelectrodeand whentherewasno extrinsiccurrent.Hyperpolarizationof the cell
increased
all responses,
whiledepolarization
decreased
them.The input-outputfunctionswere
verticallytranslatedby currentinjection.The extentof translationwasa functionof current
level. In addition,the amountof current-inducedchangewasfrequencydependent.Largest
changeswereseenat low frequencies
and the current-induced
changetendedtowarda constant
high-frequency
asymptotebetween1-2 kHz. Changesin the dc response
componentwere
considerablyin excessof thosefor the fundamentalac response.The frequency-dependent
effectsare quantifiedwith the aid of a hair cell circuitmodel [ P. Dallos,Hear. Res. 14, 281291 (1984) ]. It is assumedthat the quantityalteredby polarizingcurrent(actuallyby the
transmembrane
voltage)is the resistance
of the cell'sbasolateralmembrane.
PACS numbers: 43.64.Ld, 43.64.Bt, 43.64.Kc
INTRODUCTION
A windowwasopenedin theboneoverthe striavascularis;the cochleawasbacklightedto aid in aimingthe electrode toward the shadowof the organ of Corti. The electrodeswere introducedthrough the stria, through scala
media,and into the organof Corti, trackingparallelto the
reticularlamina.The recording(and current-passing)
electrodes were fabricated from 1.2-mm-o.d. glass with a
Brown-Flaminghorizontal puller. They were backfilled
with 2M KAc and had resistances
rangingbetween80 and
150Mfg. Preamplificationandcurrentpassingwereaccomplishedwith a high-impedance,capacitance-compensated
amplifier/constantcurrent sourcebridge circuit (Dagan
8700).
circuit of
0001-4966/90/041636-12500.80
1636
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whosefrequencies
arerelativelyhighevenfor lowerfrequency fundamentals.The presentpaperdoesnot dealwith these
harmonics.
Several measurements
from
Fourier
-2 nA
UI,,
0nA
'
'
'
0 nA
+1
nAUL
UI'
+1
nA
11 0
Time
(mS)Goin:200.OX
21 0
31 0
41 0
51 0
61 0
tie(ms)Goin:200.OX
FIG. 1. Averagedresponse,waveforms
(labeled"raw data") obtainedfrom
two inner hair cells in the samecochlea. In both, the stimulus is 700 Hz at 70
withthecellwasmaintained
for 53 min.'Organof Corti
responses
weremeasured
beforepenetrationandafterlossof
the IHC, and they remainedinvariant.This signifiesthe stability of thepreparationoverthe recordingperiodof interest.
In Fig. 2, ac magnitudefunctionsare shownfor a frequency(700 Hz) that is somewhatbelowthe BF for two
polarizingcurrentlevels, + 1 and -- 2 nA, and for the nocurrentcondition.The functionsappearto shiftin the vertical directionwithoutchangingshape.With hyperpolarizing
(negative)current,thereisan increasein response;
depolarizing (positive) current causesa decrease.While the depolarizingand hyperpolarizingcurrentswere differentin
this case, it is still clear that the latter is more effective in
increasingresponses
than the former is in decreasingthem.
Theseplots simply affirm observations
alreadymade, that
depolarizingand hyperpolarizingcurrentsare effectivein
alteringthesound-induced
response
magnitude,andthat the
effectsare asymmetrical(Russell, 1983;Nuttall, 1985;Dal-
AND DISCUSSION
arepresentedprimarily asfrequencyresponse
functionsover
the relevantfrequencyrange.The bestfrequency(BF) of
the cell is 1000Hz at low sound-pressure
levels.The apparent bestfrequencyat 50 dB SPL, wheremostmeasurements
were taken, is shifted down to 800 Hz. This downshift of the
frequencyof maximumresponse
with increasingintensityis
well documented(Russell and Sellick, 1978;Dallos, 1985a)
and is probablyrelatedto a similar nonlinearphenomenon
los, 1986).
reportedin the literature,which tendto conformto the patternsof rectangularhyperbolas.In fact,for the morelimited
1637
1637
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Frequency
0.2
-2 nA4ra'<zx)oOOOo
(kHz)
05
I
i
ill
IO
rr
02
0.
700 Hz
0.5
0.2
FIG. 4. Ac response
magnitudeasa
functionof stimulusfrequencyat a
constant,50-dB sound-pressure
level at the eardrum. Responsesare
MR05
'0.02
50 dB
MR056
from a third-turn inner hair cell. Data are obtained from Fourier transforms
of theaveragedresponses
to tonebursts.Stimulusfrequencyis700Hz. Data
are shownfor threecurrentlevels,0, - 2, and d- 1 nA passedinto the cell
throughthe recordingelectrode.
rangeof + 1 Pa, suchan analyticaldescriptionis appropriate for these data (Dallos and Cheatham, 1989a,b). The
manner.
current-dependentincreases(with hyperpolarization) or
45
+1 nA
-2
Peak
Pressure
(Pa)
-4501
.I 0.2
I I I0.5
I IIlllI
Frequency (kHz)
1638
1638
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2. Discussion
blytheshapefactor/3,or thefractionalresistance
changey/,
or both. Changesin the shapefactor imply that current
modifieseitherthe apicalor the basolateralresistances
of the
IHC membrane.Inasmuch as voltage-dependent
conductanceshave been reportedfor the latter (Kros and Crawford, 1988, 1989), thisis a reasonable
possibility.
Thealternative,
a current-dependent
changeinyI, suggestsan alterationof the input machineryof the IHC. This
could occurby either a changein the transducerchannels
dueto currentor by a modificationof the mechanicalinput
itself,conceivablyby someeffecton the cilia. The transducer
conductanceis probablynot voltagedependent(Corey and
Hudspeth, 1979; Ohmori, 1985; Holton and Hudspeth,
1986) but, dueto reciprocity,the gatingcompliancemay be
(Howard and Hudspeth, 1988). In fact, Assadet al. ( 1989)
haveshownrecentlythat electricalpolarizationof saccular
1639
hair
aroundthebestfrequency,whilethecell'stransduction
processhasmajorinfluenceawayfrom the bestfrequencyof the
cell (Patuzzi and Sellick, 1983). Since the influence of cur-
1639
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(Mountain et al., 1983), and its correlateshave been measuredin turtle cochlearhair cells (Crawford and Fettiplace,
1985) and in frog vestibularhair cells (Howard and Hud-
to be made. To obtain fits for the actual data, one must add
11.6 dB for the - 2-nA case,5 dB for -- 1 nA, and subtract
somemagnitudecorrectionsare necessary
to obtaina good
match.Thesecorrectionsare relativelysmall:2.6 dB for the
- 2-nA case,0.4 dB for -- 1 nA, and -- 0.4 dB for + 1 nA.
Eitherthelow- or thehigh-pass
modelcanyieldtheconfigurationof amplitudeand phasechangesseen.Consideration
of the physicalnatureof a putativehigh-pass(ciliary mechanics)versuslow-pass(cell membrane)filter,alongwith
their locationcomparedto the nonlinearelement,as discussed
above,suggests
that the low-passmechanism
islikely
to be dominant in producing the large low-frequency
changes.
A knownlow-passfilter associated
with innerhair cells
is dueto the parallelcombinationof membranecapacitance
andresistance.
Voltage-dependent
conductances
in thecell's
basolateralmembranewould affectthe cutofffrequencyat
different membrane voltages.Specifically,depolarization
Frequency
I
O.I
i
i i iii
, i
! I I ill
change
(dB)
o..
o.
-45t I
-90
,,
i
o
chnge(O!4
F-----__;__
, ,
(a)
90'
'
II
45
-:::::
0-
(b)
1640
quency,while hyperpolarization
shouldresultin lowercutoff. Recall that hyperpolarizationincreasedthe low-frequencyresponsein our experiments.Loweringthe cutoff
frequencyof a low-passfilter [seeFig. 6(a) ] producedthe
correspondingprofile of frequency-dependent
changes.
Thus the mechanismwhereby extrinsiccurrent influences
the impedanceof the basolateralcell membraneand,consequently,itsfiltercutoff,produces
theappropriate
patternof
changes.In the Appendix,we includea morequantitative
treatmentof such changes.Basedon the model (Dallos,
1984), changesin filter functionare computedassuming
current-induced
sistance,
R b. We showthat goodagreementmay be found
with the experimentalresults(comparedatapointsand interruptedlinesin Fig. 5). It is concluded
that thefrequencydependentchangesseenin the fundamentalresponse
componentcanbeaccounted
for asa consequence
of thechange
in the resistance of the IHC's
maybe expressed
differentlyby statingthat the controlling
influenceoverfrequency-dependent
response
changes
is the
current-inducedmodificationof the shape-factor
fl. We see
in theAppendixthat,fromitsnormalvalueoffl - 0.05,the
three current levelsused, -- 2, -- 1, and + 1 nA, alter fl to
values0.15, 0.09, and 0.042, respectively.
1640
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frequencies,of the order of 25 dB for -- 2 nA. Thesedecreaseand appearto asymptoteat higher frequencies.In
1985).
orderto providereadycomparisonwith the fundamentalac
To summarize,current-inducedfrequency-dependent response
component,corresponding
changesin thismeasure
effectsseenin the fundamentalcomponentof ac receptor are alsoincludedin the figurerepresentedby the theoretical
potentialscannotbe due to electrodefilter artifacts.The efcurvescomputedin the Appendix[interruptedlinesin panel
fectsare characterizedby gain and phaselag with hyperpo(b) ]. It is observedthat the changesin the dc component
larization versuslossand phaselead with depolarization. exceedthosein the fundamentalat any corresponding
freNumericalresultscouldbe fit by appropriatelyshiftingthe
quencyfor both currentlevels.
cutofffrequencyof a low-passfilter and compensating
the
Our resultshowingthat electricalpolarizationhasa freresultinglosswith a constantgain. Modeling the current
quency-dependent
effectuponthe dc response
might appear
effectswith this simplechangein a low-passfilter cutoff
to be contraryto the findingof Nuttall ( 1985). He showed
frequencyprovidesthe heuristicexplanationof the phenom- that passingcurrent into IHCs produceda frequency-indeenon.A moreappropriatemodelingapproachtakesinto acpendentshift in the equipotentialresponse(sensitivity) of
count the behavior of the IHC as an electric circuit (Dallos,
the cell, as determinedfrom the dc receptorpotential.Nut1983, 1984). In the Appendix,we examinethe quantitative tall recordedfrom basalturn cellshavingvery highbestfreconsequences
of current-inducedalterationin the resistance quencies.Theseare well abovethe regionof frequency-deof the cell's basolateralmembrane (and, hence,of/3). It is
pendent changesseen in our work. The effectsthat we
shownthat excellentfits of the amplitudeand phasedata
observeasymptoteto a constantvaluesomewhatabove1000
may be obtained.
Hz. Nuttall's data wereobtainedon this asymptoticportion
of the function.
2. Discussion
25
-2
25
20
20
os-
c I0
'- I0
o-
00.5
I
5O dB
O0)L
MR056
i
02
(a)
2-2
;,7-4-
! i Iiii
05
02
(b)
05
i
02
i ! ! iIlll
05
Frequency
(kHz) (c)
release.
and Santos-Sacchi,
1983). Theoreticalexplanationfor this
findinghasbeenprovided(Dallos et al., 1972;Billone and
Raynor, 1973;Freemanand Weiss,1988). This meansthat
dc componentspresentin basilarmembranemotion are effectivelydecoupledfrom stimulatingIHC cilia and will not
serveas direct inputs to this cell type, contraryto the assumptionsof LePage (1987, 1989). Of course,due to the
P. Dallos and M. A. Cheatham: Polarizationof inner hair cells
1641
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firm contact between outer hair cell cilia and tectorial mem-
transformations
r 0,2
o.
do
o.
,oo
ioo
Inasmuch
as the basola-
teral conductanceversustransmembranepotentialfunction
isnaturallytruncatedfor both the all-channels-open
and allchannels-closedsituations,it is inherently nonlinear. Since
at the restingmembranepotentialthe numberof openand
closedchannelsis unequal,it is also asymmetrical.Sucha
function can be derived from the conductance-data
of Kros
rangein excess
of a hundredfold.
3 We havealreadynoted
that the frequencydependence
of the current-inducedac receptorpotentialchangeappearsto dependon modification
of the conductance
of the basolateral
cell membrane.
It is
nonlinear
nentsof thereceptorpotential/
FIG. 8. Input-output functionsfrom a differentinner hair cell obtainedin
the electrodetrack prior to the one in which the other cell was located.
Membranepotentialof thiscellwas -- 20 mV. In theleft panel,theacmagnitudefunctionsare givenfor 0-, + 1-, and -- 2-nA conditions.Stimulus
1642
Membranepotentialchangesoccurduringintracellular
recordingevenif not artificiallyinducedby polarizingcurrent. Receptor potential changescommonly accompany
suchvariations(Dallos, 1985b). One may surmisethat variationsin hair cell membranepotentialscantakeplacein the
P. Dallos and M. A. Cheatham: Polarizationof inner hair cells
1642
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potentialsand,consequently,
in receptorpotentials.To illustrate theseinteractions,we presentinformation that is in
additionandcomplementaryto resultsfrom electricalpolarization experiments.A particularlyinformativeexampleis
shownin Fig. 9. Data aresummarizedherefor two recording
periods;duringthe first,the membranepotentialof the IHC
graduallyincreasedfrom -- 22 to -- 27 mV, while, during
the second,it held constant.During both periods,responses
trasted with
tone
--0.33
dB/mV
slopebetweendc andfundamentalmagnitudes
hasbeentested for statistical significance(F ratios; Pedhazur, 1982,
Chap. 12), and it exceedsa criterionlevelof 1%.
We may surmisethat, inasmuchas the transducerfunction is unlikely to be voltagedependent,evenduring "naturally occurring" changesin membranepotential, it is the
nonlinearityof the basolateralmembranethat producesthe
excessvulnerabilityof the dc response.If thesefindingscan
be generalized, then one may argue that pathological
changes,evensubtleones,could have seriouseffectson the
high-frequencyresponseof the cochleawherethe output is
completelydependenton the IHC's dc receptorpotential.
There hasbeenonebrief reporton researchwith similar
concernsasthe presentwork. Mountainet al. (1989) noted
that, in basal-turninnerhair cells,usinglow-frequencystimuli, currentinjectiondid not alter the responsewaveformor
the relative second-harmonic
tic
=.6
-
- 90
a_ -8O
/ =.76,0.6E
''U
-20
-25
Membrane
Potential
-30
(mY)
spethand Corey, 1977;Boston,1980;Crawfordand Fettiplace,1981;Russellet al., 1986). The transducernonlinearity further distortsthe alreadynonlinearsignal.
It isnot clearif thepotentialmeasured
by theintracellular electrodeclearly reflectseither the voltagedrop across
the cell's basolateralmembrane that is establishedby the
transductioncurrent itself, or the voltagedrop due to a secondarycurrentgatedby the receptorpotential.In nonmammalianhair cells,the latter caseprevails,the recordedvol-
tagedropbeingdominated
by K + andCa + currents
that
aresecondaryto the receptorpotential(CrawfordandFettiplace,1981;Lewisand Hudspeth,1983). As a consequence,
the transducernonlinearity is "hidden" under normal recordingcircumstances.
Considering
that in mammalianhair
cells,the receptorpotentialsshowsignificantrectification,
unlike normal turtle hair cells,it is possiblethat theseare
P. Dallosand M. A. Cheatham:Polarizationof innerhair cells
1643
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duringdepolarization
(KrosandCrawford,
1988).6Second,
basolateral
membrane
nonlinear
IIR nonlinear
?N
',input
L
I' bill
N,,_I ,
~1200HzlI
' ciliary
receptor
potential
transduction
...................................
of
asa consequence
of the resistance
change,thelow-pass
electrical filter of the basolateralmembraneis altered.Hyperpo-
larization(increasedresistance)pushesthe filtercutofffrequencylower,whiledepolarization
increases
thebandwidth.
Thesefilter effectsare bestseenin changesof magnitudeand
phaseofthefundamental
response
to tones.Thechanges
can
beaccounted
for by usingthehair cellcircuitmodel(Dallos,
1984)shownin theAppendix.
7 In addition,by movingto
differentpointsonthenonlinearRo functiondueto extrinsic
current,differingamountsof distortioncomponents
(here
exemplifiedby de) are generatedin the cell'svoltageresponse.
distorted input
A hi.gh-pass
filtered
. '"""/ry
motion
ACKNOWLEDGMENTS
potential ]"nonlinear
Ibasolateral membrane
filter (current-dependent)
e...
influencingvoltage-dependent
channelstherein.
5 The
changein drivingforcecouldbe estimatedfrom the highfrequencyasymptotesof the changein fundamentalresponse.For plusandminus1-nA current,onecancomputea
decrease
of approximately5 mV andan increaseof approximately 4 mV in E.
In Fig. 10, the block "basolateralmembrane"symbolizes the latter secondclassof effectstwo ways. First is a
J. Acoust.
Soc.Am.,Vol.87, No.4, April1990
intracellular
electrode
locationcan be expressedas
-- ,8(El + Er )Y
(A1)
(1 -F//) (1
wheree; is the receptorpotentialamplitude,E is the biochemicalrestingpotentialoftheinnerhaircell,andEr isthe
endocochlear
potential.The quantity//wasdefinedas the
"shapefactor."It wasexpressed
astheratioof restingresistancesof basolateraland apicalcell membranes://=R o/
R. The input is in the form of parametricexcitation:
y; = (Ra - R )/R isthefractionalresistance
change,
with
R a beingthe instantaneous
valueand R the resting(no
stimulus) value of the resistanceof the cell'sapicalmembrane.When thefractionalresistance
changeissmall,asfor
smallinputs,onecansimplifythe aboveexpression:
e;...
-- ,8(El + ET)yI
.
(A2)
(] +fi)2
The computations
below are basedon this small-signal
expression
inasmuchas we are interestedin assessing
responses
to a moderate,
50-dBSPLinput.In thebestfrequency region,thesmall-signal
assumption
is probablyviolated;
however,the simplifiedanalysisdoesyieldqualitativelycorrectdescriptions
of the system's
behavior.The formulation
wasextendedto the generalcasewhen the cell membrane
containscapacitances
in parallelwith resistances
(Dallos,
1984).In thissituation,
theexpression
ford takestheform
ez (,j2rrf)
#q2rf) (E, +
[] +
r'q2rf)
P.DallosandM.A.Cheatham:
Polarization
ofinnerhaircells
(A3)
1644
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The frequency-dependent
quantitiesmaybeexpressed
asfol-
lows:
(A4)
(A5)
(A6)
f3:
( 1 q-/)/2rr(%
q-/7'a ),
2Thechoice
of500Hz isnotarbitrary.Wehaveshownthatthird-turnIHCs
shifttheir modeof response
from velocitycontrolledat low frequencies
to
possiblydisplacementcontrolledat higher frequencies.The corner freP. Dallos and M. A. Cheatham: Polarizationof inner hair cells
1645
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quencyof thischangewasapproximately470 Hz (Dallos, 1984). The 500Hz choiceis simplya roundednumber.It maybe worth mentioningthat
the apparentshiftfrom velocitycontrolledto displacement
controlledresponsecan be due to a low-passfilter imposedeither by the viscoelastic
propertiesof cilia-tectoriumcoupling,or by the electricalpropertiesof
innerhair cell membrane.In eithercase,the approximately6-dB/oct rise
in IHC response,
in excess
of OHC response,
seenat thelowestfrequencies,
Dallos,P., andSantos-Sacchi,
J. (1983). "AC receptorpotentialsfrom hair
cellsin the low-frequencyregionof the guineapig cochlea,"in MechanismsoHearing,editedby W. R. Websterand L. M. Aitkin (Monash
U. P., Clayton, Australia), pp. 11-16.
Dallos, P., Schoeny,Z. G., Worthington,D. W., and Cheatham,M. A.
(1969). "Cochleardistortion:Effect of direct current polarization,"
Dallos, P., Billone, M. C., Durrant, J. D., Wang, C. Y., and Raynor, $.
3Incorporation
of theKros-Crawford
dataintoourearliermodel(Dallos,
1983)yieldspredictions
asto thechanges
in response
thatmaybeexpected
with polarizationof the basolateralmembrane.We find that, asthe membranepotentialisalteredfrom0 to -- 60 mV, thecomputedshapefactor/,
changes
overa 130-foldrange,andthecomputedfundamental
acresponse
canchangeasmuchas20 dB. Thesecomputations
do not takefrequencydependent
effectsintoaccountthat wouldreducetheeffectiveness
of polarizationwith increasing
frequency,asdemonstrated
in the Appendix.Our
datafor thefundamentalcomponent's
changewithcurrentandfrequency
can be accommodated
by a modestoverallchangein/ of only threeand
one-half-fold.A directcomparisonwith Kros andCrawford'sin vitrodata
isdifficultsincewedid not measurethe actualchangein membranepotential due to polarization.
4Similar conclusionscan be drawn from our data about other even-order
harmoniccomponents,
well exemplifiedby the currentdependence
of the
secondharmonicresponse,
5Thethirdpossibility,
voltage-dependent
alteration
ofciliarystiffness,
cannot be ignored.It is, however,not treatedherein detail.
6Itisreasonable
toassume
that,inthesediscussions,
Rbrepresents
theslope
resistance.
7Inoursimplified
model,andin all discussions,
wehaveassumed
thatcurrent-inducedeffectiveresistancechangesin the basolateralmembraneare
sufficientto accountfor the observedphenomena.Another possibilityis
that polarizationcanchangethekineticpropertiesofbasolateralchannels,
with largereffectslikely to occurat lowerfrequencies.
It is possible
that a
modelcouldbe constructedon this basiswhich would yield an equally
satisfactory
fit of theexperimental
resultsastheonedetailedin the Appendix.
8Afterthesubmission
of thismanuscript,
startingfromsomewhat
different
considerations,
the samevaluesfor E l and/ wereproposedby Mountain
(1989).
Corey,D. P., andHudspeth,A. J. (1979). "Ionicbasisof thereceptorpotential in a vertebratehair cell," Nature 281, 675-677.
Crawford,A. C., and Fettiplace,R. (1981). "Non-linearitiesin the responseof turtle hair cells,"J. Physiol. (London) 315, 317-338.
Crawford,A. C., andFettiplace,R. (198;)."Themechanical
properties
of
ciliarybundlesof turtle cochlearhair cells,"J. Physiol.(London), 364,
359-379.
edin innerhaircellresponses,"
in Mechanics
ofHearing,editedby D. T.
Kemp andJ.P. Wilson (Pergamon,London),pp. 197-204.
Dallos,P., Santos-Sacchi,
J.,andFlock,.. (1982)."'Intracellular
recordingsfrom cochlearouterhair cells,"Science218, 582-584.
Davis, H. (1965). "A model for transducer action in the cochlea," Cold
Flock,
.. (1965)."Transducing
mechanisms
inlateral
linecanal
organ
receptors,"Cold SpringHarbor $ymp. Quant. Biol. 30, 133-145.
Freeman, D. M., and Weiss, T. F. (1988). "The role of fluid intertia in
mechanical stimulation of hair cells," Hear. Res. 35, 201-208.
Goodman, D. A., Smith, R. L., and Chamberlain, $. C. (1982). "Intracellu-
lar andextracellularresponses
in the organof Corti of the gerbil,"Hear.
Res. 7, 161-179.
Hudspeth,
A. J.,andCorey,
D. P. (1977)."Sensitivity,
polarity,
andconductancechangein the response
of vertebratehair cellsto controlledmechanical stimuli," Proc. Natl. Acad. Sci. USA 74, 2407-2411.
Johnstone,
J. R., and Johnstone,B. M. (1966). "Origin of summatingpotential," J. Acoust. Soc. Am. 40, 1405-1413.
Kimura, R. S. (1966). "Hairs of the cochlearsensorycellsand their attachmentto the tectorialmembrane,"Acta Oto-Laryngol.61, 55-72.
Konishi,T., and Yasuno,Y. (1963). "Summatingpotentialof the cochlea
of the guineapig," J. Acoust.Soc.Am. 35, 1448-1452.
Kros, C. J., and Crawford, A. C. (1988). "Non-linear electricalproperties
of guinea-piginner hair cells:A patch-clampstudy," in BasicIssuesin
Hearing, editedby H. Duifhuis, J. W. Horst, and H. P. Wit (Academic,
London), pp. 27-31.
Kros, C. J., and Crawford, A. C. (1989). "Componentsof the membrane
currentin guinea-piginnerhair cells,"in MechanicsofHearing,editedby
D. T. Kemp and J.P. Wilson (Pergamon,London), pp. 189-195.
Laval16e,M., Schanne,O. F., and H6bert, N. C. (1969). GlassMicroelectrodes(Wiley, New York).
LePage,E. L. (1987). "Frequency-dependent
self-inducedbiasof the basilar membraneand its potentialfor controllingsensitivityand tuning in
the mammalian cochlea," J.Acoust.Soc. Am. 82, 139-154.
LePage,E. L. (1989). "Functionalrole of the olivo-cochlear
bundle:A motor unit control systemin the mammaliancochlea,"Hear. Res. 38, 177198.
mechanicalprocesses
in the cochlea,"in MechanicsofHearing,editedby
E. de Boer and M. A. Viergever(Delft U. P., Delft, The Netherlands),
pp. 119-126.
Mountain,D.C., Zagaeski,M., Cody,A. R., and Russell,I. J. (1989). "Effectsof thevoltage-dependentpropertiesof theIHC membraneonreceptor potentialdistortion," Abstractsof the 1989 Winter Meeting of the
Associationfor Researchin Otolaryngology,p. 171.
Nuttall, A. L. (1985). "Influenceof directcurrentondc receptorpotentials
from cochlearinnerhair cellsin the guineapig," J. Acoust.Soc.Am. 77,
165-175.
Nuttall, A. L., Brown, M. C., Masta, R. I., and Lawrence, M. (1981). "In-
nerhaircellresponses
to velocityofbasilarmembranemotionin theguinea pig," Brain Res.211, 171-174.
1646
1646
Redistribution subject to ASA license or copyright; see http://acousticalsociety.org/content/terms. Download to IP: 128.151.161.115 On: Fri, 11 Sep 2015 20:53:49
phonics
andactionpotentials
by KC1solutionandbydirectcurrents,"J.
1231.
Russell,I. J., and Sellick, P.M. (1978). "Intracellular studiesof hair cellsin
1647
Neurophysiol.15, 497-512.
Weiss,T. F., andLeong,R. (1985). "A modelfor signaltransmission
in an
earhavinghair cellswithfree-standing
stereocilia.
IV. Mechano-electric
transductionstage,"Hear. Res.20, 175-195.
Weiss,T. F., Mulroy, M. J., and Altmann, D. W. (1974). "Intracellular
responses
to acousticclicksin the innerear of the alligatorlizard," J.
Acoust. Soc. Am. 55, 606--619.
_
P. Dallosand M. A. Cheatham:Polarizationof,innerhaircells
1647
Redistribution subject to ASA license or copyright; see http://acousticalsociety.org/content/terms. Download to IP: 128.151.161.115 On: Fri, 11 Sep 2015 20:53:49