Basilar-membrane responses to clicks at the base
of the chinchilla cochlea
Alberto Recio,a)Nola C. Rich,b)S. Shyamla Narayan, and Mario A. Ruggeroc)
The Hugh Knowles Center, Department of Communication Sciences and Disorders, and Institute for
Neuroscience, Northwestern University, 2299 North Campus Drive, Evanston, Illinois 60208-3550
?Received 25 September 1997; revised 19 December 1997; accepted 31 December 1997?
Basilar-membrane responses to clicks were measured, using laser velocimetry, at a site of the
chinchilla cochlea located about 3.5 mm from the oval window ?characteristic frequency or CF:
typically 8–10 kHz?. They consisted of relatively undamped oscillations with instantaneous
frequency that increased rapidly ?time constant: 200 ?s? from a few kHz to CF. Such frequency
modulation was evident regardless of stimulus level and was also present post-mortem. Responses
grew linearly at low stimulus levels, but exhibited a compressive nonlinearity at higher levels.
Velocity-intensity functions were almost linear near response onset but became nonlinear within
100 ?s. Slopes could be as low as 0.1–0.2 dB/dB at later times. Hence, the response envelopes
became increasingly skewed at higher stimulus levels, with their center of gravity shifting to earlier
times. The phases of near-CF response components changed by nearly 180 degrees as a function of
time. At high stimulus levels, this generated cancellation notches and phase jumps in the frequency
spectra. With increases in click level, sharpness of tuning deteriorated and the spectral maximum
shifted to lower frequencies. Response phases also changed as a function of increasing stimulus
intensity, exhibiting relative lags and leads at frequencies somewhat lower and higher than CF,
respectively. In most respects, the magnitude and phase frequency spectra of responses to clicks
closely resembled those of responses to tones. Post-mortem responses were similar to in vivo
responses to very intense clicks. © 1998 Acoustical Society of America. ?S0001-4966?98?02504-1?
PACS numbers: 43.64.Kc, 43.64.Ha ?RDF?
The basilar membrane of the mammalian cochlea re-
sponds nonlinearly to stimulation with tones ?e.g., Rhode,
1971; Sellick et al., 1982; Robles et al., 1986; Cooper and
Rhode, 1992; Nuttall and Dolan, 1996; Russell and Nilsen,
1997; reviewed by Ruggero, 1992b; and Patuzzi, 1996?.
Since, for nonlinear systems, the responses to tones cannot
generally be used to predict the responses to arbitrary
stimuli, a thorough understanding of basilar-membrane be-
havior requires the use of other stimuli, such as tone com-
plexes, noise and clicks. Clicks are especially useful because,
being punctate and wide-band in nature, they permit precise
timing of a system’s responses while simultaneously testing
it over a wide range of frequencies. In the case of linear
systems, the Fourier transform of the unit impulse response
is identical to the system’s transfer function. Departures from
such identity in the case of nonlinear systems may provide
clues about the nature of the nonlinearities.
The first in vivo study of basilar-membrane responses to
clicks was carried out in the 8-kHz region of the squirrel
monkey cochlea ?Rhode and Robles, 1974; Robles et al.,
1976?. Although hampered by substantial waveform distor-
tion introduced by the Mo ¨ssbauer technique, this pioneering
investigation established that basilar-membrane responses to
clicks consisted of a brief and low-frequency initial segment,
which grew linearly with stimulus intensity, and a longer-
lasting segment with periodicity corresponding to the char-
acteristic frequency ?CF? measured using single tones, which
grew at compressive rates with stimulus level. Mildly non-
linear growth of basilar-membrane responses to clicks was
also measured with a capacitive probe at the basal region of
guinea pig cochleae that had been severely traumatized by
the experimental procedures ?LePage and Johnstone, 1980?.
More recently, laser methodology and improved surgical
techniques have made it possible to obtain undistorted re-
cordings of responses to clicks in the basal region of rela-
tively healthy cochleae of chinchilla ?Ruggero and Rich,
1990, 1991a, b; Ruggero et al., 1991, 1992a, b, 1993, 1996?
and guinea pig ?Nuttall and Dolan, 1993; de Boer and Nut-
tall, 1997?, as well as near the apex of guinea pig and chin-
chilla cochleae ?Cooper and Rhode, 1996?. To date, how-
ever, reports of these recordings ?including those from our
laboratory? have been very limited in scope and detail.
The present paper provides an extensive description of
basilar-membrane responses to clicks for the 8–10 kHz re-
gion of the chinchilla cochlea. At this site, responses to
clicks are frequency modulated, exhibiting a low-to-high-
frequency glide both in vivo and post-mortem. In vivo, the
responses to clicks grow at compressive rates within 100 ?s
of response onset, and accurately predict the main features of
responses to tones. Taking the frequency glide into account,
nonlinear feedback appears to accompany, nearly instanta-
neously, the CF spectral components of basilar-membrane
a?Current address: Department of Physiology, University of Wisconsin, 1300
University Ave., Madison, WI 53706.
b?Current address: 1193 Liberty Church Road, Mocksville, NC 27028.
c?Electronic mail: email@example.com
19721972 J. Acoust. Soc. Am. 103 (4), April 19980001-4966/98/103(4)/1972/18/$10.00© 1998 Acoustical Society of America
A. Animal preparation
Male chinchillas, weighing about 0.5 kg, were anesthe-
tized with an initial dose of Ketamine ?100 mg/kg, S.C.? and
supplementary doses of sodium pentobarbital ?I.P.?, or with
Ketamine ?20 mg/kg, I.M.? and Dial ?50 mg/kg? in urethane
?200 mg/kg, I.P.? and supplementary doses of Dial in ure-
thane. They were tracheotomized and intubated but forced
ventilation was rarely used. Core body temperature, mea-
sured using a rectal probe, was maintained at 38 °C using a
servo-controlled electrical heating pad. The left pinna was
resected, the bulla was widely opened, the tensor tympani
was cut and the stapedius was detached from its anchoring.
A silver-wire electrode was placed on the round window to
record compound action potentials ?CAPs? evoked by tone
bursts. A small hole was made in the basal turn of the otic
capsule by first thinning and drilling the bone using a dental
bur and then chipping away bone fragments with a metal
pick. The hole allowed direct visualization of the basilar
membrane and placement on it of a few glass microbeads
?10–30 ?m in diameter?, which served as reflecting targets
for the laser beam. In most experiments, the otic-capsule
hole was left open. In six experiments, basilar-membrane
recordings were made after the hole was covered with a win-
dow fashioned from slide coverslip glass ?to minimize mo-
tion of the perilymph meniscus overlying the recording site;
see section A of Discussion?. In these experiments, the
basilar-membrane recordings were complemented by vibra-
tion measurements from the stapes or the incus, near the
incudostapedial joint ?without using reflecting beads?.
B. Acoustic stimulation
Acoustic stimuli were produced by exciting a Beyer
DT-48 earphone with electrical signals from a custom-built
digital waveform generator ?Ruggero and Rich, 1983? or
from a commercial system ?Tucker-Davis Technologies?.
Electrical clicks, which had durations of 50-?s or 10-?s ?up
to and following experiment L131, respectively?, were pre-
sented with repetition periods of 20–53 ms ?usually 25 ms?.
Single-tone stimuli were modulated at onset and offset by
1/2 period of a raised cosine waveform ?1.16 ms rise/fall
time?. The tone bursts had durations of 5, 10, 25 or, excep-
tionally, 3 ms and repetition periods of 25, 50, 100 or 15 ms,
respectively. At the beginning of each experiment, the probe
tip of a calibrated miniature microphone ?Knowles 1842 or
1785? was placed within 2 mm of the tympanic membrane.
Using this microphone, the transfer function of the electroa-
coustic stimulus system was measured for 100 Hz–24 kHz
tones, with 100-Hz resolution. The amplitude and phase
spectra of the transfer function were stored digitally and
were later used to compute the acoustic-click waveform by
Fourier synthesis. A simulated electrical click was convolved
with the transfer function in the frequency domain to obtain
the spectrum of the acoustic click. Inverse Fourier transfor-
mation of this spectrum yielded the time waveform of the
acoustic click. Throughout this paper click levels are given
as the peak pressures of the synthesized clicks, expressed
relative to 20 ?Pa.
C. Laser velocimetry
Basilar-membrane vibrations were recorded using a la-
ser velocimeter, which measures the velocity of a vibrating
object by detecting the Doppler frequency shift of light re-
flected from it. In our application, the laser beam was re-
flected from glass microbeads placed on the basilar mem-
brane. The velocimeter consisted of a 20 mW He–Ne laser
?Spectra Physics 106-1?, a fiber vibrometer ?Dantec 41X60?
and a Doppler frequency tracker ?Dantec 55n20?. The veloci-
meter was coupled to a compound microscope ?Olympus
BHMJ? equipped with 5X and 20X ultralong working-
distance objectives ?Mitutoyo Plan Apo 5X, N.A. 0.14, and
20X, N.A. 0.42?. The electrical output of the Doppler fre-
quency tracker, a voltage proportional to the velocity, was
filtered with a bandpass frequency response ?1–15 000 Hz?.
The output of the filter was sampled by a computer at a rate
of 40 kHz ?up to L131? or 100 kHz ?after L131?.
D. Data analysis
Responses to clicks or tones were averaged over 512,
1024 or 2048 stimulus repetitions. The magnitude and phase
spectra of the average-response waveforms were routinely
calculated by Fourier transformation using time windows of
12.8 or 10.24 ms ?i.e., 512 25-?s bins or 1024 10-?s bins?.
In addition, short-term Fourier transforms ?STFTs; see Fig.
5?C? were computed using 0.8-ms Hanning windows cen-
tered at each delay and zero padded to an overall duration of
3.2 ms. Consecutive STFTs were computed at 0.4-ms inter-
vals. The envelope and instantaneous frequency of the re-
sponses to clicks were estimated using their analytic signal
representation ?Bennett, 1970?. The analytic signal of a
waveform is a complex quantity whose real part is the wave-
FIG. 1. Responses to intense rarefaction clicks recorded from the incus ?top?
and a basal site of the basilar membrane ?bottom? in a single chinchilla ear.
The thin vertical line intersects the incus response at the time it reaches 20%
of its maximum value and may be taken as marking the onset of the input to
the cochlea. Click peak pressure was 102 dB re: 20 ?Pa.
1973 1973 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998Recio et al.: Basilar-membrane responses to clicks
form itself and whose imaginary part is the Hilbert transform
of the real part. The envelope of the waveform is equal to the
magnitude of the analytic signal and the instantaneous fre-
quency corresponds to the derivative of the phase of the ana-
Basilar-membrane responses to clicks were recorded at a
region of the chinchilla cochlea located about 3.5 mm from
the oval window. Data from two representative cochleae
?L13 and L113? are highlighted throughout the paper. Re-
sponses from these cochleae were selected for presentation
because: ?1? they were exceptionally stable ?remaining in-
variant over several hours of recording?; ?2? they were col-
lected in near-normal ears ?judging from surgically induced
CAP threshold elevations at CF of 6–12 dB?; ?3? they were
especially sensitive; and ?4? extensive samples of responses
to tones in the same cochleae are available for comparison
?Ruggero et al., 1997?.
A. Main features of basilar-membrane responses to
Figure 1 allows a comparison of velocity responses to
identical intense acoustic clicks measured in a single chin-
chilla ear from the incus ?top panel? and from a basilar-
membrane site located about 3.5 mm from the oval window
?bottom panel?. The response of the incus consisted of a
short oscillation, consistent with the untuned, wide-band na-
ture of middle-ear vibrations. The basilar-membrane re-
sponse, much larger ?note ordinate scales? and longer lasting
than the incus response, was relatively undamped, displaying
the characteristic ‘‘ringing’’ of a well-tuned bandpass sys-
tem. In the overwhelming majority of experiments, rarefac-
tion clicks evoked basilar-membrane responses whose first
peak ?‘‘P1’’ in Fig. 1? was in the direction of scala vestibuli.
membrane motion, using intense clicks and 100-kHz sam-
pling frequency, were performed in 7 ears. In 6 of these, the
basilar-membrane recordings were carried out after covering
the otic capsule hole with a glass window. Defining response
onset as the time at which oscillations first reached 20% of
their maximum value, the cochlear delay of the basilar-
membrane response was computed as the interval between
the onset of motion at the incus and at the basilar membrane.
The cochlear delay measured in these 6 ears was 29.8?12.4
?s ?mean?standard deviation?.
Figure 2 presents basilar-membrane responses to clicks
plotted with uniform scales of velocity ?left column? and
velocity normalized to stimulus pressure ?right column?. If
the basilar membrane vibrated linearly, neither the response
wave shapes nor their normalized magnitudes would vary as
a function of stimulus level. In fact, increases in click level
ofincus and basilar-
FIG. 2. Basilar-membrane responses to rarefaction clicks presented at several intensities. The responses are displayed with uniform scales of velocity ?left
column? and normalized velocity ?velocity divided by peak click pressure, right column?. The thin vertical lines indicate the onset of middle ear ossicular
vibration. Response polarity as in Fig. 1. The parameter next to each trace indicates the peak click pressure, expressed relative to 20 ?Pa.
1974 1974 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998Recio et al.: Basilar-membrane responses to clicks
FIG. 3. Basilar-membrane responses to rarefaction clicks. The responses are displayed with scales that are systematically compressed by a ratio of 2 ?i.e., 6
dB? for every increment of 10 dB in stimulus intensity. Such scaling, which de-emphasizes intensity-dependent changes in response magnitude, allows for
easier comparison of the response wave shapes.
FIG. 4. Basilar-membrane responses to condensation clicks. All details as for Fig. 3.
19751975 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998Recio et al.: Basilar-membrane responses to clicks
were accompanied both by changes in response wave shape
and by decreases in normalized velocity ?right column?.
Compressive growth was obvious at all stimulus levels but it
became less evident at the very highest levels.
Figure 3 shows a more complete series of basilar-
membrane responses to rarefaction clicks ?from the same co-
chlea of Fig. 2? with scales chosen to facilitate comparison of
the wave shapes without regard to their magnitudes: the
scales are compressed by a factor of 2 ?6 dB? for every
10-dB increase of stimulus intensity. For most click intensi-
ties, the envelopes of the responses consisted of two adjacent
spindle-shaped lobes. This ‘‘two-lobe’’ wave shape was
characteristic of cochleae that were in good physiological
state, it was absent in cochleae that were surgically trauma-
tized and disappeared after death ?Fig. 13? or acoustic over-
stimulation ?Figs. 6 and 8 of Ruggero et al., 1996?. The early
response peaks grew with stimulus intensity at faster rates
than later ones, giving rise to a systematic skewing of the
envelope toward earlier times. For example, at low stimulus
levels ?14–24 dB SPL?, the response maximum corre-
sponded to the ninth positive peak ?P9? but the maximum
shifted to earlier peaks with increases of stimulus level: P8 at
34 dB, P6 at 54 dB, and P2 at 94 and 104 dB. The time
elapsed between the response onset ?0.38 ms? and the maxi-
mum of the response envelope decreased from 0.97 ms for
24-dB clicks to 0.25 ms for 104-dB clicks.
Figure 4 shows responses to condensation clicks re-
corded in an exceptionally sensitive preparation. Apart from
the long-lasting ringing, with duration longer than in any
other cochlea in our sample, these responses share the same
characteristics observed in Figs. 1–3, including initial re-
sponse polarity ?i.e., responses to condensation and rarefac-
tion clicks, respectively, begin with motion toward scala
tympani and scala vestibuli?, compressive growth, and skew-
ing of the envelope toward earlier times as a function of
increasing stimulus level.
B. Frequency modulation in basilar-membrane
responses to clicks
Close inspection of the waveforms of responses to clicks
?e.g., Fig. 2, 104 dB SPL? reveals that their periodicity or
instantaneous frequency changed as a function of time. To
quantify this frequency modulation, we computed the instan-
taneous frequency and the envelope of the response wave-
forms using the ‘‘analytic signal’’ representation ?Bennett,
1970; see Methods?. Figure 5 shows the response to a click
presented at 84 dB SPL ?panel A?, as well as its envelope
?continuous line, panel B? and its instantaneous frequency
?dashed line, panel B?, plotted against time. The instanta-
neous frequency increased rapidly within several hundreds of
microseconds: it was initially about 1 kHz, surpassed 5 kHz
by the time of the first positive peak and saturated at about
10 kHz. An exponential fit had a time constant of 0.2 ms.
The variation of frequency with time was also measured
using short-term Fourier transforms ?STFTs; see Methods?.
Panel C of Fig. 5 displays the magnitude part of the STFTs
for the response of panel A as a family of contour lines
spaced at 2-dB intervals relative to the ensemble peak, with
the thicker contour lines indicating higher spectral magni-
tudes. Also indicated is the frequency at which the peak
magnitude of the STFT occurs as a function of time ?dashed
line?. Both the STFT contours and the peak instantaneous
frequency show that the frequency content glides from low
to high (?CF?. The increase in response frequency was ac-
companied by a narrowing of the bandwidth. This may be
ascertained from the STFT contours of Fig. 5C by measuring
the frequency range encompassed by a fixed number of con-
tour lines along any given time ‘‘slice.’’ The equivalent rect-
angular bandwidth and the 10- and 20-dB bandwidths were
3.9, 4.0 and 8.3 kHz, respectively, at 0.8 ms and decreased to
2.8, 3.3, and 4.4 kHz at 2 ms.
Instantaneous frequency was influenced by stimulus
level but its time trajectory retained its main features even at
the highest levels and post-mortem ?Fig. 6A?. Thus, it is
clear that the frequency modulation is not a byproduct of
nonlinear or ‘‘active’’ cochlear processing. In contrast, the
response envelopes were highly dependent on stimulus inten-
sity. Figure 6B shows the envelopes of responses to clicks
with peak pressure of 64-, 84- and 104-dB, normalized to
104-dB. Had responses grown linearly, the normalized enve-
lopes would be identical throughout their extent. In fact, due
FIG. 5. Instantaneous frequency and envelope of basilar-membrane re-
sponses to 84-dB clicks. ?A? Original response waveform. ?B? Envelope
?continuous line? and instantaneous frequency ?dashed line? of the waveform
depicted in A. ?C? Magnitude of short-time Fourier transforms ?STFTs; see
Methods? of the same waveform, displayed as a function of time ?abscissa?
and frequency ?ordinate?. The thickness of the contour lines indicates the
STFT amplitude, expressed relative to the ensemble maximum. The thickest
line indicates a relative amplitude of ?2 dB and the thinner lines correspond
to lower levels, in steps of ?2 dB. The frequency of the STFT maximum is
also shown as a function of time ?dashed line?. The thin vertical line indi-
cates the onset of middle-ear ossicular vibration.
1976 1976J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
to the compressive growth of responses, the envelopes coin-
cide only at the onset ?where responses grow linearly?.
C. Growth of responses as a function of click intensity
The initial peaks of responses to clicks grew with inten-
sity at faster rates than later peaks ?Figs. 2–4?. To quantify
these rates, peak times were determined in the responses to
high-intensity clicks and the corresponding magnitudes
?measured in the response envelopes? were plotted against
click intensity ?Fig. 7?. With the exception of animal L13,
the magnitudes measured were those corresponding to veloc-
ity maxima toward scala vestibuli ?i.e., positive peaks in re-
sponses to rarefaction clicks?. At low levels of stimulation
?peak pressure: ?30–40 dB re: 20 ?Pa?, all peaks grew
linearly or nearly so. The initial oscillation, P1, grew in an
almost linear fashion at all levels. Peaks 3–7 grew compres-
sively at intermediate levels but tended to become linear
again at the highest levels of stimulation. Later peaks grew
nonlinearly ?at rates as low as 0–0.2 dB/dB? throughout the
range of moderate and high stimulus levels.
To further explore the development of compressive non-
linearity as a function of time, we computed the slopes of the
velocity-intensity functions for the positive peaks and aver-
aged the slopes over 50-dB ranges encompassing the highest
stimulus levels. Figure 8 displays such averages for the four
cochleae represented in Fig. 7. Nonlinear growth was evident
within 100 ?s ?i.e., 1 CF period? of response onset ?vertical
line?. In a sample of 8 sensitive cochlea ?including the 4 of
Fig. 8? the first positive and negative peaks, respectively,
grew at rates of 0.950?0.035 and 0.883?0.053 dB/dB ?over
40-dB ranges?. Such slopes differed significantly from 1
dB/dB (p?0.005, one-tailed t test?.
Slopes diminished rapidly as a function of time, from
values approaching linearity immediately after response on-
set, to minima as low as 0.1–0.2 dB/dB at 1.3–1.9 ms. At
later times, growth slopes waxed and waned and exhibited
local maxima as high as 0.5–0.6 dB/dB and minima as low
as 0.1 dB/dB. Inspection of the curves for cochleae L13 and
L113 in Fig. 8 indicates that the slope maxima ?i.e., com-
pression minima? were approximately synchronous with the
constrictions that demarcate adjacent lobes of the time-
domain response waveforms ?Figs. 3 and 4?. This was also
true for the other cochleae represented in Fig. 8.
D. The magnitude-frequency spectra of
basilar-membrane responses to clicks
Figure 9 shows the magnitude of the Fourier transforms
of the waveforms depicted in Figs. 3 and 4 ?computed using
12.8-ms windows?. At low spectral frequencies, the re-
sponses grew linearly: for 10-dB increments in click level,
the responses grew by a factor of 3.1 ?10 dB?. At frequencies
around CF, response growth was linear at the lowest stimu-
lus levels but quite compressive at high intensities. The re-
sponse bandwidth changed systematically with click inten-
sity: for low stimulus levels, responses were largely confined
to frequencies near CF, whereas at high stimulus levels re-
sponses encompassed a broad range of frequencies. The
change in bandwidth was accompanied by an overall fre-
quency shift toward lower frequencies. At the highest click
intensities, the frequency of the spectral maximum was about
?0.5 octave relative to CF. The Q10?peak frequency divided
by 10-dB bandwidth? decreased substantially as a function of
click intensity. In cochlea L113, for example, Q10was 4.06
for 44-dB clicks and 1.08 for 104-dB clicks. At frequencies
near CF, some of the frequency spectra included sharp
notches. These were seen only in the most sensitive and non-
linear preparations, and disappeared as the state of the prepa-
ration deteriorated with the passage of time, after death ?note
notches at 8.48 kHz in in vivo responses of L13 ?Figs. 9 and
10? and their absence post-mortem ?Fig. 10?? or after acous-
tic overstimulation ?Fig. 9 of Ruggero et al., 1996?.
The intensity-dependent nonlinear growth of responses
is best visualized by normalizing the spectra of Fig. 9, fre-
quency by frequency, to stimulus pressure ?using the acous-
tic calibration tables; see Methods?, thus producing estimates
of basilar-membrane gain ?Fig. 10?. ?In a linear system, such
a procedure eliminates entirely the effects of irregularities in
the stimulus spectrum. The usefulness of the correction is
less certain in the case of a nonlinear system.? For clarity, the
gains have been smoothed using a 3-point running average.
At frequencies lower than 1/2 octave below CF, the curves
coincided, indicating linear growth. Nonlinear behavior was
FIG. 6. Instantaneous frequency ?A? and envelope ?B? of basilar-membrane
responses to clicks as a function of time and stimulus level. The thick
dashed line in panel A corresponds to responses recorded post-mortem
?94-dB clicks?. The vertical continuous line in panel B indicates the onset
time of middle-ear vibration. The vertical dashed lines indicate the times of
the first and second positive peaks and the first negative peak. The ordinate
in panel B has units of micrometer/s and are normalized to 104-dB ?i.e., the
velocities of responses to 84- and 64-dB clicks are magnified 10 and 100
times, respectively?. Data are those represented in Figs. 2 and 3.
19771977J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
evident at higher frequencies (?6 kHz?, specially near CF ?9
or 10 kHz?, where gains became smaller with increases of
stimulus level. Compressive growth persisted even at the
highest levels of stimulation ?compare the curves for 104 or
106 dB with those for 94 or 96 dB?.
E. The phase-frequency spectra of basilar-membrane
responses to clicks
Figure 11A displays the phases of responses to clicks in
one cochlea, obtained by Fourier transformation of some of
the waveforms of Fig. 3. The curves represent the phases of
basilar-membrane displacement toward scala tympani rela-
tive to maximum condensation at the eardrum. The curves
show a monotonically increasing phase lag, interrupted in
some cases by abrupt shifts at frequencies corresponding to
notches in the magnitude spectrum ?Fig. 9A?. Slopes were
shallower at frequencies lower than 7 kHz than at higher
frequencies and were steepest near 11 kHz, a frequency
somewhat higher than the CF ?estimated from responses to
low-level clicks?. ?Slopes were steepest at CF only in the
cases in which there were abrupt phase changes near this
frequency ?64–94 dB; see Fig. 13B?.? In the range 3–7 kHz,
the average slope was ?250 ?s. In the 8–10 kHz region, the
slopes varied between about ?560 ?s for the responses to
clicks presented at 104 dB SPL ?both in vivo and post-
mortem? and ?826 ?s for 24-dB clicks ?not illustrated?.
Figure 11B shows a representative sample of phase-vs-
frequency curves, normalized to inward stapes displacement,
for responses to clicks recorded in several cochleae. The
basilar-membrane sites had CFs in the range 8–12 kHz and
the clicks were presented at comparable levels ?82–88 dB
SPL?. The low-frequency segments (?6–7 kHz? had slopes
confined to a relatively narrow range, ?137 to ?269 ?s,
irrespective of CF. The high-frequency segments diverged
FIG. 7. The magnitudes of selected positive peaks of the responses to clicks, plotted against stimulus level. Also indicated are lines with slopes of 1 dB/dB
and 0.2 dB/dB. Each panel represents data from one sensitive cochlea.
FIG. 8. Average slopes of the magnitude-intensity functions for the re-
sponses to clicks of 4 sensitive cochleae. The average slopes of curves such
as those depicted in Fig. 7 were computed over 50-dB ranges ?54–65 to
103–115 dB SPL?. The thin vertical line indicates the onset time of basilar-
membrane vibration ?325 ?s, averaged across the 4 cochleae?.
1978 1978J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
increasingly at frequencies higher than 1/2 octave below CF.
In general, the phase-frequency slopes were steepest near
CF. At CF, the phase lags amounted to 1.5–2 cycles. Aver-
age group delays were measured over 1-kHz ranges centered
at CF in responses to low-level clicks. ?Phase-vs-frequency
curves for responses to more intense clicks ?such as those of
Fig. 11B? included irregularities at frequencies near CF
which rendered the measurement of group delays unreliable.?
The cochleae represented in Fig. 11B had near-CF group
delays averaging 779?147 ?s ?mean?s.d.?. Group delays
measuredbetween7 kHzand1 kHz belowCF
?or somewhat smaller ranges if limited by the noise floor?
averaged 410?109 ?s.
The dependence of response phases on stimulus inten-
sity ?shown in Fig. 15B? re-plots the data of Fig. 11A after
normalization to the phases of responses to 64-dB clicks. For
low frequencies (?5–6 kHz? the phases varied little with
stimulus intensity, consistent with the linearity of response
growth in that frequency region. For frequencies ?6–9 kHz?
just below CF, the phases of responses exhibited increasing
lags as a function of increasing click level. The lags were
small except at levels higher than 74 dB. For frequencies just
FIG. 9. Magnitude-frequency spectra for the velocity responses to clicks in two sensitive cochleae. Clicks were presented at levels of 24 or 26 dB up to 104
or 106 dB, in steps of 10 dB. Data are those represented in Figs. 2 and 3.
FIG. 10. Gain-frequency spectra for the responses to clicks in two cochleae. Gains were computed by dividing, frequency by frequency, velocity magnitudes
?shown in Fig. 9? by the peak click pressure ?parameter?. The thick lines indicate the gains of responses recorded 10–20 minutes postmortem; dashed lines:
94 dB ?L113? and 96 dB ?L13?; continuous lines: 104 dB ?L113? and 106 dB ?L13?. Curves were smoothed using a 3-point running average.
19791979 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
higher than CF, the response phases showed increasing leads
as a function of increasing intensity. A similar intensity de-
pendence of phase ?lags and leads, respectively, for frequen-
cies lower and higher than CF, as a function of increasing
intensity? could be usually demonstrated in the responses of
all sensitive cochleae.
F. Relation between time-domain lobes and
magnitude notches and phase jumps in the frequency
To explore the spectral notches observed in the CF re-
gion ?Fig. 9?, as well as the associated phase jumps ?Fig. 11?,
the responses to clicks were studied using Fourier analysis of
selected time windows. Figure 12 shows such an analysis for
the response waveform shown in the inset. The waveform
was divided into two nonoverlapping segments ?B and C,
inset in Fig. 12A?. Segment B spans the first 1.6 ms of the
response and extends to the transition between the two re-
sponse lobes. Segment C, encompassing the second lobe,
starts at 1.6 ms and ends at 6.4 ms. The magnitude spectra
for these two segments are shown in Fig. 12A ?B: dotted
line; C: long-dash line?, together with the spectrum of the
entire original waveform ?solid line?. The magnitude spec-
trum of segment C ?long-dash line? is sharply tuned to fre-
quencies centered at 10.234 kHz, the frequency of the spec-
tral notch of the original waveform. The notch is absent from
segments B and C, which suggests that its presence in the
original waveform resulted from destructive interference be-
tween early and late out-of-phase spectral components. Fig-
ures 12B and 13 illustrate this.
Figure 12B shows the origin of the 360-degree phase
jumps ?Fig. 11?. At frequencies lower than that of the notch,
the phase-vs-frequency curve of the entire response was
dominated by the phase spectrum of segment B, whereas at
higher frequencies it was dominated by the phase spectrum
of segment C. At the notch frequency, the phases of seg-
ments B and C differed by 174 degrees ?i.e., they were es-
sentially in phase opposition?. Figure 13 demonstrates that
the response phases at the notch frequency exhibited a mono-
tonically increasing lag in the time interval of 1–2 ms ?i.e.,
straddling the constriction between the two lobes; indicated
by the bracket in Fig. 13?. Phases became stable within the
second lobe, after accumulating a phase lag of nearly 180
FIG. 11. Phase-vs-frequency curves for basilar-membrane responses to
clicks. ?A? The ordinate indicates the phases of displacement toward scala
tympani ?ST? referred to peak positive pressure ?condensation? at the ear-
drum. Phases were obtained by Fourier transformation of the data depicted
in Figs. 2 and 3 ?cochlea L113?. The thick dashed line indicates post-
mortem responses to intense clicks ?94-dB SPL?. The symbols indicate the
phases of responses to tones. ?B? Phase-vs-frequency curves for basilar-
membrane responses to clicks in 8 cochleae, including L113 ?identified by
an open circle?. The symbols indicate phases at CF ?measured in responses
to low-level clicks?. The phase curves are presented relative to inward stapes
motion. In one case ?L163, indicated by a triangle?, basilar-membrane and
stapes response phases were measured in the same ear; in the other cases,
basilar-membrane phases were normalized to previously published average
stapes data for chinchilla ?Fig. 9 of Ruggero et al., 1990?. Clicks had peak
pressures of 82–88 dB.
FIG. 12. Time-dependent variation of the magnitude- and phase-frequency
spectra of responses to clicks. Top panel: magnitude spectra. The continuous
line shows the variation of magnitude as a function of frequency for the
entire waveform ?6.4 ms? of averaged responses to 74-dB clicks in cochlea
L113 ?inset?. The other curves depict the magnitude-frequency spectra of the
waveform segments indicated in the inset ?A: 0–0.7 ms, short-dash line; B:
0–1.7 ms, dotted-line; C: 1.7–6.4 ms, long-dash line?. Bottom panel: phase
spectra. The continuous line indicates the variation of phase with frequency
for the entire waveform. The dotted and long-dash lines depicts phases for
segments B and C, respectively.
19801980J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
degrees. Thus, it is clear that the notch in the magnitude
spectrum was generated by a phase cancellation at the notch
frequency between response components in the two lobes.
Figure 12A also shows the amplitude spectrum of seg-
ment A ?short-dash line?, which indicates that most of the
low-frequency (?7 kHz? response components of the origi-
nal waveform are confined to the response onset ?consistent
with the analytic-signal representation and the short-term
Fourier transform: Fig. 5?.
G. Effects of death on basilar-membrane responses
Figure 14 illustrates the effects of death on responses to
clicks presented at 84 and 104 dB SPL. ?The scale for the
responses to 104-dB clicks is compressed by a factor of 10
?i.e., 20 dB? relative to the scale for responses to 84-dB
clicks. Therefore, response features that grew linearly have
identical magnitudes in the 84- and 104-dB traces.? When
the cochlea was healthy ?left column?, all but the earliest
peaks grew at highly compressive rates, so that wave shapes
were skewed toward earlier times and gains became smaller
as a function of increasing stimulus intensity. Post-mortem,
the amplitude of all but the earliest response peaks were
drastically reduced relative to the in vivo responses, with the
responses to the weaker stimuli being more strongly affected
?right column of Fig. 14; see also Figs. 7 and 8 of Ruggero
and Rich, 1991a, and Figs. 1 and 3 of Ruggero et al., 1992a?.
After death, responses grew almost linearly, so that re-
sponses at all stimulus levels resembled scaled versions of a
single wave shape, similar to that of in vivo responses to
intense clicks. However, post-mortem responses ?recorded
within 10–20 minutes after death? were not completely
stable and exhibited vestiges of nonlinearity ?note the late
oscillations in the traces of Fig. 14 and the post-mortem
magnitude spectra of Fig. 10?.
Post-mortem, the response gains ?thick lines in Fig. 10?
FIG. 13. The variation of response phase at the notch frequency ?10.23 kHz?
as a function of time. Phases were computed by Fourier transformation of
200-?s segments of the responses to clicks of cochlea L113, including the
waveform of the inset of Fig. 12A. The bracket indicates the times of the
transitions between the time-domain lobes ?see Fig. 3?.
FIG. 14. The effect of death on basilar-membrane responses to clicks. Responses to clicks, presented at 84 and 104 dB SPL, were recorded in vivo ?left
column? and about 10 minutes post-mortem ?right column?.
1981 1981J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
were reduced by 3–4 orders of magnitude at CF, relative to
in vivo responses to low-level clicks ?by 58–64 dB in L113
and 78–91 dB in L13?, the bandwidths were broadened and
the peaks of the gain spectra shifted down to frequencies
about 0.5 octave lower than CF. Post-mortem, the Q10’s
?peak frequency divided by bandwidth? were reduced to
1.12–1.21 ?L113? and 1.42–1.53 ?L13?. Overall, the post-
mortem gain spectra were very similar to ?but somewhat
lower than? the spectra of in vivo responses to intense ?104-
or 106-dB? clicks.
In relation to in vivo responses to low-level clicks, post-
mortem responses exhibited phase lags and leads, respec-
tively, at frequencies lower and higher than CF ?thick-dash
lines in Figs. 11 and 15B; see also Fig. 2 of Ruggero, 1994?.
Death abolished the phase jumps evident in vivo at near-CF
frequencies ?compare in vivo and post-mortem responses to
94-dB clicks in Figs. 11A and 15B?. The phase effects of
death could not be assessed with any precision at frequencies
higher than CF, at which responses were buried in the back-
H. Comparison of basilar-membrane responses to
clicks and tones
As described in the preceding sections, the features of
basilar-membrane responses to clicks varied systematically
as a function of time: ?1? the initial oscillation was nearly
linear, whereas later oscillation peaks grew at compressive
rates that waxed and waned as a function of time ?Figs. 7 and
8?; ?2? the instantaneous frequency increased ?Figs. 5–6 and
12A?; and ?3? the phases of near-CF components shifted by
nearly 180 degrees ?Figs. 12B and 13?. We investigated how
these time-varying features of basilar-membrane vibration
relate to steady-state behavior by recording responses to
tones and clicks in the same cochleae in close temporal prox-
Responses to clicks and tones were compared in the fre-
quency domain by plotting their gains and phases as a func-
tion of frequency and stimulus level ?Fig. 15?. There was an
excellent match between the gains ?Fig. 15A? of responses to
clicks ?replotted from Fig. 10? and to tones ?from Fig. 9 of
Ruggero et al., 1997? not only at low frequencies ?below
6–7 kHz?, where responses were linear, but also at frequen-
cies around CF, where responses were strongly compressive.
Figure 15A is representative of many other comparisons ?not
illustrated? in that they demonstrate a close correspondence
between the gains of basilar-membrane responses to tones
and clicks at the 3.5-mm site of the chinchilla cochlea ?see
also Fig. 3 of Ruggero et al., 1992a and Fig. 6 of Ruggero
et al., 1992b?. Such close correspondence was evident re-
gardless of the health of the cochlea and/or the strength of
the basilar-membrane nonlinearities and could be demon-
strated whenever responses to both types of stimulus ?click
or tones? were recorded over a wide range of stimulus inten-
sity. For the data of Fig. 15A, for example, the magnitude
spectrum of responses to clicks with peak pressure of 104 dB
matched accurately the magnitude of responses to 90-dB
tones; responses to 94-dB clicks matched responses to 80-dB
tones; and so on down to 24- and 34-dB clicks, which
matched responses to 10- and 20-dB tones. In other words,
over wide ranges of frequency and level, the spectrum of
responses to clicks presented at a given level predicted accu-
rately the responses to tones presented at a constant level.
Furthermore, once the appropriate correspondence was as-
certained for one click level ?for example: in the case of
cochlea L113, 60-dB tones corresponded to 74-dB clicks?,
all other levels were simultaneously determined.
Figures 11A and 15B allow comparison of the phases of
responses to clicks ?lines? and tones ?symbols? recorded in
the same cochlea. As in the case of the gain functions ?Fig.
15A?, there is a good match between the response phases for
the two types of stimulus for frequencies lower than CF. The
response phases for click and tone stimuli ?lines and sym-
bols, respectively, in Figs. 11A and 15B? vary as a function
of increasing stimulus intensity in a qualitatively similar
fashion. Phases tend to lag for frequencies ?e.g., 8.5–9 kHz?
lower than CF and to lead for frequencies ?e.g., 10.3–10.8
kHz? higher than CF. There is little phase variation at CF or
at frequencies lower than 5–6 kHz. Comparable matches be-
tween the phases of responses to tones and clicks were also
obtained for other cochleae ?not illustrated here; see Fig. 4 of
Ruggero et al., 1992a?.
A. Methodological considerations
In analyzing basilar-membrane recordings using laser
velocimetry, it is important to take into account an artifact
due to stapes-driven motion of the fluid meniscus overlying
the recording site ?Cooper and Rhode, 1992?. Such motion
changes the effective path length of the laser beam and mim-
ics the Doppler shifts due to basilar-membrane motion. The
artifact principally affects low-frequency measurements,
when ossicular motion is largest and basilar-membrane mo-
tion is small ?Cooper and Rhode, 1992; Ruggero et al.,
We were especially concerned that motion of the fluid
meniscus could introduce a spurious low-frequency oscilla-
tion, mimicking an early-onset basilar-membrane response to
clicks. To control for this possibility, basilar-membrane re-
sponses were measured in 6 cochleae before and after place-
ment of a small window ?made up of slide coverslip glass?
on the otic-capsule hole overlying the basilar-membrane re-
cording site, a procedure that diminishes the motion of the
fluid meniscus ?Cooper and Rhode, 1996?. ?For illustration
purposes, we present here responses to intense clicks, for
which near-CF basilar-membrane response gains are lowest
?e.g., Fig. 10? and therefore the effects of fluid-meniscus mo-
tion ?which grow linearly with stimulus intensity? are rela-
tively large. In the case of low-level stimulation, the effects
of fluid-meniscus motion are negligible.? The window al-
tered the recorded waveforms consistently ?Figs. 16–17?. In
5 of the 6 cochleae, the initial oscillation ?as usual, toward
scala vestibuli for rarefaction clicks? grew larger after place-
ment of the glass window ?e.g., Fig. 16, left panel?. In one
exceptional cochlea ?Fig. 16, right panel? the initial oscilla-
tion was originally negative and became positive after the
glass window was installed. Significantly, the onset delays
were only minimally changed. Placement of the glass win-
1982 1982 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998Recio et al.: Basilar-membrane responses to clicks
dow reduced the cochlear delays ?relative to the onset of
incus motion? from 43.0?21.1 ?s to 29.8?12.4 ?s ?mean
?s.d., N?6?. Cochlea L163 was exceptional in that the delay
increased, from 14 to 36 ?s.
The effects of covering the otic-capsule hole were espe-
cially obvious in the frequency domain ?Fig. 17?. The upper
panels of Fig. 17, depicting the magnitude spectra of the
waveforms of Fig. 16, show that the response components
above 2–3 kHz were largely unaltered but those at lower
frequencies decreased in magnitude by as much as 20 dB.
Correspondingly, after the placement of the window re-
sponse phases ?lower panel of Fig. 17? increasingly lagged
?by as much as 90 degrees? those measured with the open
otic capsule as the frequency decreased below 3–4 kHz.
These results indicate that fluid-meniscus motion typically
does not alter drastically the polarity, magnitude or onset
FIG. 15. Comparison of basilar-membrane responses to clicks ?curves? and tones ?symbols? recorded in the same cochlea. ?A? Gain-vs-frequency spectra as
a function of stimulus intensity. ?B? Phase-vs-frequency spectra as a function of stimulus intensity. At each level, the phases responses to clicks are expressed
relative to the phases of responses to 64-dB clicks. The phases of responses to tones are expressed relative to the phases of responses to 50-dB tones, whose
magnitudes closely matched the spectral responses to 64-dB clicks ?panel A?. Positive values indicate relative phase leads
1983 1983J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
time of the initial oscillation of responses to clicks, whose
dominant spectral components have frequencies higher than
2–3 kHz ?Figs. 5–6 and 12A?.
In the course of measuring responses to clicks at the
apex of the cochlea, Cooper and Rhode ?1996? found evi-
dence for another artifact, also related to the opening of the
otic capsule but still present after placement of a glass win-
dow. This artifact, which produced an initial oscillation last-
ing 1–1.5 ms and a spectral magnitude notch, was abolished
by restoring the hydraulic seal of the cochlea. ?In our prepa-
rations, placement of a glass window on the otic capsule hole
also failed to abolish the spectral notches ?not illustrated? but
increased the magnitude of the initial oscillation ?Fig. 16?.?
We did not attempt to fully restore the hydraulic seal and,
therefore, we cannot rule out that our measurements were
affected by a similar artifact. Nevertheless, we deem this an
unlikely possibility. The apical preparation of Cooper and
Rhode ?1996? involved opening scala vestibuli. In contrast,
in our preparation the cochlea is opened near its basal end,
overlying scala tympani. Although the round window does
influence pressure at nearby scala tympani sites ?Ned-
zelnitsky, 1980?, the differential pressure across the cochlear
partition is dominated by pressure in scala vestibuli, which
substantially exceeds that in scala tympani ?Dancer and
Franke, 1980; Nedzelnitsky, 1980?. The implication is that
opening a hole in the otic capsule near the round window
should not have significantly altered the differential pressure,
which is the driving force to basilar-membrane motion ?Voss
et al., 1996?.
B. Basilar-membrane responses to clicks at the base
of the chinchilla cochlea compared with
measurements in other species and other cochlear
The present results are generally consistent with the
main findings of the pioneering Mo ¨ssbauer study of Robles
et al. ?1976; Rhode and Robles, 1974? at a site of the squirrel
monkey cochlea with CF of 6–7.8 kHz. At that site, basilar-
membrane responses to clicks consisted of two segments.
The initial segment was of short duration, exhibited a rela-
tively low frequency of oscillation and grew linearly with
stimulus intensity. The second segment was a relatively un-
damped oscillation with frequency corresponding to CF,
which grew at compressive rates. Nonlinear growth of
basilar-membrane responses to clicks has also been demon-
strated at the base of the cochleae of chinchilla ?Ruggero
et al., 1992a,b? and guinea pig ?LePage and Johnstone, 1980;
de Boer and Nuttall, 1997?. Frequency modulation has been
described in basilar-membrane responses to clicks at the base
of the guinea-pig cochlea ?de Boer and Nuttall, 1997?. At the
base of the chinchilla cochlea, both the frequency of oscilla-
tion and the extent of the nonlinearity increase continuously
over several hundreds of microseconds ?Figs. 5–8?. The fre-
quency modulation is not abolished by death ?Fig. 6A? and,
therefore, must be viewed as a ‘‘passive’’ feature of both
linear and nonlinear basilar-membrane responses. Thus, it is
not surprising that frequency modulation can be mimicked
by some linear models of basilar-membrane vibration ?Nils-
son and Mo ”ller, 1977; Mo ”ller and Nilsson, 1979; Lyon,
1997; de Boer and Nuttall, 1997?.
Mechanical responses to clicks at the apex of guinea pig
cochleae grow linearly with stimulus intensity ?Cooper and
Rhode, 1996?. It is likely that the linearity of such responses
reflects surgically induced cochlear damage. Responses to
clicks at the apex of chinchilla cochleae do exhibit a mild
compressive nonlinearity, with output/input slopes no lower
than 0.76 dB/dB ?Cooper and Rhode, 1996?, which contrast
with slopes as low as 0.2 dB/dB at the cochlear base ?e.g.,
Figs. 7–8?. It is not clear whether this quantitative discrep-
ancy reflects greater surgical damage in apical preparations
or a genuine difference in the extent of nonlinearity between
the apex and the base of the cochlea. The latter possibility
FIG. 16. Basilar-membrane responses to clicks recorded in open and closed cochleae. The dashed and continuous lines, respectively, identify responses
recorded before and after covering the otic-capsule hole with a glass window. The clicks had peak pressures of 78 dB ?L157? and 92 dB ?L163?.
19841984 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998Recio et al.: Basilar-membrane responses to clicks
merits consideration because some properties of auditory-
nerve responses suggest, in fact, that compressive nonlinear-
ity is less salient in low-CF than in high-CF cochlear regions
?e.g., Cooper and Yates, 1994; Sewell, 1984; Temchin et al.,
Responses to clicks at the apex of the chinchilla cochlea
also differ from those at the base in that they apparently lack
a ?nearly? linear initial segment ?Cooper and Rhode, 1996?.
We suppose that this difference reflects the distinct manner
in which nonlinearities are distributed at the two recording
sites as a function of time and in the corresponding fre-
quency spectra. At basal locations, the initial ?almost linear?
oscillation has a spectral content heavily weighted by fre-
quencies well below CF ?Figs. 5–6?, at which responses
grow linearly, whereas nonlinear compressive growth is con-
fined to later oscillations ?Figs. 7–8? and to frequencies near
CF ?the ‘‘tip’’ of tuning curves; Fig. 11?. At apical locations,
compressive growth occurs over a wide frequency region ?so
that there is no distinction between nonlinear ‘‘tip’’ and lin-
ear ‘‘tail’’? and the spectral content of the initial oscillation
of responses to clicks falls within the frequency range of
nonlinear growth, which spans more than 3 octaves ?Rhode
and Cooper, 1996?.
C. Polarity and latency of the onset of basilar-
membrane responses to clicks
At the base of the chinchilla cochlea, the initial basilar-
membrane response to rarefaction clicks consists of motion
toward scala vestibuli ?Figs. 1–2, 4, and 16? and, appropri-
ately, responses to condensation clicks begin with motion
toward scala tympani ?Fig. 3?. Other investigations of
basilar-membrane responses to clicks at the cochlear base
?Rhode and Robles, 1974; Robles et al., 1976; LePage and
Johnstone, 1980; Nuttall and Dolan, 1993; de Boer and Nut-
tall, 1997? did not report the polarity of responses. At the
apex of chinchilla and guinea pig cochleae ?at locations ap-
proximately 14 and 16.5 mm, respectively, from the stapes?,
the responses to clicks ?recorded from the scala-media sur-
faces of Claudius cells, Hensen’s cells or the tectorial mem-
brane? contain a ‘‘fast’’ ?short-latency? component, which is
presumably artifactual ?see Discussion Section III A?, and a
‘‘slow’’ component, which begins as late as 1.5 ms after the
onset of ossicular motion ?Cooper and Rhode, 1996?. The
polarity of the onset oscillation of this slow component ?i.e.,
motion toward scala vestibuli for rarefaction clicks? is the
same as we found at the cochlear base. This suggests that the
same onset polarity holds throughout the cochlea.
At the 3.5-mm site of the chinchilla cochlea, basilar-
membrane responses to clicks begin approximately 30 ?s
after the onset of ossicular motion. This delay is smaller than
a previous preliminary estimate from our laboratory ?90 ?s;
Ruggero et al., 1992a?. The latter were not based on middle-
ear and basilar-membrane responses to clicks recorded in the
same ears and probably underestimated delays in the stimu-
Reports of responses to clicks at basal locations of
guinea pig cochleae ?LePage and Johnstone, 1980; Nuttall
and Dolan, 1993; de Boer and Nuttall, 1997? did not provide
estimates of onset delay. A cochlear delay of 300–390 ?s
was measured at a squirrel monkey basilar-membrane site
with CF of 6–7.8 kHz ?Robles et al., 1976?. According to a
CF-distance map proposed by Greenwood ?1990?, such CFs
correspond to a distance of 8.3–9.5 mm from the oval win-
dow. The difference between the delays at the 3.5-mm
basilar-membrane site of chinchilla and the 8.3–9.5-mm site
of squirrel monkey probably reflects the slowing down of the
basilar-membrane wave as it travels from base to apex.
D. Is there a traveling wave on the basilar membrane?
The mechanical responses to clicks at the base of the
chinchilla cochlea ?the present work?, at apical sites of the
guinea pig and chinchilla cochleae ?Cooper and Rhode,
1996?, as well as those at an intermediate cochlear location
in squirrel monkey ?Robles et al., 1976?, imply that there is a
progressive phase accumulation or increasing delay as a
function of distance from the oval window. Responses to
identical stimuli at closely spaced basilar-membrane loca-
tions in individual cochleae also show phase accumulation or
increasing delay as a function of distance from the oval win-
dow ?Rhode, 1971; Kohllo ¨ffel, 1972; Cooper and Rhode,
1996; Russell and Nilsen, 1997?. Thus, the bulk of the
basilar-membrane data on cochlear delays provide strong
FIG. 17. The effects on basilar-membrane responses to clicks of covering
the otic capsule hole with a glass window. Upper panels: magnitude-
frequency spectra of the responses of Fig. 16. Lower panel: phase effects.
Positive phases indicate leads relative to responses before placement of the
19851985 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
support for the classical view of the traveling wave ?von
Be ´ke ´sy, 1960?. Indirect estimates of traveling-wave delays
based on cochlear microphonic responses to low-frequency
tones ?Tasaki et al., 1952; Dallos and Cheatham, 1971;
Dancer et al., 1997? do not differ greatly from the latencies
of responses to clicks at the basilar membrane of squirrel
monkeys, chinchillas and guinea pigs ?Robles et al., 1976;
Cooper and Rhode, 1996, and the present work?. At sites
located about 4, 9 and 14 mm from the oval window in the
guinea pig cochlea, such delays amount to 25, 250 and 1000
?s, respectively ?Dancer et al., 1997?.
The latency of responses to clicks of auditory-nerve fi-
bers increases systematically as a function of decreasing CF
?Kiang et al., 1965; Kim and Molnar, 1979; Siegel et al.,
1982; Ruggero and Rich, 1983, 1987; Ruggero, 1992a?. In
the chinchilla, latencies for rarefaction clicks range from
about 1 ms for fibers with CFs higher than 3–4 kHz to about
2.7 ms for fibers with CF of 320 Hz ?Ruggero and Rich,
1983, 1987; Salvi et al., 1979?. If synaptic and neural delays
account for a 1-ms delay, regardless of CF ?discussed by
Ruggero and Rich, 1987?, the neural data imply that me-
chanical travel time is almost nil at basal cochlear locations
and 1.7 ms near the apex. These delays are fairly consistent
with those measured on the basilar membrane or the organ of
Corti at basal ?e.g., Fig. 1? and apical ?Cooper and Rhode,
1996? sites of the chinchilla cochlea.
Dancer has suggested that the basilar membrane does
not sustain a traveling wave ?Dancer, 1992; see also Dancer
et al., 1997?. He offered two main arguments. The first was
that the onset latencies of cochlear responses are shorter than
those predicted by Zwislocki’s ?1948? model of basilar-
membrane vibration. We do not view this quantitative dis-
crepancy between measurements and one particular math-
ematical model as evidence against the very existence of a
traveling wave. The onset latencies of basilar-membrane and
auditory-nerve responses to clicks increase systematically as
a function of distance from the oval window, as expected for
a mechanical wave that propagates from base to apex ?Rug-
gero, 1994?. Further, Zwislocki ?1974? has shown that his
model can be adjusted ?by increasing stiffness? to yield la-
tencies that closely match in vivo empirical data for the
guinea pig cochlea ?see his Fig. 5?. Dancer’s second argu-
ment was that the substantial phase accumulations exhibited
by basilar-membrane responses at near-CF frequencies
?equivalent to 1–2 CF periods at both basal and apical sites
of the chinchilla cochlea: the present work and Cooper and
Rhode, 1996? are due mostly to ‘‘active’’ cochlear processes
and should not be taken as evidence for the existence of a
?‘‘passive’’? traveling wave. Our data on the effects of death
on the phases of basilar-membrane responses clearly contra-
dict this argument: the phases of post-mortem responses are
fully within the range of those observed in vivo ?Figs. 11A
E. Nonlinear phase shifts in responses to clicks and
their relation to gain spectra
A striking aspect of the phases of post-mortem re-
sponses to clicks, as well as in vivo responses to intense
clicks, is that they did not differ substantially from in vivo
responses to low-level clicks. Although death, as well as in-
creases in click level in vivo, did cause phase changes ?and
abolished the phase jumps?, the changes ?Fig. 15B? were
small in comparison to the accumulated phase lags exhibited
by in vivo responses at CF, regardless of stimulus level. This
is somewhat paradoxical, in view of the substantial broaden-
ing of the bandwidth of response gain that accompanies ei-
ther death or increases in stimulus level in vivo ?Fig. 10?.
Since, in general, sharper frequency tuning requires longer
response delays ?Bode, 1946; Goldstein et al., 1971; Geisler
and Rhode, 1982?, the large increases in bandwidth observed
post-mortem ?or at intense click levels in vivo? might have
been expected to result in correspondingly large decreases of
phase lag or group delay at frequencies near CF. In fact, the
phases of post-mortem and in vivo responses to intense clicks
did not change at CF and group delays decreased by only
small amounts or not at all ?Figs. 11A and 15B?.
Basilar-membrane responses to clicks in healthy chin-
chilla cochleae often have two- ?or even multiple-? lobed
waveforms ?e.g., Figs. 2–4; also see Fig. 6 of Ruggero and
Rich, 1991a, and Fig. 6 of Ruggero et al., 1996? and their
spectra may include a notch ?e.g., Figs. 9, 10, and 12; also
see Fig. 9 of Ruggero et al., 1996?. Two-lobed mechanical
responses to clicks and/or spectral notches have also been
observed at a basal cochlear site in guinea pig ?Nuttall and
Dolan, 1993; de Boer and Nuttall, 1997? and at the apex of
guinea pig and chinchilla cochleae ?Cooper, 1997?.
At the base of the chinchilla the spectral notches arise
from cancellations due to phase opposition between same-
frequency components in the ?time-domain? lobes of the re-
sponses to clicks ?Figs. 12 and 13?. The phase modulation of
basilar-membrane responses to clicks may be related to the
asymmetry of their magnitude spectra, given that the impulse
responses of asymmetrical filters generally exhibit such
modulation ?Papoulis, 1977, p. 123?. However, the origin of
the notches and the underlying phase modulation is obscure
and we are uncertain about their significance. We doubt that
they are solely artifacts ?e.g., due to opening the otic capsule:
Cooper, 1997; see Section III A of Discussion?, since such
artifacts should be relatively invulnerable to physiological
deterioration and should exhibit linear properties. In contrast,
notches and phase shifts were present only in sensitive co-
chleae, at or near CF at certain stimulus levels ?i.e., their
presence was CF-specific and intensity dependent? and dis-
appeared postmortem. All these features indicate that the
phase modulation and associated notches are linked to non-
linear and physiologically vulnerable processes. Most impor-
tantly, the notches occurred at levels at which response
growth was highly compressive ?see Fig. 7, L113?, thus rul-
ing out such linear artifacts as motion of the fluid-meniscus
?see Section A of Discussion?. However, we cannot rule out
that these phenomena arise from an interaction between co-
chlear nonlinearities and stimulus artifacts ?such as ringing
in the acoustic click waveform?.
19861986 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998Recio et al.: Basilar-membrane responses to clicks
F. Interpretation of the close resemblance between
basilar-membrane responses to tones and
clicks: Linearlike correspondences in spite of
Robles et al. ?1976? noted that at the basilar membrane
of the squirrel monkey, responses to clicks could be mim-
icked to a fair extent by a Fourier synthesis based on
magnitude-vs-frequency spectra measured with tones and de-
rived phase-vs-frequency functions ?computed from the
magnitude data on the assumption of minimum-phase behav-
ior?. Our present findings show that, indeed, basilar-
membrane responses to clicks and tones are generally well
matched ?Fig. 15; see also Figs. 3 and 4 of Ruggero et al.,
1992a, and Fig. 6 of Ruggero et al., 1992b?, so that re-
sponses to tones can be predicted, with good accuracy, from
responses to clicks, and vice versa.
It seems remarkable that reasonably accurate cross-
stimulus predictions are possible for such a highly nonlinear
system as the one underlying basilar-membrane vibration at
the base of the cochlea. We surmise that the system proper-
ties that make such predictions possible are the same that
severely restrict the prominence of basilar-membrane har-
monic distortion and other nonlinearities, especially when
stimulation is confined to a single spectral level ?e.g., Evans,
1989; de Boer and Kruidenier, 1990; Zwislocki et al., 1997?.
?1? The magnitude- and phase-frequency spectra of re-
sponses to a given type of stimulus ?click or tone? presented
at any one level accurately predicts responses to the other
type of stimulus only at a single, specific level. In the case of
Fig. 15A, for example, responses to 54-dB clicks predict
accurately the magnitudes of responses to 40-dB tones but
grossly overestimate the responses to 70-dB tones. ?2?
Basilar-membrane responses to single tones at the base of the
cochlea exhibit no dc components ?Cooper and Rhode, 1992?
and contain little ?perhaps negligible? harmonic distortion
?Cooper and Rhode, 1992; Ruggero et al., 1992c, 1997?. ?3?
Responses to white noise can be accurately predicted by
first-order Wiener kernels ?Recio et al., 1996, 1997?. ?4? The
magnitude of odd-order distortion products elicited by pairs
of equal-level tones rarely exceeds 10% of the responses to
the primary tones ?Robles et al., 1991, 1997; Nuttall et al.,
1990; Rhode and Cooper, 1993?.
G. Frequency modulation, the extent of nonlinearity
as a function of time, and the speed of the
Nonlinear compressive growth at the 3.5-mm site of the
chinchilla basilar membrane is evident within 100 ?s states
of response onset ?Figs. 6 and 8?. By implication, the organ
of Corti feedback that boosts basilar membrane vibrations
?‘‘the cochlear amplifier’’? starts its operation within 1 CF
period following the arrival of the traveling wave at the re-
cording site. The strength of the feedback ?as indicated by
the magnitude of compressive nonlinearity? varies signifi-
cantly as a function of time, increasing rapidly from a mini-
mum at onset to a maximum 1–1.6 ms later but waxing and
waning thereafter ?Fig. 8?. One plausible interpretation of the
initial variation is that the feedback is tuned to CF and thus
merely follows the ‘‘passive’’ frequency glide, which is
present both in vivo and post-mortem ?Figs. 5 and 6?. Taking
the frequency glide into account, the onset of nonlinearity
appears to be an almost instantaneous response to the CF
spectral components of the ‘‘passive’’ vibrations.
However, the time course of the frequency glide cannot
fully account for the time course of the compressive nonlin-
earity. The frequency glide consists of a roughly monotonic
saturating-exponential increase, whereas the magnitude of
the compressive nonlinearity undergoes waxing and waning,
with compression minima ?i.e., slope maxima? corresponding
approximately to the wave shape constrictions. The nearly
synchronous occurrence of the constrictions and the com-
pression minima suggests that response sensitivity and non-
linear growth are tightly linked, which is consistent with the
operation of a ?nearly? instantaneous nonlinear ‘‘cochlear
H. Comparison between responses to clicks at the
basilar membrane and auditory-nerve responses
to clicks and noise
The responses to clicks of the basilar-membrane site
with CF of 9–10 kHz cannot be compared in any detail with
those of auditory-nerve fibers with similar CFs because such
neurons do not phase lock at near-CF frequencies. Except for
rectification ?presumably due to synaptic processes?, the re-
sponses to clicks of low-CF neurons resemble qualitatively
the high-CF basilar-membrane responses in several respects.
First, low-CF auditory-nerve fibers respond to rarefaction
clicks with shorter latencies ?by about 1/?2*CF?? than to con-
densation clicks ?Kiang et al., 1965; Goblick and Pfeiffer,
1969; Pfeiffer and Kim, 1972; Kim and Molnar, 1979; Siegel
et al., 1982; Ruggero and Rich, 1983, 1987?. This is consis-
tent with the onset polarity of basilar membrane responses
?the present work and Cooper and Rhode, 1996? on the as-
sumption that, in apical cochlear regions, auditory-nerve ex-
citation occurs when the basilar membrane is deflected or in
motion toward scala vestibuli ?Ruggero and Rich, 1983,
1987?. Second, neural responses exhibit nonlinear properties
reminiscent of those at the basilar membrane, including a
skew of their envelope toward earlier times as a function of
increasing stimulus intensity ?e.g., Kiang et al., 1965; Pfe-
iffer and Kim, 1972? and an amplitude nonlinearity in re-
sponses to paired clicks ?Goblick and Pfeiffer, 1969?. This
amplitude nonlinearity may reflect directly the nonlinear
growth of responses at the basilar membrane. The envelope
skew, on the other hand, probably reflects mixed contribu-
tions from both basilar-membrane nonlinearities ?Figs. 2–4,
7 and 8? and neural and synaptic processes ?e.g., Gray, 1967;
Schoonhoven et al., 1994?. Third, the responses to clicks of
7% of low-CF fibers exhibit lobes reminiscent of those ?Figs.
3 and 4? characterizing basilar-membrane responses at the
cochlear base ?Pfeiffer and Kim, 1972?. However, it is puz-
zling that such lobes should be only present in a small mi-
nority of fiber responses, if in fact they reflect basilar-
Revcors ?de Boer, 1967; de Boer and de Jongh, 1978?
for responses to noise of low-CF auditory-nerve fibers re-
semble basilar-membrane responses to clicks even more
closely than do auditory-nerve fiber responses to clicks. This
19871987J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
is because the first-order cross-correlation between the spike
train and the noise stimulus removes rectification and other
even-order nonlinearities, which are largely ?but not entirely:
Rhode and Cooper, 1996? of synaptic and/or neural origin
?Recio et al., 1996, 1997?. Revcors of neural responses to
noise ?Mo ”ller and Nilsson, 1979? exhibit a frequency modu-
lation very much like that seen in basilar-membrane re-
sponses ?Figs. 5–6?. They also show a deterioration of fre-
quency tuning and a spectral shift toward lower frequencies
with increasing stimulus intensity ?Evans, 1977; de Boer and
de Jongh, 1978; Mo ”ller, 1978?. Again, it is likely that these
nonlinearities reflect both basilar-membrane and more cen-
tral ?synaptic and neural? contributions.
Many thanks to Andrei Temchin for help in the prepa-
ration of figures and to Mary Ann Cheatham, Peter Dallos,
Luis Robles and especially Nigel Cooper for their comments
on previous drafts of this paper. We were supported by
Grants Nos. 5-P01-DC-00110-23 and 2-R01-DC-00419-10
from the National Institute on Deafness and Other Commu-
Be ´ke ´sy, G. von ?1960?. Experiments in Hearing ?McGraw-Hill, New York?.
Bennett, W. R. ?1970?. Introduction to Signal Transmission ?McGraw-Hill,
Bode, H. W. ?1946?. Network Analysis and Feedback Amplifier Design ?Van
Nostrand, New York?.
Cooper, N. P. ?1997?. ‘‘Mid-band sensitivity notches in apical cochlear me-
chanics,’’ in Diversity in Auditory Mechanics, edited by E. R. Lewis, G.
R. Long, R. F. Lyon, P. M. Narins, C. R. Steele, and E. Hecht-Poinar
?World Scientific, Singapore?, pp. 298–304.
Cooper, N. P., and Rhode, W. S. ?1992?. ‘‘Basilar membrane mechanics in
the hook region of cat and guinea-pig cochleae: Sharp tuning and nonlin-
earity in the absence of baseline position shifts,’’ Hearing Res. 63, 163–
Cooper, N. P., and Rhode, W. S. ?1996?. ‘‘Fast travelling waves, slow trav-
elling waves and their interactions in experimental studies of apical co-
chlear mechanics,’’ Aud. Neurosci. 2, 289–299.
Cooper, N. P., and Yates, G. K. ?1994?. ‘‘Nonlinear impact-output functions
derived from the responses of guinea-pig cochlear nerve fibres: Variations
with characteristic frequency,’’ Hearing Res. 78, 221–234.
Dallos, P., and Cheatham, M. A. ?1971?. ‘‘Travel time in the cochlea and its
determination from cochlear-microphonic data,’’ J. Acoust. Soc. Am. 49,
Dancer, A. ?1992?. ‘‘Experimental look at cochlear mechanics,’’ Audiology
Dancer, A., and Franke, R. ?1980?. ‘‘Intracochlear sound pressure measure-
ments in guinea pigs,’’ Hearing Res. 2, 191–205.
Dancer, A., Avan, P., and Magnan, P. ?1997?. ‘‘Can the travelling wave be
challenged by direct intracochlear pressure measurements?’’ in Diversity
in Auditory Mechanics, edited by E. R. Lewis, G. R. Long, R. F. Lyon, P.
M. Narins, C. R. Steele, and E. Hecht-Poinar ?World Scientific, Sin-
gapore?, pp. 340–346.
de Boer, E. ?1967?. ‘‘Correlation studies applied to the frequency resolution
of the cochlea,’’ J. Aud. Res. 7, 209–217.
de Boer, E., and de Jongh, H. R. ?1978?. ‘‘On cochlear encoding: Potenti-
alities and limitations of the reverse-correlation technique,’’ J. Acoust.
Soc. Am. 63, 115–135.
de Boer, E., and Kruidenier, C. ?1990?. ‘‘On ringing limits of the auditory
periphery,’’ Biol. Cybern. 63, 433–442.
de Boer, E., and Nuttall, A. L. ?1997?. ‘‘The mechanical waveform of the
basilar membrane. I. Frequency modulations ?‘glides’? in impulse re-
sponses and cross-correlation functions,’’ J. Acoust. Soc. Am. 101, 3583–
Evans, E. F. ?1977?. ‘‘Frequency selectivity at high signal levels of single
units in cochlear nerve and nucleus,’’ in Psychophysics and Physiology of
Hearing, edited by E. F. Evans and J. P. Wilson ?Academic, London?, pp.
Evans, E. F. ?1989?. ‘‘Cochlear filtering: A view seen through the temporal
discharge patterns of single cochlear nerve fibers,’’ in Cochlear Mecha-
nisms: Structure, Function and Models, edited by J. P. Wilson and D. T.
Kemp ?Plenum, New York?, pp. 241–250.
Geisler, C. D., and Rhode, W. S. ?1982?. ‘‘The phases of basilar-membrane
vibrations,’’ J. Acoust. Soc. Am. 71, 1201–1203.
Goblick, Jr., T. J., and Pfeiffer, R. R. ?1969?. ‘‘Time-domain measurements
of cochlear nonlinearities using combination click stimuli,’’ J. Acoust.
Soc. Am. 46, 924–938.
Goldstein, J. L., Baer, T., and Kiang N. Y.-S ?1971?. ‘‘A theoretical treat-
ment of latency, group delay and tuning characteristics for auditory nerve
responses to clicks and tones,’’ in The Physiology of the Auditory System,
edited by M. B. Sachs ?National Educational Consultants, Baltimore,
MD?, pp. 133–141.
Gray, P. R. ?1967?. ‘‘Conditional probability analyses of the spike activity
of single neurons,’’ Biophys. J. 7, 759–777.
Greenwood, D. D. ?1990?. ‘‘A cochlear frequency-position function for sev-
eral species—29 years later,’’ J. Acoust. Soc. Am. 87, 2592–2605.
Kiang, N. Y.-S., Watanabe, T., Thomas, C., and Clark, L. F. ?1965?. Dis-
charge Patterns of Single Fibers in the Cat’s Auditory Nerve ?MIT, Cam-
Kim, D. O., and Molnar, C. E. ?1979?. ‘‘A population study of cochlear
nerve fibers: comparison of spatial distributions of average-rate and phase-
locking measures of responses to single tones,’’ J. Neurophysiol. 42, 16–
Kohllo ¨ffel, L. U. E. ?1972?. ‘‘A study of basilar membrane vibrations. II.
The vibratory amplitude and phase pattern along the basilar membrane
?post-mortem?,’’ Acustica 27, 66–81.
LePage, E. L., and Johnstone, B. M. ?1980?. ‘‘Nonlinear mechanical behav-
iour of the basilar membrane in the basal turn of the guinea pig cochlea,’’
Hearing Res. 2, 183–189.
Lyon, R. F. ?1997?. ‘‘All-pole auditory filter models,’’ in Diversity in Au-
ditory Mechanics, edited by E. R. Lewis, G. R. Long, R. F. Lyon, P. M.
Narins, C. R. Steele, and E. Hecht-Poinar ?World Scientific, Singapore?,
Mo ”ller, A. R. ?1978?. ‘‘Responses of auditory nerve fibres to noise stimuli
show cochlear nonlinearities,’’ Acta Oto-Laryngol. 86, 1–8.
Mo ”ller, A. R., and Nilsson, H. G. ?1979?. ‘‘Inner ear impulse response and
basilar membrane modelling,’’ Acustica 41, 258–262.
Nedzelnitsky, V. ?1980?. ‘‘Sound pressures in the basal turn of the cat co-
chlea,’’ J. Acoust. Soc. Am. 68, 1676–1689.
Nilsson, H. G., and Mo ”ller, A. R. ?1977?. ‘‘Linear and nonlinear models of
the basilar membrane motion,’’ Biol. Cybernet. 27, 107.
Nuttall, A. L., and Dolan, D. F. ?1993?. ‘‘Basilar membrane velocity re-
sponses to acoustic and intracochlear electric stimuli,’’ in Biophysics of
Hair Cell Sensory Systems, edited by H. Duifhuis, J. W. Horst, P. van
Dijk, and S. M. van Netten ?World Scientific, Singapore?, pp. 288–294.
Nuttall, A. L., and Dolan, D. F. ?1996?. ‘‘Steady-state sinusoidal velocity
responses of the basilar membrane in guinea pig,’’ J. Acoust. Soc. Am. 99,
Nuttall, A. L., Dolan, A. F., and Avinash, G. ?1990?. ‘‘Measurements of
basilar membrane tuning and distortion with laser Dopler velocimetry,’’ in
The Mechanics and Biophysics of Hearing, edited by P. Dallos, C. D.
Geisler, J. W. Matthews, M. A. Ruggero, and C. R. Steele ?Springer-
Verlag, Berlin?, pp. 288–295.
Papoulis, A. ?1977?. Signal Analysis ?McGraw-Hill, New York?.
Patuzzi, R. ?1996?. ‘‘Cochlear micromechanics and macro mechanics,’’ in
The Cochlea, edited by P. Dallos, A. N. Popper, and R. R. Fay ?Springer-
Verlag, New York?, pp. 186–257.
Pfeiffer, R. R., and Kim, D. O. ?1972?. ‘‘Response patterns of single co-
chlear nerve fibers to clock stimuli: Descriptions for cat,’’ J. Acoust. Soc.
Am. 52, 1669–1677.
Recio, A., Narayan, S. S., and Ruggero, M. A. ?1996?. ‘‘Wiener-kernel
analysis of basilar membrane responses to noise,’’ ARO Mid-Winter
Meeting Abstract 19, 55.
Recio, A., Narayan, S. S., and Ruggero, M. A. ?1997?. ‘‘Wiener-kernel
analysis of basilar-membrane responses to white noise,’’ in Diversity in
Auditory Mechanics, edited by E. R. Lewis, G. R. Long, R. F. Lyon, P. M.
Narins, C. R. Steele, and E. Hecht-Poinar ?World Scientific, Singapore?,
1988 1988J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998 Recio et al.: Basilar-membrane responses to clicks
Rhode, W. S. ?1971?. ‘‘Observations of the vibration of the basilar mem- Download full-text
brane in squirrel monkeys using the Mo ¨ssbauer technique,’’ J. Acoust.
Soc. Am. 49, 1218–1231.
Rhode, W. S., and Cooper, N. P. ?1993?. ‘‘Two-tone suppression and dis-
tortion production on the basilar membrane in the hook region of cat and
guinea pig cochlea,’’ Hearing Res. 66, 31–45.
Rhode, W. S., and Cooper, N. P. ?1996?. ‘‘Nonlinear mechanics in the apical
turn of the chinchilla cochlea in vivo,’’ Aud. Neurosci. 3, 101–121.
Rhode, W. S., and Robles, L. ?1974?. ‘‘Evidence from Mo ¨ssbauer experi-
ments for nonlinear vibration in the cochlea,’’ J. Acoust. Soc. Am. 55,
Robles, L., Rhode, W. S., and Geisler, C. D. ?1976?. ‘‘Transient response of
the basilar membrane measured in squirrel monkey using the Mo ¨ssbauer
effect,’’ J. Acoust. Soc. Am. 59, 926–939.
Robles, L., Ruggero, M. A., and Rich, N. C. ?1986?. ‘‘Basilar membrane
mechanics at the base of the chinchilla cochlea. I. Input–output functions,
tuning curves and response phases,’’ J. Acoust. Soc. Am. 80, 1364–1374.
Robles, L., Ruggero, M. A., and Rich, N. C. ?1991?. ‘‘Two-tone distortion in
the basilar membrane of the cochlea,’’ Nature ?London? 349, 413–414.
Robles, L., Ruggero, M. A., and Rich, N. C. ?1997?. ‘‘Two-tone distortion
on the basilar membrane of the chinchilla cochlea,’’ J. Neurophysiol. 77,
Ruggero, M. A. ?1992a?. ‘‘Physiology and coding of sound in the auditory
nerve,’’ in The Mammalian Auditory Pathway: Neurophysiology, edited
by A. N. Popper and R. R. Fay ?Springer-Verlag, New York?, pp. 34–93.
Ruggero, M. A. ?1992b?. ‘‘Responses to sound of the basilar membrane of
the mammalian cochlea,’’ Current Opinion in Neurobiology 2, 449–456.
Ruggero, M. A. ?1994?. ‘‘Cochlear delays and traveling waves: Comments
on ‘Experimental look at cochlear mechanics’ ?A. Dancer, Audiology
1992, 31: 301–312?,’’ Audiology 33, 131–142.
Ruggero, M. A., and Rich, N. C. ?1983?. ‘‘Chinchilla auditory nerve re-
sponses to low-frequency tones,’’ J. Acoust. Soc. Am. 73, 2096–2108.
Ruggero, M. A., and Rich, N. C. ?1987?. ‘‘Timing of spike initiation in
cochlear afferents: Dependence on site of innervation,’’ J. Neurophysiol.
Ruggero, M. A., and Rich, N. C. ?1990?. ‘‘Systematic injection of furo-
semide alters the mechanical response to sound of the basilar membrane,’’
in The Mechanics and Biophysics of Hearing, edited by P. Dallos, C. D.
Geisler, J. W. Matthews, M. A. Ruggero, and C. R. Steele ?Springer-
Verlag, Berlin?, pp. 314–321.
Ruggero, M. A., and Rich, N. C. ?1991a?. ‘‘Application of a commercially-
manufactured Doppler-shift laser velocimeter to the measurement of
basilar-membrane vibrations,’’ Hearing Res. 51, 215–230.
Ruggero, M. A., and Rich, N. C. ?1991b?. ‘‘Furosemide alters organ of Corti
mechanics: Evidence for feedback of outer hair cells upon the basilar
membrane,’’ J. Neurosci. 11, 1057–1067.
Ruggero, M. A., Rich, N. C., Robles, L., and Shivapuja, B. G. ?1990?.
‘‘Middle ear response in the chinchilla and its relationship to mechanics at
the base of the cochlea,’’ J. Acoust. Soc. Am. 87, 1612–1629.
Ruggero, M. A., Rich, N. C., and Recio, A. ?1991?. ‘‘Responses to clicks of
the chinchilla basilar membrane,’’ Soc. Neurosci. Abst. 17, 1106.
Ruggero, M. A., Rich, N. C., and Recio, A. ?1992a?. ‘‘Basilar membrane
responses to clicks,’’ in Auditory Physiology and Perception, edited by Y.
Cazals, L. Demany, and K. Horner ?Pergamon, London?, pp. 85–91.
Ruggero, M. A., Robles, L., Rich, N. C., and Recio, A. ?1992b?. ‘‘Basilar
membrane responses to two-tone and broadband stimuli,’’ Philos. Trans.
R. Soc. London, Ser. B 336, 307–315.
Ruggero, M. A., Robles, L., and Rich, N. C. ?1992c?. ‘‘Two-tone suppres-
sion in the basilar membrane of the cochlea: Mechanical basis of auditory-
nerve rate suppression,’’ J. Neurophysiol. 68, 1087–1099.
Ruggero, M. A., Rich, N. C., and Recio, A. ?1993?. ‘‘Alteration of basilar
membrane responses to sound by acoustic overstimulation,’’ in Biophysics
of Hair Cell Sensory Systems, edited by H. Duifhuis, J. W. Horst, P. van
Dijk, and S. M. van Netten ?World Scientific, Singapore?, pp. 258–264.
Ruggero, M. A., Rich, N. C., and Recio, A. ?1996?. ‘‘The effect of intense
acoustic stimulation on basilar-membrane vibrations,’’ Aud. Neurosci. 2,
Ruggero, M. A., Rich, N. C., Recio, A., Narayan, S. S., and Robles, L.
?1997?. ‘‘Basilar-membrane responses to tones at the ase of the chinchilla
cochlea,’’ J. Acoust. Soc. Am. 101, 2151–2163.
Russell, I. J., and Nilsen, K. E. ?1997?. ‘‘The location of the cochlear am-
plifier: Spatial representation of a single tone on the guinea pig basilar
membrane,’’ Proc. Natl. Acad. Sci. USA 94, 2660–2664.
Salvi, R. J., Henderson, D., and Hamernik, R. P. ?1979?. ‘‘Single auditory-
nerve fiber and action potential latencies in normal and noise-treated chin-
chillas,’’ Hearing Res. 1, 237–251.
Schoonhoven, R., Keijzer, J., Versnel, H., and Prijs, V. F. ?1994?. ‘‘A dual
filter model describing single-fiber responses to clicks in the normal and
noise-damaged cochlea,’’ J. Acoust. Soc. Am. 95, 2104–2121.
Sellick, P. M., Patuzzi, R., and Johnstone, B. M. ?1982?. ‘‘Measurement of
basilar membrane motion in the guinea pig using the Mo ¨ssbauer tech-
nique,’’ J. Acoust. Soc. Am. 72, 131–141.
Sewell, W. F. ?1984?. ‘‘The effects of furosemide on the endocochlear po-
tential and auditory-nerve fiber tuning,’’ Hearing Res. 15, 69–72.
Siegel, J. H., Kim, D. O., and Molnar, C. E. ?1982?. ‘‘Effects of altering
organ of Corti on cochlear distortion products f2-f1 and 2f1-f2,’’ J.
Neurophysiol. 47, 303–328.
Tasaki, I., Davis, H., and Legouix, J.-P. ?1952?. ‘‘The space-time pattern of
the cochlear microphonics ?guinea pig? as recorded by differential elec-
trodes,’’ J. Acoust. Soc. Am. 24, 502–519.
Temchin, A. N., Rich, N. C., and Ruggero, M. A. ?1997?. ‘‘Low-frequency
suppression of auditory-nerve responses to characteristic-frequency
tones,’’ Hearing Res. 113, 29–56.
Voss, S. E., Rosowski, J. J., and Peake, W. T. ?1996?. ‘‘Is the pressure
difference between the oval and round windows the effective acoustic
stimulus for the cochlea?’’ J. Acoust. Soc. Am. 100, 1602–1616.
Zwislocki, J. J. ?1948?. ‘‘Theorie der Schneckenmechanik: Qualitative and
Quantitative Analyse,’’ Acta Oto-Laryngol. Suppl. 72, 1–76.
Zwislocki, J. J. ?1974?. ‘‘Cochlear waves: Interaction between theory and
experiments,’’ J. Acoust. Soc. Am. 55, 578–583.
Zwislocki, J. J., Szymko, Y., and Hertig, L. Y. ?1997?. ‘‘The cochlea is an
automatic gain control system after all,’’ in Diversity in Auditory Mechan-
ics, edited by E. R. Lewis, G. R. Long, R. F. Lyon, P. M. Narins, C. R.
Steele, and E. Hecht-Poinar ?World Scientific, Singapore?, pp. 354–360.
1989 1989 J. Acoust. Soc. Am., Vol. 103, No. 4, April 1998Recio et al.: Basilar-membrane responses to clicks