Inferred response polarities of cochlear hair cells* W. G. Sokolich,R. P. Hamernik, • J. J. Zwislocki,and R. A. Schmiedt Institutefor SensoryResearch,SyracuseUniversity,Syracuse,New York 13210 (Received30 July 1975;revised22 December 1975)

Single-fiber responses wererecordedfrom the auditorynervesof kanamycin-treated gerbilswhosecochleas weresubsequently processed for histologicalexamination.On the basisof their abnormalresponses to inferredtrapezoidaldisplacements of the basilarmembrane,the contactedfiberswereclassified accordingto the direction of basilar-membranedeflection that was associatedwith theft excitation. A frequency-distance

map was constructedfor the gerbil'scochleawith the help of cochlear-microphonic recordingsand was usedto infer the locationof the hair cells innervatedby the contactedfibers.Our correlationsindicatethat fibersinnervatingcochlearregionssubstantiallydepletedof outer hair cellswere abnormaland were scalavestibuliexcitatory.Furthermore,fibersinnervatingcochlearregionscontainingfull or nearly full complements of both inner and outer hair cellswere eitherabnormaland scala-tyrnpani excitatory,or were normal.Theseresponse polaritiesare consistentwith the previouslyproposedpolarity-opposition modelof interaction

between inner and outer hair cells in the cochlea.

Subject Classification: [43] 65.28, [43] 65.35,[43] 65.40,[4'3]65.42,[43]65.59.

INTRODUCTION

This article is part of a series describing our research on the problem of interaction between the inner and outer

hair

cells.

The

research

was

initiated

as a

result of growing circumstantial evidence that the two cell populations interact. Perhaps the most important

pieces of evidence are (1) the discovery by Spoendlin (1966, 1970) that about 95% of all afferent auditorynerve

axons stem

from

cell bodies

whose

dendrites

are

the radial fibers termir/ating solely on inner hair cells,

and (2) the finding of Kiang, Moxon, and Levine (1970) that single-fiber tuning curves are broadened when the outer hair cells are destroyed by kanamycin. In light

of Spoendlin'sdiscovery, practically all primary-fiber activity recorded from the auditory nerve must arise in the radial fibers. Accordingly, the changes in the tuning curves of primary fibers associated with cochlear regions void of outer hair cells suggest that outer hair cells play a role in determining the activity of these

fibers.

After Dallos et al. (1972) had concluded on the basis of their cochlear-microphonic experiments that outer hair cells respond to basilar-membrane displacement and that inner hair cells respond to its velocity, there appeared to be a way of demonstrating the suspected interaction between the two hair-cell populations more directly. The demonstration would be provided if both displacement and velocity responses were shown to occur in the temporal firing pattern of the same auditorynerve fiber. In order to separate the two responses, a low-frequency trapezoidal time pattern of basilarmembrane displacement was used. Early recordings (Sokolich and Smith, 1973; Zwislocki and Sokolich,

1973; Zwislocki, 1974a)revealed the presence of distinct displacementand velocity responsesin the same fibers The recordings were viewed as a demonstration of interaction between inner and outer hair cells, under the

assumption that the conclusion of Dallos et al. (1972) was correct. In spite of the demonstration they seemingly provided, the early recordings contained a rather baffling feature. Single-fiber excitation occurred during both motion and sustained displacement of the bas963

J. Acoust.Soc.Am., Vol. 59, No. 4, April 1976

ilar membrane toward scala tympani, a direction which is believed to correspond to the bending of hair-cell stereocilia away from the basal body. This outcome seems to contradict the body of evidence linking the excitation of hair cells and of corresponding nerve fibers with the bending of stereocilia toward the basal

body (Flock, 1971). Nonetheless, this outcomewas in agreement with a report by Konishi and Nielsen (1973) that static displacement of the basilar membrane toward scala tympani resulted in the excitation of most auditory-nerve fibers which they contacted.

Later, more extensive recordings (Sokolich and Zwislocki, 1974a; Zwislocki and Sokolich, 1974; Zwislocki, 1974b) revealed that the polarity of both the velocity and displacement responses (i.e., whether they were excitatory or inhibitory) changed in a systematic way with CF.

The systematic dependence of

the polarity of the responses on CF (e.g., Fig. 4) implied that both inner and outer hair cells change their response polarity from one region of the cochlea to anotherø In view of the morphological homogeneity within each hair-cell population, such a change appeared unlikely. Accordingly, the explanation of the responses in terms of a simple superposition of displacement and velocity signals was abandoned and a polarity-opposition hypothesis (Zwislocki, 1974b) was proposed. The latter hypothesis maintained that the responses resulted from the summation of two displacement signals of opposite polarity that did not cancel one another completely. In fact, it was possible to reconstruct each of the response patterns by subtracting from each other two hypothetical displacement signals whose relative amplitudes and time registration varied slightly with CF. The polarity-opposition model was further elaborated upon by assuming that, at the level of the radial fibers, the inner hair cells produce an excitatory signal and the outer hair cells produce an inhibitory one during basilar-membrane displacement toward scala vestibuli. Both signal polarities reverse during displacement in the opposite direction. The latter assumption was made in view of the morphological polarization of the hair cells Copyright¸ 1976 by the Aco•cal

Societyof America

963

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964

Sokolich eta/.' Response polarities of cochlear haircells

(Flock, 1971)a•ndthe fact that radial fibers enddirectly

responsepolaritiesof fiberscontacted inthekanamycin-

upon inner hair cells.

treated gerbils showeda strong.correlation with CFo

In this article we provide experimental evidence consistent with one of the two principal assumptionsof the

vestibuli excitatory, whereas most fibers having rela.lively low CF's were scala-tympaniexcitatory. Statis-

polarity-opposition model,namely,the assumption that signals from inner and outer hair cells interact and are oppositein polarity. The experimentsperformed are not suitable for testing the remaining

principalassumption that, in a normalear, the sensitivities of the inner and outer hair cells are nearly

equal. Accordingto the model, auditory-nervefibers innervatingportionsof a cochleain whichonlyinner hair cells are preserved shouldshowexcitationduring

the displacement of thebasilar membranetowardscala vestibuli.

Fibers receiving a weakened input from

inner hair cells should show excitation during its dis-

placementtowardscalatympani. All thesefibers should be inhibited during the nonexcitatory half-cycle.

Accordingly,trapezoidaldisplacementsof the basilar membrane should result in a response pattern that is

simpleby comparison with thoseproducedin fibers controlledby normally functioninginner and outer hair cells.

In an attemptto eliminate, or at least weaken,the presumedsignalfrom outerhair cells, we tookadvantage of the knownreproducibleeffect of kanamycin sulfate of producinga hair-cell lesionin the cochlear base, whichaffectsouterhair cells overa greaterdislance than it affects inner hair cells.

In addition, if

functionalchangesprecede gross anatomicalchanges, the data of Engstr/Jmand Kohonen(1965)suggestthat

the presumedinfluenceof apicalinner hair cells on single-fiberresponses maybe weakened by kanamycin. Preliminary results of our experimentson kanamycintreated gerbils were presentedin previouspublications (Sokolichand Zwislocki, 1974a;ZwislockiandSokolich, 1974; Zwislocki,1974b). In thesegerbils,trapezoidal displacement of thebasilar membraneproducedeither simpleunipolarresponses or complex responses typical of untreated gerbils. Of the former, some were scalavestibuli excitatory, some were scala-tympani excitatory, and many of each type followed the trapezoidal time pattern of basilar-membrane displacementø However, the predictions of the model were not completely satisfied, since many of the abnormal unipolar responses of both types followed basilar-membrane velocity instead. This outcome may have two inter-

pretations. Oneis that the modelis at least part,ially invalid. The other is that kanamycin may have affected the mode of hair-cell excitation. Although it is not within the bounds of this article to specify whether cochlear hair cells follow the velocity or the displacement of the basilar membrane, it should be noted that recent histological observations by Spoendlin(1975) indicate a collapse of stereocilia as one of the early changes in the remaining inner hair cells of kanamycinpoisoned cochleas. It is quite possible that such a collapse could make a hair cell less sensitive to the displacement of the basilar membrane and more sensitive to its velocity.

All fibers havingrelatively high CF's were scalatical distributions

derived from these data and relating

responsepolarities of fibers to their CF's were remarkably similar to distributions derived from the anatomicaldata of Engstr/Jmand Kohonen(1965) relating populationdensitiesof inner and outer hair cells to cochlear location in guinea pigs treated with ototoxic antibiotics. This similarity was initially pre-

sented (Sokolichand Zwislocki, 19•4b) as indirect evidence that fibers excited during deflection of the basilar

membrane

toward scala vestibuli

were con-

trolled predominantlyby the inputsfrom the inner hair cells, andthat fibers excitedduringdeflectionin the oppositedirectionwere controlledpredominantly by the inputsfrom the outerhair cells. To obtainmore direct evidencefor this interpretation,the cochleasof the treated gerbils usedin thephysiologicalexperiments were preparedfor subsequent histologicalexamination. A frequency-distance map was constructedfor the gerbil's cochlea,whichhasenabledus to relate our histological findingsdirectly to our single-fiber recordings. This article presents the correlations that have resulted.

The study described here consistedof three parts'

(1) recordingsingle-fiber responseswithinthe auditory nerve, (2) histologicaldeterminationof hair-cell loss from surfacepreparations, and (3) constructionof the gerbil's cochlearmap from microphonicanddistance measurementsalong the organ of Corti. ' This breakdownreflects primarily the order in which the researchprogressedrather thanthat of its presentation. I.

METHODS

Mongoliangerbils (Merionesunguiculatus) servedas experimentalanimals in all of the experiments. Only those animals destined for single-unit recording and subsequent histological examination were treated with kanamycin. Data for the cochlear map were obtained later

from

the cochleas

of untreated

animals.

The kanamycin treatment consisted of subcutaneous

injections of kanamycinsulfate (Kantrim) at dosage

levels of either 300, 400, or 500 mg/kg. Ninegerbils received a daily treatment for 11 consecutive days. Following an interim period of about 3 months, five of the original gerbils received a daily treatment for 9 additional consecutive days.

The variations in dosage

level and period were intended to produce various amounts of hair-cell damage without attempting to study systematically the gerbil's susceptibility to the drug. None of the treated gerbils served as experimental animals within 2 months of either treatment period, but all did so within

6 months

of the final

one.

In preparation for surgery, the selected gerbil was anesthetized with an intraperitoneal injection of sodium

pentobarbital(Nembutal,35 mg/kg). It was subseA preliminary analysis of our data revealed that the

quently shaved around the head and neck and tracheoto-

J. Acoust. Soc. Am., Vol. 69, No. 4, April 1976

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965

Sokolicheta/.: Response polaritiesof cochlearhair cells

mized. During the experiment, supplementary anesthetic was administered when necessary. In addition, the

gerbil's rectal temperature was maintainedat approximately 37 øC with a dc-powered electric heating pad. During the collection of all electrophysiological data, the animal

was enclosed

vibration-insulated

in a double-walled

sound-

and

965

Single-fiber responses were processed on line and displayed in the form of two-cycle histograms. The histograms were generated by a special-purpose com-

puter (Fabritek). • The responsesand other associated signals were recorded in analog form on magnetic tape for off-line processing and documentation.

booth.

The same acoustic system was used in all auditorynerve and cochlear-microphonic experiments. Its I ß stainless-steel body housed two •-tn. condenser micro-

All single-fiber responses presented here resulted from an inferred low-frequency trapezoidal time pattern of basilar-membrane displacement. The trapezoidal wave was produced by applying a 40-Hz triangle with

phones (Brflel & Kjser, model 4134), one serving as the

rounded

sound source and the other as a monitor.

trical triangle was bandlimited to about 1000 Hz and integrated with a time constant of about 4 msec. It produced a similar pattern of sound pressure in the ear canal (Fig. 3, upper trace) as a result of the approximately flat low-frequency transfer characteristic of the acoustic system. A trapezoidal time pattern of basilar-membrane displacement is produced at the cochlear base by the smoothed triangular soundpressure waveform because of the time derivative relating them. This theoretically derived relationship

The entire

assembly formed an integral part of the headholder

and, whenin position,coupled eachtransducerthrough isolated pathways to the air space within the external meatus. A spongy cushionsealed the system's slightly protruding concentric tubes at their interface within the opening of the osseous meatus.

The seal was verified

by comparing a 40-Hz triangular signal applied to the source transducer with the sound-pressure waveform it produced. The acoustic system was calibrated against a wide-band high-impedance probe inserted into the ear canal through the bony tympanic annulus and placed within

2 mm of the umbo.

A. Animal preparation andsingle-fiber recording Accessto the gerbil's auditory nerve was gained ventrolaterally

according to a procedure introduced

corners

to the source

transducer.

This

elec-

(Zwislocki, 1965, 1974a)was shownto be approximately valid in both the guinea pig and the rat (Dallos, 1970) and, more recently, in the gerbil (Schmiedt and Smith, 1974). Because of the low-frequency content

and small wave reflection at the gerbil's helicotrema, the trapezoidal pattern is reasonably well preserved throughout the cochlea.

previously (Sokolichand Smith, 1973). The surgery is rapid, produces only superficial bleeding, and is less extensive than that required for other current auditory-

B. Histological preparation and light microscopic

nerve preparations. Briefly, the right pinna is incised along its perimeter, is separated from underlying connective tissue, muscles, and glands, and is removed. Following their exposure, the lateral translucent walls

Immediately following each anditory-nerve experiment, the gerbil was decapitated and within a minute both bullas were removed, openedwidely, and placed

of the inferior mastoid cavity and of the posterior portion of the tympanic chamber are chipped away. Finally, an openingis made through the transparent dorso-

with buffers and salts (Pease, 1964). Both scala tympani and scala vestibuli of the right cochlea were opened for perfusion. The fixative was introduced into

roedial

the basal scala-tympani inlet under gentle mouthpressure for about 5 min. It flowed freely through the scala and out the apical scala-vestibuli perforation. The

wall

of the round-window

antrum

into the internal

meatus.

Glass microelectrodes were used for all single-fiber recordings. They were fabricated according to the method of Tasaki et al. (1968) and were filled with 3M NaC1. Only those with tip resistances between 30 and 70 Mf• were used. An electrode, mounted at the end of a hydraulic drive (Kopf Instruments), was aimed at the opening into the internal meatus along a line connecting the opening and the lateralmost extent of the basioccipital paramastoid process. The electrode was subsequently advanced from outside the recording booth. Units

contacted

within

the internal

examination

in a dish containingZeiterqvist's formulationof OsO4

stapes was then removed and the fixative introduced

through the oval window openingand into scala vestibuli for a few more minutes.

The left cochlea was likewise

vented and perfused, and both were refrigerated in the osmium bath for two hours.

The cochleas were then

washedin Tyrodes, dehydratedto 70% ethyl alcohol, and subsequently dissected.

The entire basilar mem-

brane with the organ of Corti, the spiral ligament, and the stria vascularis was removed piecewise and mounted in glycerin for light-microscopic examination.

meatus were identi-

fied as primary fibers according to three criteria: (1) their recorded waveforms were positive andmonophasic (Kiang et al., 1965); (2)the latencies of their responses to a rarefaction click were comparable to those reported for other standard auditory-nerve preparations

(Kiang et al., 1965; Evans, 1972); and (3) they were contactedwithin approximately 500 /•m of penetration. The latter correlates well with the depth of fiber tissue traversed by the electrode (Fig. 3, Chamberlain,

The percentages of missing inner and outer hair cells

were determined as a function of distance along the cochlear

duct.

The latter

apical termination,

was measured

relative

to its

with a cumulative error of less

than 0.1 min. A hair cell was countedas present when

the cuticular plate-reticular-lamina complexappeared intact and the individual hair-cell body was present. Hair cells countedas present could not, however, be evaluated

as to their

functional

status.

A hair cell

was counted as missing when the cell body was not J. Acoust.Soc.Am., Vol. 59, No. 4, April 1976 Redistribution subject to ASA license or copyright; see http://acousticalsociety.org/content/terms. Download to IP: 130.88.90.140 On: Thu, 18 Dec 2014 18:02:29

966

Sokolicheta/.: Responsepolaritiesof cochlearhair cells

present.

When an animal is allowed to survive sever-

966

through chlorided silver wires to unit-gain followers

(Picometric) having capacitance compensation and in-

al weeks after trauma, as was done in our experiments, the location of the missing hair cell is marked by very

put impedanceson the order of 10•a •.

characteristicfeatures [see Fig. 6(b)]. The upper

signals appearing at the outputs of the followers were

platelike expansion of the phalangeal processes of the

voltage amplified by a factor of 1000 and brought out-

Deiter

side the booth, where the difference signals were derived. The magnitudes of both microphonic and acoustic-monitor signals were read directly from the calibrated voltmeter of a General Radio wave analyzer

cells

unite

to form

a characteristic

"x-like"

cell complex at the location of the missing hair cell. These "scarlike" elements were counted and percentages were computed to yield a cochleogram. Both right and left cochleas of nine kanamycin-treated gerbils were examined. In order to obtain a reference, six cochleas of untreated animals were also examined.

C. Cochlear-microphonic recording In order to make the bony capsule of the cochlea accessible for the differential recording of cochlear microphonics, the bulla had to be exposedventromedially. The additional surgery continued following com-

pletion of the previously described ventrolaterai exposure of the bulla for auditory-nerve access. After the pinna has beenremoved, the neck is incised laterally and ventrally, and the skin and superficial fascia are separated to expose the underlying glands. The entire ipsilateral glandular complex is tied off anteriorly and posteriorly and removed. The muscle overlying the ventromedial wall of the bul-la is removed and the tympanic and mastold chambers are opened widely. The additional surgery produces only superficial bleeding and does not elevate the click threshold

of the round-window Nx response.

Numerous anomalies in the gerbil's anatomy restrict the locations and scalae that are practically accessible for recording intracochlear potentials. The recording sites were therefore confined to four locations. Differential recordings between scala media and scala tympani were obtained at all but the most apical site, There, cochlear microphonics were measured with a single electrode in scala media. All microphonic potentials were recorded from the scalae with glass pipettes having tip diameters of about 5 •m. The pipettes were tapered on averttcal electrode puller (Narashigi, model PE2) and were broken under microscopic observation to the appropriate diameter. Scala-media electrodes were filled with 0.15M KC1; scala-tympani electrodes with 0.15M NaC1. All had tip resistances between 8 and 12 M•.

The electrodes were placed into the scalae through

The low-level

(model 1900A). The latter was set at a bandwidth of 3 Hz. The dc output of the scala-media electrode was continuously monitored. During electrode placement, it provided positional feedback, whereas during the experiment it served to indicate the state of the cochlea. Endolymphatic potentials between 70 and 90 mV were obtained. They remained within about 5 mV of their initial values during the course of the experiment. The cochlear-microphonic recording system was calibrated prior to the electrophysiological experiments, using a sample of five representative glass electrodes. Interelectrode variability amounted to 3 dB at 15 kHz, and the mean magnitude response was flat within

+ 2 dB from

0.2

Hz to 15 kHz.

D. Distance measurementsalong the organ of Corti Following each cochlear-microphonic experiment,

the right bulla was removed from the gerbil's skull and placed in an open dish to dry. A few days later, most of the brittle cochlear shell was ground away using a motor-driven dental drill. Only those portions adjacent to the spiral ligament and those near the electrode openings remained, the medial wall of the temporal bone serving as their support. The locations of the electrode holes were initially specified in terms of their distances along the estimated

center

of the basilar

membrane.

Distances

along the basal coil were specified relative to the basal termination of the basilar membrane; those along the upper coils were specified relative to its apical

termination. To be compatiblewith the histological measurements, all four recording sites were eventual-

ly specified in terms of their distances along the tunnel of Corti relative to its estimated apical termination. All dimensional

measurements

on the dissected

cochleas

were made visually to the nearest 40 •m by means of a dissecting microscope equippedwith a calibrated reticle.

Distances to the recording sites within the basal halfturn were measured directly. Thin pliable wires were

small (100 •m) holes in the thin cochlear shell. Each

formed to fit the curvature

opening was bored mid-scala with a motor-driven dental burr having a conical tip. Drilling commenced with

along its scala-tympani side from its basal termination to each of the sites. The wires were subsequently straightened and their lengths measured using the calibrated microscope.

the application of gentle pressure, proceededwith a slow rate of rotation, and was terminated as soon as the membranous labyrinth became Visible. Care was taken against further advancement of the drill so as to avoid injury to either the spiral ligament or the stria vascularis.

All intrascalae potentials were measured with respect to an Ag-AgCi ground wire inserted into the neck muscles. The outputsof the pipettes were coupled

of the basilar

membrane

Distances to recording sites within the upper turns were calculated from the equation /• site

d=[

J • a•x

r(O) dO,

(1)

where 8 is the angle aboutthe modiolar axis of the upper coils, and r(O) is the radius of curvature of the

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967

Sokolicheta/.' Responsepolaritiesof cochlearhair cells

i

i

_

?

I

-

bJ

shown in Fig. 1. The filled symbols are associated with microphonics recorded differentially between scalae media and tympani, the untilled circles with microphonics recorded between scala media and a ground electrode in the neck muscles. The approximate location of each recording site is shown along the

i

9

967

cochlear spiral (upper left, Fig. 1) by the symbol as-

II

s ociated with the data obtained there.

Each data point

indicates the mean sound-pressure level at the eardrum required to produce a constant microphonic potential of 10 •V rms.

For comparison, the curves of Fig. i have been shifted along the ordinate axis to coincide approximately with that corresponding to the basalmost recording site. The latter curve should reflect predominantly the transfer function of the middle ear up to at least 20 kHz

• 60o •

_

>

0.8

80

MM

(Schmiedt and Smith, 1974). Relative to it, the others .02

FIG.

1.

. 5 .I .2 .5 I SOUND FREQUENCY

2 IN

I

20

KHZ

SPL at the eardrum for a constant CM ampltiude of

10 #V rms at several

electrode

locations.

Filled

circles:

11.6 mm from apex, three gerbils (mean data), SM-ST; filled triangles: 9.2 ram, three gerbils (mean data), SM-ST; filled squares: 4.4 mm, two gerbils (mean data), SM-ST; unfil[ed circles: 0.8 mrn, one gerbil, SM re neck; untilled triangles: 9.2 mm, one gerbil (typical data), SM-ST.

exhibit relative maxima followed by rather steep highfrequency cutoffs. It is striking that the maximum at 9 kHz is much less pronounced than those at 500 Hz and 2 kHz. The apparent depression of the 9-kHz maximum may be due in part to an integration of out-of-

phase microphonic contributions. The latter may also serve to explain the relative minima at 1.5 and 8 kHz.

curvature is greater than about three times the distance between the adjacent turns of a three-dimensional

The maxima of the curves in Fig. 1 are expected to be closely associated with the vibration maxima of the basilar membrane, as may be inferred from a comparison between microphonic and mechanical tuning characteristics measured in guinea pigs (Dallos, Cheatham, and Ferraro, 1974; Wilson and Johnstone, 1975). Accordingly, we have used the cochlearmicrophonic data to infer the frequencies and corre-

spiral.

spondinglocationsof vibration maximain the gerbil's

basilar membrane as a function of the angle.

Equation

(1) is exact only for a spiral in a plane but gives a satisfactory approximation (within 5%) if the radius of

The latter condition is satisfied in the gerbil's

cochlea everywhere except in its extreme half-turns.

The function r(e) was estimated as follows. Two mutually perpendicular reference planes were established, their intersection coinciding with the estimated modiolar axis of the upper turns. The plane nearest

which

both extremes

of the basilar

membrane

terminate is approximately parallel to the medial wall

of the tympanic bulla (upper left, Fig. 1). The perpendicular distance between the modiolar axis and each intersection

of the basilar-membrane

center

with

the

planes was estimated by using the calibrated micro-

scope and was taken as a point on r(•;). The latter function was constructed piecewise linearly and was graphically integrated to obtain the desired distances. The mean length of the tunnel of Corti was estimated from dissected cochleas as well as from surface preparations. A sample of five dissected dried cochleas yielded a mean length of 12.2 mm; a sample of 15 surface preparations yielded one of 12.1 min. Their close agreement demonstrates the compatibility of both methods in specifying distance along the cochlear partition.

II.

RESULTS

A. Cochlear map of Meriones unguiculatus Microphonic data representative of those used in

estimatingpoints on the gerbil's cochlear map are

cochlea. Microphonic data obtained from cochleas of both gerbils and guinea pigs indicate that the best frequency of a particular location is equally well specified

by recordings between scala vestibuli andscala tympani, between scala media and scala tympani, or from scala

media alone (Schmiedt, unpublisheddata).

Points on the gerbil's cochlear map (Fig. 2) were determined from cochlear-microphonic data obtained from three cochleas. The variability among the data from these and other cochleas was sufficiently small so that averaging over a larger population was considered unnecessary. The cochlear microphonics were recorded differentially between scala media and scala

tympani in the first and second turn of two gerbils and between a neck electrode and scala media in the apical turn of the third. Recording-site locations along each

organ of Corti, were determined (see Sec. I) and referredtoa meanlength of 12.1 mm. Theunfilled circles in Fig. 2 indicate the mean frequency and distance coordinates

inferred

from

the two differential-electrode

sites; the unfilled triangle shows the coordinate inferred from the single apical site. In many mammalian species the frequency dependence of the location

of the vibration

maximum

in the coch-

lea is knownto be essentially logarithmic (yonB•k•sy, 1944). Accordingly, such an approximate dependence has been assumed for the gerbil, and the two midcoch-

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968

Sokolicheta/.' Responsepolaritiesof cochlearhair cells

968

25

MSEC

I

I

12

x

8

•

6

LU 4

/

CM'T2

i i i . ,•1i iiiI

.2

SOUND

i i i 5I I i iiiI0

FREQUENCY

IN

location

of vibration

•. ,l,SV

:

.:

'k, X,,.,,•

\

...

tST

.

20 KHZ

FIG. 2. Frequency-distance map of gerbil's cochlea which shows inferred

/

•'

(SMST)/ ß

i i i50i

2

•'

.:

maximum

as a function

of

soundfrequency. Unfi[led circles refer to differential CM

FIG. 3. Upper record shows •he •0-•s •an•u•a• •me pa•e•n of sound p•essu•e in •he ea• canM. •idd•e •eco•d shows •esu•n• •me pa•e•n oE po•en• •eco•ded nea• •ound w•ndow. •owe• •eco•d shows •he •esu•Hn• •me pa•e•a of coch[ea•

m•c•ophon•cs•eco•ded dfffe•en•aH• (S•-S•)

•n •he second

(SM-ST) and distance measurements (mean data, three cochlea).

Untilled triangle refers to CM (SM re neck) and distance mea-

bull, and scMa •mpani,

•espec•e•.

surements.from one cochlea. Vertical lines intersecting solid curve indicate highest and lowest CF's of auditory-nerve or cochlear

nucleus

units.

lear coordinates (unfilled circles) in Fig. 2 have been joined by a straight-line segment. Beyond this segment, the curve has been extrapolated by curvilinear segments to include the apical coordinate and to take

The lower record shows the potential obtained from the secondturn with glass electrodes in scalae media and tympani. The time patterns of both microphonic recordings are approximately trapezoidal, demonstrat-

25

account of the highest and lowest CF's of units encountered in the gerbil's auditory nerve (Sokolich, unpublished data) and cochlear nucleus (Schmiedt, unpublished data). The curve of Fig. 2 represents our best estimate of the relationship between sound frequency and the location of the vibration maximum in the gerbil cochlea.

.'.... .':;': .-.

ß ...• ..

ßß

U.23-19

.'.•

CF=I.8 KHZ

...::o.. ,.; ß.' ;.. ':/,',::":':

.•

.. ß

'.•::•; ß '•'•.,,.•,::•.':*_..; ß ßß ß "i•'

B. Single-fiber responses

' '-::"' '

ß

.

,.%

',,.

.,:

.•

'Z,.'

&...

.

,..?-.:,, ß ß .! .•,•,..' ßi ß .'.•,•..: '

U.23-17 CF =4.9 KHZ

All single-fiber responses presented here resulted from the application of the 40-Hz triangular time pattern

3.

i

ß' 'v. , "'::.'.-:'

of soundpressure at the eardrum (see Sec. I). The pressure pattern is shownin the upper record of Fig.

MSEC

I

..

,½,

ß

. •

.-...

.•

.

•'-.

....

:":':"' ""':*:'•. ' ßß "' •.(.,':.:,'.,:.-;'):'...5...',• .,., ;.':•-_:,-.':2; ::':;:.•.:.'.',;•'%,.:.,',.'.;':'.;;:*. ,.... '.':.'-5' :n.:q::. ß:z,".:.:;..•.,::',;' .:'.....

On theoretical grounds, it is expected to cause a

traveling wave of trapezoidal displacement along the

cochlear partition (Zwislocki, 1974a). In lieu of direct displacement measurements, we recorded cochlear microphonics to confirm the theoretical expectation. There is ample evidence that cochlear microphonics follow low-frequency time patterns ofbasilar-membrane

displacement (B•k•sy, 1951; Dallos, 1970; Wilson and Johnstone, 1975). Mircophonic potentials resulting from the application of the triangular pressure pattern are shown in the lower two records of Fig. 3.

They

were recorded simultaneously from the cochlea 'of an untreated gerbil. The middle record shows the potential measured with a silver wire electrode placed on the bony dorsal ridge of the round-window antrum.

FIG. 4. Single-fiber responses producedby trapezoidal wave pattern: untreated gerbils. Upper record shows averaged round-window microphonic with suppressed whole-nerve respouses and basilar-membrane deflections toward scala vestibull (SV) and scala tympani (ST). Middle records are PST

histograms (0.1-msec bins; 2000 sweeps)illustrating the three typical response patterns associated with low, medium, and high CF fibers in untreated gerbils (adaptedfrom Zwislocki and Sokolich, 1974). SPL= 85 dB.

J. Acoust. Soc. Am., Vol. 59, No. 4, April 1976

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969

Sokolicheta/.' Response polaritiesof cochlearhair cells

ing that the displacement of the basilar membrane at the cochlear base is, to a good approximation, pro-

portional to the time derivative of the sound-pressure

waveformat the eardrum, andthat the trapezoidal wave is propagatednearly nondispersivelyalong the cochlear partition. The fluctuationsassociatedwith the ascendingand descendingportions of the roundwindowpotential disappearrapidly during anoxia and after death, and are absent in microphonicsrecorded differentially between scalae media and tympani. Accordingly, they appear to be contaminations of the round-window microphonic potential by whole-nerve

969

tympani and a decreased rate during the sustained displacement in the opposite directionø The relative amounts by which their firing rates are increased diminishes with increasing CF. Accordingly, fibers whose CF's

are above about 6 kHz show a decreased

firing rate during sustained basilar-membrane

dis-

placement in both directions. Transient velocity-like responses are also present in the response patterns shown in Fig. 4. The firing rates of low-CF fibers are increased during motion of the basilar membrane toward scala vestibuli, and are decreased during its motion in the opposite direction. In fibers with medium

action potentials.

CF's, the polarity of each of these responses is reversed. Finally, fibers with high CF's show an in-

For the purpose of subsequent comparison, response patterns produced by three fibers of one untreated gerbil are shown in Fig. 4. The patterns shown are representative of those producedby 86 fibers studied during the course of 12 experiments employing untreated gerbils. The top record shows the roundwindow microphonic potential obtained during anoxia at the end of the experiment and reflects the trapezoidal time pattern of basilar-membrane displacement. The

creased firing rate during both directions of basilarmembrane motion. The temporal structure of the patterns shown in Fig. 4 appeared to be invariant with stimulus level below the upper limit of our acoustic system at low frequencies, which was about 90 dB

three middle records show the single-fiber

in the form of two-cycle histograms.

responses

The first of these

is typical of fibers whose CFs are below about 2 kHz; the second, of fibers whoseCF's are betweenabout 2

and6 kHz; andthe third, of fibers whoseCF's are above about 6 kHz.

The bottom record

indicates

the

level of spontaneousactivity of the fiber with the 6.1kHz CF. Perhaps the most noteworthy aspect of the response patterns is the systematic dependence of their temporal structure on CF range. Fibers of low and medium CF's show an increased firing rate during sustained basilar-membrane displacement toward scala

25

Response patterns representative of those produced by 85 fibers contacted in seven kanamycin-treated

gerbils are shownin Figs. 5(a) and 5(b). As in Fig. 4, the microphonic potential obtained during anoxia at the end of an experiment on an untreated gerbil appears as the top record in each part of Fig. 5 and serves to infer a trapezoidal time pattern of basilar-membrane displacement. Also, as in Fig. 4, single-fiber response patterns are presented below the microphonic record in the form of two-cycle

histograms.

Response

patterns produced by four different fibers are shown in Fig. 5(a), whereas those producedby the same fiber at four different sound-intensity levels are shown in Fig.

5(b). Note that all of the patterns shown in Fig. 5 are

MSEC

I

CM: RW .;/"

SPL.

I

\\

./

FIBER K3-1 CF= 7.0 KHZ

SPA. •85/SEC CF TH = 54 dB SPL

FIG. 5. Single-fiber responses produced bytrapezoidal wavepattern:kanamycin-treated gerbils. (a)Upperrecordsameasin Fig, 4, Lower records are PST histograms (0, 1-msec bins) showingthe abnormal unipolar responses of four fibers.

Fiber K2-13

is ST and follows basilar-membrane motion, Fiber K8-1 is also ST but follows basilar-membrane displacement. Fibers K4-1 and K2-11 are both SV and likewise illustrate motion sensitivity and displacement sensitivity. (b) Intensity series for SV fiber K3-1, illustrating intensity dependent response: displacement response at lower intensities, both displacement and velocity responses at higher intensities.

J. Acoust.Soc. Am., Vol. 59, No. 4, April 1976 Redistribution subject to ASA license or copyright; see http://acousticalsociety.org/content/terms. Download to IP: 130.88.90.140 On: Thu, 18 Dec 2014 18:02:29

970

Sokolich et al.' Responsepolarities of cochlear hair cells

simple by comparison with the normal patterns shown in Fig. 4. Fiber K2-13 shows an increased firing rate during basilar-membrane motion toward scala tympani and a decreased rate during motion in the opposite direction. Fiber K8-1 has the same response polarity

970

(N). All fibers contacted in two of our nine kanamycintreated gerbils produced normal response patterns, and subsequent histological examination of their cochleas revealed that only a small basal lesion was

as fiber K2-13, but the time structure of its response

present in each. Accordingly, all fibers contacted in these two gerbils were associated with full comple-

follows predominantly the displacement of the basilar

ments

membrane

rather

than its motion.

In contrast

fibers K2-13 and K8-1, both fibers K4-1 and K2-11 have the opposite response polarity. Whereas fiber K4-1

follows

basilar-membrane

motion

and fiber

K2-11

follows its displacement, both fibers show an increased firing rate during the deflection of the basilar membrane toward scala vestibuli. The responses of some fibers, however, followed basilar-membrane displacement at lower levels of sound intensity, and followed to some extent both displacement and motion at higher levels. As an example of this behavior, the responses produced by fiber K3-1 at four levels of sound intensity are

shownin Fig. 5(b). Two features of the responsesof fiber K3-1 may be particularly worthy of note. First, at higher-intensity levels, excitatory responses are associated with both motion and displacement of the basilar

membrane

toward

scala

vestibuli.

of hair

cells.

with

Such an uni-

polar response of this polarity is distinctly abnormal, and was never produced by fibers contacted in untreated gerbils. Second, both excitatory and inhibitory responses are present. This observation follows from a direct comparison between the bottom histogram and each of those above it (Fig. 5). The firing rate shown in the bottom histogram is due almost entirely to spontaneous activity. Since the CF threshold of this fiber was elevated by about 50 dB, it is quite unlikely that its spontaneous activity was acoustically generated.

It should

be mentioned

that the CF thresholds

of ab-

normalST andSVfiberswereelevated by upto 30 dB and 70 dB, respectivelyø

Additionally,

all SV fibers

having medium and high CF's were associated with broadened tuning curves. Fibers contacted in our kanamycin-treated gerbils and classified as N were all associated with normal CF thresholds and tuning curves.

C. Histological findings' Correlation with fiber response polarity An example of hair-cell lesions produced in our gerbils' cochleas by kanamycin is illustrated in Fig. 6, which shows micrographs of comparable regions in the basal turn of an untreated control (upper) and of a kanamycin-treated gerbil (lower). Although the inner hair cells are present in both micrographs, the outer hair cells are completely absent in the lower one. The lesion of outer hair cells illustrated

in Fig. 6 is typical

of those produced in our treated gerbils.

The extent of

OHC

Of the 23 fibers that showed an increased firing rate

during basilar-membrane motionand/or displacement toward scala vestibuli, 50%were classified as velocity responders, 30% as displacement responders, and 20% as velocity-displacement responders. Of the 49 fibers that showed an increased firing rate during basilar-

membrane motion and/or displacementtoward scala tympani, the correspondingpercentagesare 74%, 6%,

IHC

and 20%.

The unipolar responses produced by the abnormally responding fibers of our kanamycin-treated gerbils can be classified either according to their response polarity

(scala-vestibuli excitatory or scala-tympani excitatory) or according to their response mode (displacement, velocity, or displacement-velocity). However, we found a strong correlation of cochlear damage with response polarity, but not with response mode. We have therefore classified these fibers accordingly. Fibers that showed an increased firing rate during

basilar-membrane displacementand/or motiontoward scala

vestibuli

were

classified

scala-vestibuli

tory (SV), whereas those that showedan increased firing rate during basilar-membrane displacementand/or motion toward scala tympani were classified scala-

tympani excitatory (ST). Some fibers in some kanamycin-treated gerbils produced normal response patterns, had CF threshold in the normal range, and had sharp tuning curves.

These fibers were classified

IHC

excita-

as normal

FIG. 6. Micrographs of organ of Corti (surface preparation) from an untreated control (a) and a kanamycin-treated gerbil (b). Inner hair cells are present in both micrographs but outer hair cells are completely absent in the lower one. Both micrographs are from comparable locations approximately 8 mm from apex.

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971

Sokolicheta/.' Response polaritiesof cochlearhair cells

BEST 0.4 i

FREQUENCY

I i

i

2

i

i

vSV ß ST

4

!

i

i

IN 6

!

I

KHZ

I0 I

!

i

971

i

i

ß IHC o OHC

BEST

20

0.4

40

i

!

i

i

GERBIL K4- R

FREQUENCY

I I

i

2

i

i

4

i

i

i

IN

6 i

KHZ

I0

iI i

i ii

i

20

40

I

I i

v SV

ß IHC

GERBIL

ß ST

oOHC

K2-R

{N

z z

z

u I00

80

z

80

J

60

• 4o z z

2o

20

z

z

=

•

o

0 .

•

I

I

4

FIG. 7.

I

6

DISTANCE

I

8

FROM

I

I0

APEX

IN

12

I

I

0

2 DISTANCE

.

I

I

4

6 FROM

I

8 APEX

I

I0 IN M M

I

12

MM

Cochleogram of the right ear of gerbil K4.

Filled and

unfil[ed circles indicate the percentages of remaining inner and outer hair cells. Filled diamonds indicate normally re-

FIG. 9. Coch[eogram of the right ear of gerbil K2; otherwise, same as Figs, 7 and 8. Note SV response polarity associated with depleted outer hair cell regionsin both base and apex.

sponding fibers and the inferred location of their innerration,

Filled and untilled triartgles indicate response polarities (un-

filled. scala-vestibuli excitatory; filled: scala-tympani excitatory) of abnormally respondingfibers and the inferred location of their innerration. Best-frequency scale taken to represent the CF scale. Best-frequency and distance scales related by coch[ear map of Fig. 2.

the lesionwas variable not onlyamonggerbilsreceiving identical treatments but also between the right and left coch!eas

of each.

Coch!eograms of three treated gerbils are shown in

.

BEST I

0.4 -i

i

i

i

vvSV ß ST

FREQUENCY 2 4 6 i

i

i

i

i

IN KHZ I0 20

I i i ii

i

ß IHC oOHC

40

i

i i

GERBIL K6-R

Figs, 7-9. In each, fi!led circ!es represent the population of inner hair cells and opencircles the population of outer hair cel!s in 400- to 600-/• strips. The resuiting curves showthe percentagesof remaining inner and outer hair cells as functions of both distance from

the cochlear apex (bottomscale) and correspondingbest frequency (top scale). The relationship betweenthe two scales is in accordancewith the cochlear map of Fig. 2. Each cochleogramshowsa nearly complete loss of both inner and outer hair cells at the extreme

base, and an adjacent region of variable location and extent over which inner hair cells are preserved and

z

z

80

J

60

outer hair cells are either missing or are substantiaily depleted. The latter region is typically fol!owed apicalward by a fu11complement of both inner and outer hair cells (Figs, 7 and 8). The only exceptionwas the right cochlea of gerbi! K2 (Fig. 9), which had an additional lesion at its apex. Under the assumption that stimulation by a CF tone produces a maximum of basilar-membrane vibration

• z

20

at or near a fiber's place of innervation,the best-fre. quency scales of Figs. 7-9 become those of CF. Accordingly, the response polarities of fibers with ab. normal response patterns are indicated at their in-

z

•

o i

;[

I

I

2

4

6

8

DISTANCE

FROM

APEX

I..

,

I0 IN

12

MM

ferred spacecoordinatesby filled andurdilledtriangles, the former for ST and the latter for SV fibers.

Filled

FIG. 8. Cochleogram of the right ear of gerbil K6, Rare-

diamonds'indicatefibers with normal responsep•..

faction-click responses of SVfibers arbitrarilyplacedat

terns. Eachcoch!eogram demonstrates .thestriking

9, 0 mm indicate that their (unknown)CF's are above 9,0 •z;

association of SV fibers with coChlear regions highly

otherwise,

depleted or entirely void of outer hair cells.

same as Fig, 7.

This

J. Acoust..qec.Am., Vol. 59, No. 4, April 1976 Redistribution subject to ASA license or copyright; see http://acousticalsociety.org/content/terms. Download to IP: 130.88.90.140 On: Thu, 18 Dec 2014 18:02:29

972

Sokolich eta/.' Response polarities of cochlear haircells

.

creasesks thepercentage of remaining outerhair

Isv=elsv:5 sv:olsv: Isv:e

_•

972

IST=OIST= I IST=41ST=61ST=38

cells decreases and reaches zero when the percentage

,,, !oiN=O IN=O IN=O IN=13

falls below 20%. The lower diagram in the figure indicates

how the ratio

of the number

of SV fibers

to the

n- U

number of ST fibers varies with the percentage of remaining outer hair cells. The ratio is small when the

ZbJ

percentage is equal to or greater than 50%, indicating

'r'z

60

-

a predominant association of ST fibers with cochlear regions containing full or nearly full complements of outer hair cells. As the percentage of remaining outer hair cells decreases below 50%, the ratio increases rapidly and tends toward infinity. This occurs because

(DZ

_Z--

ILl

I

n-

0

20 i, 40

I

I

60

80

I00

the number

of abnormal

ST fibers

decreases

toward

zero.

io

I

!

i

I

III.

DISCUSSION

The general findings of our auditory-nerve experiments on kanamycin-treated gerbils are illustrated in Figs. 7-9 and are summarized in Fig. 10. Perhaps the mo•t significant outcome of these experiments is the consistent

association

of abnormal

SV fibers

with

cochlear regions having either an infinite or a large ratio of preserved innear hair cells to preserved outer

zz

hair

O0

20

REMAINING

40

60

80

OUTER HAIR IN PERCENT

cells.

Of the SV fibers

for which we have the

necessary data, more than 90% showeddefinite excitation during basilar-membrane deflection (displacement and/or velocity) toward scala vestibuli and definite

I00

CELLS

FIG. 10. Upper diagram summarizes correlations between fiber classification and hair-cell loss in kanamycin-treated

gerbils. Each bin occupiesa 20%x20% range of remaining hair cells. Given within each bin are the numbers of SV, ST, and N fibers associatedwith percentagesincludedby the bin SV, ST, N: scala-vestibuli excitatory, scala-tympaai excitatory, normal. Lower graph shows how the ratio (number of SV

inhibition of spontaneous activity during its deflection toward scala tympani. This SV response polarity is consistent with the morphological polarization of the inner hair cells, as well as with that of other mechanoreceptive hair cells. It is unlikely that this response polarity was changed by the kanamycin treatment. With respect to inhibition of spontaneous activity it

fibers)/(numberof ST fibers) varies with the percentageof re-

shouldbe emphasizedthat more than 95% of the SV

maining outer hair cells.

fibers

for which

we obtained

CF thresholds

had thresh-

old shifts of at least 40 dB, so the spontaneous activity was hardly the result of acoustic stimulation. association holds irrespective of CF or inferred cochlear location. The latter point is particularly well illustrated in the cochleogram of Fig. 9, in which SV fibers are associated with regions of depleted outer hair cells both in the apex and in the base. Fibers classified

as either

ST or N were

never

associated

with regions of highly depleted outer hair cells. Statistical

classification

results

of our correlations

and hair-cell

between

loss are summarized

fiber

in

Fig. 10. The upper diagram in the figure is a twodimensional histogram showing the response classification of the 85 fibers contacted in our kanamycin-treated gerbils as a function of the percentages of remaining inner (ordinate axis) and outer (abscissa axis) hair cells. Given within each particular 20%x 20% bin are

the numbers of SV, ST, and N fibers associatedwith the percentages of inner and outer hair cells covered by the bin. Note that fibers that produced normal response patterns were associated exclusively with cochlear regions having the highest percentages of remaining inner and outer hair cells. Only abnormal SV fibers are associated with cochlear regions containing the lowest percentages of remaining outer hair cells. Furthermore, the number of abnormal ST fibers de-

Althoughapproximately 86% of the fibers associated with cochlear regions containing either a full oranearly full complement of hair cells were classified as

either ST or N, approximately 14% of them were classified as SV. These SV fibers were predominantly associated with cochlear regions adjacent to those having depleted populations of outer hair cells. Because there is some uncertainty in correlating the CF

of an abnormal fiber with cocklear location, it is possible that these SV fibers in fact innervated the adjacent regions with depleted populations of outer hair cells. The classification of fibers contacted in our kanamycin-treated gerbils was straightforward. In general, if either the normal velocity or displacement responses were absent, or if their po:l-arities were reversed, the fibers

were

considered

abnormal

and were

classified

accordingly. Nonetheless, some ambiguity in classification did exist. The first ambiguous case refers to ST and N fibers

whose CF's

are

in the 2-6-kI-Iz

range. The ambiguity exists because of the fact that some ST fibers within this CF range showed excitation during both motion and displacement of the basilar membrane toward scala tympani and showed inhibi-

J. Acoust. Soc. Am., Vol. 59, No. 4, April 1976

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973

Sokolicheta/.: Response polaritiesof cochlearhair cells

tion during both motion and displacement in the opposite direction. The only feature distinguishing such fibers from N fibers in this CF range was the presence of an abnormal, and somewhat exponentiai, adaptation of the velocity component of their response. Consequently, unless either the normai velocity or the normai displacement response was absent, or the velocity response showed an abnormai adaptation, fibers whose

CF's were in the 2- to 6-kHz range were classificed as normal. The other ambiguous case refers to SV and N fibers whose CF's were below about 2 kHz. The ambiguity may arise here because of a qualitative similarity between the response patterns of velocity-sensitive SV fibers and N fibers, since both show excitation during basilar-membrane motion toward scala vestibuli and inhibitation during motion in the opposite direction. However, N fibers show a strong displacement

response of opposite polarity. Consequently, unless the displacement responses were either reversed, absent, or substantially reduced, or the velocity response showed an abnormai adaptation, fibers whose CP's were below about 2 kHz were classified

as normal.

The possible ambiguity in distinguishing between ST and N fibers served

lack

with medium of association

CF's

is irrelevant

of ST fibers

with

to the obcochlear

regions in which the population of outer hair cells was substantially depleted. As Fig. 10 shows, the occurrence of both ST and N responses is correlated positively with an increasing proportion of preserved outer hair

973

ly on either the inner hair cells or the radial fibers. If such synapses were inhibitory, they would invert the functional polarization of the outer hair cells. A hypothetical model of such interaction between inner and outer hair cells has been presented {Zwislocki,

1974b; Zwislocki and Sokolich, 1974b).

*Research was supported by NIH Grant NS-03950.

tPresent address: Departmentof otolarygology,State University of New York Upstate Medical Center, Syracuse, New York.

B•k•sy, G. Von (1944). "Ueber die mechanischeFrequenzanalyse in der Schnecke verschiedener Tiere,"

B•k•sy, G. von (1951). 'qVlicrophonics producedby touching the cochlea partition with a vibrating electrode," Soc. Am. 23, 29-35.

J. Acoust.

Billone, M. C. (1972). "Mechanical stimulation of cochlear

hair cells," Ph.D. dissertation(Northwestern University). Chamberlain, S.C. (1976). "Neuroanatomical aspects of the gerbil inner ear: Light microscope observations, "J. Comp. Neurol. (in press). Dallos, P. (1970). "Low frequency auditory characteristics: Species differences," J. Acoust. Soc. Am. 48, 489-499. Dallos,

P.,

Billone,

M. C., Durrant,

J. D., Wang, C.-Y.,

and Raynor, S. (1972). "Cochlear inner and outer hair cells: Functional differences,"

Science 177, 356-358.

Dallos, P., Cheatham, M. A., and Ferraro, J. (1974). "Cochlear mechanics, nonlinearities, and cochlear potentials," J. Acoust. Soc. Am. 55, 597-605.

EngstrSm, H., and Kohonen,A. (1965). "Cochlear damage

cells.

from ototoxic antibiotics,"

Because of the monotonic relationship between cochlear location and CF, the amount of hair-cell loss can be described

Akust. Z. 9,

3-11.

as a function

of either

variable.

It is

therefore necessary to emphasize that the positive correlation we have found between ST (SV) responses and the presence(absence) of outer hair ceils cannot be interpreted as an artifact of correlation between the responses and CF. When the population of outer hair cells was sufficiently depleted in the cochlear apex, we in fact found SV fibers

with low CF's.

In view of Spoendlin'sfinding that about 95% of all afferent auditory-nerve fibers end on the inner hair cells, practically all of our recordings must refer to these fibers. If this is true, the results of the present study provide strong evidence that inner hair cells produce an excitation of these fibers during either mo-

tion and/or displacementof the basilar membranetoward scala vestibuli. Furthermore, the positive correlation we found between the presence of outer hair cells and the excitation of associated fibers during

either motionand/or displacementof the basilar membrane toward scaia tympani strongly suggests that the outer hair cells do affect the firing rates of radial fibers, and that their effect is opposite in polarity to that inferred for the inner hair cells. Although the ST response polarity assigned to the outer hair cells appears to disagree with their morphological polarization, this seemingly paradoxical response polarity is physio1ogicaily possible. Given that the outer hair cells do affect the firing rates of fibers ending on the inner hair cells, they must do so through synapses ending direct-

Acta Otolaryngol.

59, 171-178.

Evans, E. F. (1972). "The frequency response and other properties of single fibers in the guinea pig cochlear nerve," J. Physiol. (London) 226t 263-287.

Flock, •. (1971). "Sensory transduction in hair cells," in Handbook of Sensory Physiology, edited by W. R. Loewenstein (Springer, Berlin), Vol. I, pp. 396-441. Kiang, N. Y. S., Watanabe, T., Thomas, E. C., and Clark, L. F. (1965), Discharge Patterns of Si,gle Fibers in the

Cat's Auditory Nerve (MIT Press, Cambridge, MA). Kiang, N.Y. S., Moxon, E. C., and Levine, R. A. (1970)o "Auditory nerve activity in cats with normal and abnormal cochleas," in Sensorineural Hearing Loss, edited by G. E. W. Wolstenholme and J. Knight (Churchill, London), pp. 241-268.

Konishi, T., and Nielsen, D. W. (1973). "The temporal relationship between motion of the basilar membrane and initiation of nerve impulses in the auditory nerve fibers," J. Acoust. Soc. Am. 53, 325(A).

Lira, D. J. (1972). "Fine morphology of the tectorial membrane; its relationship to the organ of Corti," ngo[. 96, 199-215.

Arch. Otolary-

Pease, D. C. (1964). Histological Techniquesfor Electron Microscopy (Academic, New York). Perkins, R. E. (1973). "Innerration patterns in cochleas of cat and rat: Study with rapid Golgi techniques," 175, 410 (A).

Anat. Rec.

Schmiedt, R. A., and Smith, R. L. (1974). "Middie-ear transfer function of the anesthetized Mongolian gerbil," Soc. Am. 56, S4(A).

J. Acoust.

Sokolich, W. G., and Smith, R. L. (1973). "Easy accesss to the auditory nerve in the Mongolian gerbfi," J. Acoust. Soc. Am. 54, 283(A). Sokolich, W. G., and Zwislocki, J. J. (1974a). "Evidence for phase opposition between inner and outer hair cells," J. Acoust. Soc. Am. 55, 466{A). Sokolich, W. G., and Zwislocki, J. J. (1974b). "Two classes of abnormal responses recorded from auditory-nerve fibers

J. Acoust.Soc. Am., Vol. 59, No. 4, April 1976

Redistribution subject to ASA license or copyright; see http://acousticalsociety.org/content/terms. Download to IP: 130.88.90.140 On: Thu, 18 Dec 2014 18:02:29

974

Sokolich eta/.: Response polarities of cochlear haircells

of kanamycin-treated gerbils," J. Acoust.Soc. Am. 55, S78(A).

Sokolich,W. G., andZwislocki,J. J. (1974c). "Low-level responsephasesof auditory-nervefibers," J. Acoust. Am. 56, S21(A).

Spoendlin, H. (1966). "The Organization of the Cochlear

Receptor,"Adv. Oto-Rhino-Laryngo[. 13 (S. Karger,Basel). Spoendlin,H. (1970). "Structural basis of peripheral frequencyanalysis," in FrequencyAnalysis and Periodicity Detection iv Hearing, edited by R. Plomp and G. F. Smoorenburg

(A. W. Sijthoff, Leiden, Netherlands), pp. 2-36. Spoend[in,H. (1975). Discussion: International Symposiumon The Effects of Noise on Hearing--Critical 1975, Cazenovia, NY.

Issues, 23-25 June,

Tasaki, K., Tsukahara, Y., Ito, S., Wayher, M. J., and Yu, W. T. (1968). "A simple, direct, and rapid method for filling microelectrodes," Physiol. Behar. 3, 1009-1010.

Wilson, J.P.,

and Johnstone,J. R. (1975). "Basilar mere-

974 brane and middle-ear vibration in guinea pig measured by capacitive probe," J. Acoust. Soc. Am. 57, 705-723. Zwislocki, J. J. (1965). "Analysis of some auditory charac-

teristics," in Handbookof MathematicalPsychology, edited by R. D. Luce, R. R. Bush, and E. Galanter (WHey, New York), Vol. III, pp. 1-97.

Zwislocki, J. J. (1974a). "CochIear waves: Interaction betweentheory and experiments," J. Acoust. Soc. Am. 55, 578-583.

Zwislocki, J. J. (1974b). "A possibleneuro-mechanical soundanalysis in the cochlea," Acustica 31, 354-359.

Zwislocki, J. J., andSokolich,W. G. (1973). "Velocityand displacementresponsesin auditory-nerve fibers," Science 182, 64-66.

Zwislocki, J. J., andSokolich,W. G. (1974). "Neuro-mechanicalfrequencyanalysisin the cochlea," in Facts and Models in He•/ng, edited by E. Zwicker and E. Terhardt (Springer, Berlin), pp. 107-117.

J. Amust. So• Am., Vol. 59, No. 4, April 1976

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