Microstimulation of auditory nerve for estimating cochlear place of single fibers in a deaf ear

Hearing Research 113 (1997) 140^154

Microstimulation of auditory nerve for estimating cochlear place of single ¢bers in a deaf ear C. van den Honert a *, C.C. Finley a , S. Xue ;

a

b

Center for Auditory Prosthesis Research, Research Triangle Institute, P.O. Box 12194, Research Triangle Park, NC 27009, USA

b

Department of Physics, Cook Physical Science Building, University of Vermont, Burlington, VT 05405, USA

Received 30 November 1996; revised 30 May 1997; accepted 25 July 1997

Abstract

Multielectrode cochlear prostheses seek to approximate the cochlea's normal frequency-place mapping through spatial segregation of stimulus currents. Various electrode configurations have been employed to achieve such segregation. Direct measurements of stimulation regions among single auditory nerve (AN) fibers has been possible only when normal hearing is preserved, such that each fiber's cochlear place can be inferred from its tuning curve. This precludes measurements in deafened ears, or ears compromised by implantation of the electrodes. Data presented here demonstrate that the cochlear place of an AN fiber can be estimated without acoustic sensitivity, using electrical microstimulation through a recording pipette in the AN bundle. The procedure exploits cochleotopic projection to isofrequency laminae within the contralateral inferior colliculus (IC). Microstimulation excites a small group of fibers neighboring the recorded fiber, generating centrally propagated volleys along a narrow frequencyspecific pathway. Evoked potential recordings at varying depths are made to identify the ICC lamina where the response to AN microstimulation is greatest. Preliminary data are also presented for an alternative method of identifying the lamina using a frequency domain measure of binaural interactions within the IC. Keywords :

tuning

Cochlear implant; Single unit; Cochlear place; Characteristic frequency; Tuning curve; Intermodulation; Spatial

1. Introduction

Multielectrode cochlear prostheses use electrical stimulation of auditory nerve (AN) ¢bers through arrays of electrodes to provide sound sensations to the profoundly deaf. A variety of electrode geometries have been developed with the aim of recreating the normal tonotopy of auditory nerve responses using multiple stimulation sites. This basic strategy is predicated upon the idea that excitation of nerve ¢bers innervating di¡erent cochlear locations can be independently controlled by spatial segregation of stimulating currents. Although this fundamental principle is well established, many questions remain about how much

* Corresponding author. Tel.: +1 (919) 541-5822; Fax: +1 (919) 541-6221.

spatial segregation of stimulating currents is necessary and how it can be best achieved and utilized. Historically it has been considered desirable to maximize spatial resolution by producing narrow, non-overlapping regions of excitation within tonotopically discrete groups of auditory nerve ¢bers. Various electrode con¢gurations have been considered to achieve this objective, including individual monopoles in close proximity to the ¢bers (Simmons, 1966 ; Simmons et al., 1979), intrascalar monopoles (Eddington et al., 1978 ; Chouard and MacLeod, 1976 ; House and Urban, 1973), extracochlear monopoles (Banfai et al., 1985), intrascalar dipoles with various orientations (Merzenich et al., 1979 ; Hochmair-Desoyer and Hochmair, 1980 ; Black et al., 1981; Byers et al., 1987), and multipolar arrays employing ¢eld focusing (Van Compernolle, 1985; Rodenhiser and Spelman, 1995). However, psychophysical data suggest that even relatively broad overlapping re-

0378-5955 / 97 / $17.00 ß 1997 Elsevier Science B.V. All rights reserved PII S 0 3 7 8 - 5 9 5 5 ( 9 7 ) 0 0 1 3 2 - 9

HEARES 2887 28-11-97

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

141

gions of excitation are discriminable when stimulated

estimate of place would be of great value, even if it

non-simultaneously

et

provided only relative or imprecise values. The ability

has been

to identify even approximate locations of recorded ¢-

al.,

1978).

achieved sites,

(Shannon,

And good speech

with

either

systems

that

stimulate

simultaneously

non-simultaneously

1983a,b ;

(Tyler

(Wilson

Eddington

understanding

et

al.,

as

et

few

al.,

1991 ;

as

four

1995),

Dorman

bers would signi¢cantly improve our ability to assess

or

the

spatial

et

the

cochlea.

patterning The

of

electrical

stimulation

studies

reported

here

within

represent

the

development of a method which provides more than

al., 1996) in order to reduce channel interactions. Unfortunately, relatively few data are available re-

adequate

resolution

and

accuracy

for

this

purpose.

garding the spatial patterns of auditory nerve excitation

The method provides an estimate of absolute cochlear

actually produced by various electrode con¢gurations.

place if hearing is preserved in the non-experimental

Merzenich and White (1977) estimated cochlear excita-

ear, or relative place in a bilaterally deafened animal.

tion regions by recording from binaural neurons in the

Preliminary data are also presented for an alternative

central

method which has potential for signi¢cantly greater res-

nucleus

of

stimulating

the

electrodes.

They

cat

inferior

contralateral plotted

colliculus

cochlea

electrical

(ICC)

with

while

intrascalar

threshold

for

olution and immunity from electrical artifact.

ICC

units as a function of best frequency (measured with tones

to

the

normal

ipsilateral

ear),

and

concluded

2. Methods

that radial bipolar electrodes produced greater spatial selectivity in the cochlea than monopoles. Snyder et al.

2.1. Overview of microstimulation for place estimation

(1990) have made similar measures in bilaterally deafened animals using ICC depth as an analog of the fre-

The approach presented here depends upon two ba-

quency axis. van den Honert and Stypulkowski (1987)

sic premises. The ¢rst premise is that after recording

constructed similar plots of electrical threshold vs. char-

from a single AN ¢ber, a weak electrical current can

acteristic frequency (CF) measured from ¢bers of the

be applied through

auditory nerve itself. Their preparation preserved hear-

excite a relatively small population of neighboring ¢-

ing in the implanted ear such that cochlear place could

bers. The intent is to stimulate a su¤ciently small re-

be

gion in the vicinity of the recorded ¢ber that most of

inferred

from

traditional

acoustic

tuning

curves.

order

dipoles, and the greatest selectivity with radial dipoles.

quency region. This depends upon the tonotopic organ-

Their approach su¡ers three signi¢cant disadvantages

ization of the auditory nerve bundle. Although the fre-

because it requires normal hearing in the experimental

quency

ear :

of

boundary is less systematic than within the cochlea (Ar-

electrical stimuli (low repetition rate pulses) for which

nesen and Osen, 1978), results presented below indicate

electrophonically elicited spikes (Moxon, 1965) can be

that su¤cient tonotopy is preserved to make this objec-

unambiguously excluded ; (2) it cannot be used in deaf-

tive practical. The stimulated region might also span a

ened preparations (acute or chronic) ; and (3) it cannot

fascicular boundary in the spirally organized bundle,

be used when implantation of an intracochlear electrode

activating two ¢ber groups from widely disparate coch-

array

basilar membrane tuning.

lear locations. The consequences of this possible com-

Hartmann and Klinke (1990) adopted the converse ap-

plication are discussed below. It should be noted that

proach of measuring responses from one neuron while

the intimate contact required for recording from a ¢ber

can

be

used

only

compromises normal

with

a

limited

class

organization

not

of

AN

near

its

the

small

fre-

intracranial

need

long as the microelectrode is not moved it will remain

preferentially

within

particular

electrode

(or

pair),

but

the

same

during

single

method it is possible to identify neurons which respond a

maintained

the

a

varying the location of the electrical stimulus. With this

to

be

representing

approximately

to

same

it

from

in

the

place,

arise

pipette

poles, relatively selective stimulation with longitudinal

cochlear

¢bers

recording

They found very broad stimulation with basal mono-

(1)

responding

the

tonotopic

microstimulation.

region

of

the

nerve

As

bun-

their location remains unknown. Thus the spatial locus

dle even after contact with that particular ¢ber is lost.

of excitation for any particular electrode and stimulus

Thus the procedure can be carried out

current cannot be determined.

has been studied physiologically and contact has been

Signi¢cant progress in measurement of spatial excitation patterns with electrical stimulation of the cochlea

after

the ¢ber

lost. The second basic premise is that cochleotopic projec-

requires a means of determining the cochlear location

tion

of recorded neurons from an acoustically unresponsive

pathways at the inferior colliculus (IC) can be exploited

and

ear. The lack of a method for estimating cochlear place

to infer the tonotopic `place' of the volleys elicited on

of neurons in deaf ear remains the biggest single im-

the AN. Anatomic (Oliver and Morest, 1984 ; Adams,

pediment

studies

of

the

1979 ;

comparison

to

the

(Rose et

`blind' recordings which have been used to date,

any

to

electrically

progress

stimulated

in

physiological

cochlea.

In

binaural

Oliver, al.,

convergence

1984, 1963 ;

1987)

and

of

frequency

physiological

Merzenich and Reid,

speci¢c

studies

1974)

have

shown that the ICC is topographically highly organized

HEARES 2887 28-11-97

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

142

into a series of isofrequency laminae which receive bin-

binaural interactions within the ICC. Electrical activity

aural frequency-speci¢c inputs. Provided that the mi-

in the IC is measured with a single macroelectrode dur-

crostimulation of AN is tonotopically discrete, the eli-

ing AN microstimulation. Narrowband acoustic search

cited volleys will propagate through frequency-speci¢c

stimuli with various center frequencies are presented to

pathways of the brainstem to produce maximum input

the opposite normal ear. When volleys from the normal

to the ICC within the isofrequency lamina correspond-

ear impinge upon the same lamina receiving the electri-

ing to the CF of the stimulated AN ¢bers.

cally elicited volleys, some in£uence on the evoked elec-

Assuming approximate determined

that CF

by

these of

two

the

premises

recorded

identifying

the

are

AN

best

the

trical activity is expected. Best frequency of that lamina

can

be

may be inferred from the center frequency of the search

of

the

stimulus which most strongly in£uences the evoked ac-

valid,

¢ber

frequency

methods

tivity. The in£uence of the acoustic search stimulus is

for doing so are described below. Both utilize acous-

measured in the frequency domain using spectral anal-

tic

ysis

ICC

lamina

stimuli

receiving

the

presented to

the

volleys.

normal,

Two

opposite ear,

to

of

identify the best frequency of the ICC lamina. Each

detects

method

presents

vantages

in

particular

determining

the

of

ICC

gross

potential of

two

signal. periodic

The

analysis

signals

con-

and

disad-

verging within the ICC from opposite ears. This ap-

activity

within

proach is similar to a method used to measure binoc-

advantages locus

the

intermodulation

ular

ICC.

interactions

in

the

visual

system

(Regan

and

Regan, 1989).

2.2. Method 1: evoked potential vs. ICC depth

Each ear is stimulated to produce periodic volleys to ICC along a narrow frequency pathway. The stimulus

In this method the ICC lamina receiving volleys from

to the experimental ear repeats at repetition rate

fe

and

the experimental ear is identi¢ed by a straightforward

the search stimulus to the other ear repeats at a di¡er-

`polling'

ent rate

procedure.

Brief

current

pulses

are

applied

fs .

The steady state gross potential recorded at

through the pipette within the AN, and the resulting

the ICC includes responses to both periodic inputs. The

evoked potential

a microelec-

spectral consequences of binaural interaction are most

trode at various depths along a track through the con-

easily appreciated by ¢rst considering the case where

tralateral ICC. The depth at which the EP is greatest is

there is no interaction, i.e. when volleys from the two

presumed to represent the lamina whose best frequency

ears impinge upon two

matches the CF of the excited AN ¢bers. The lamina's

within ICC. In the steady state, activity from the ¢rst

best frequency is then identi¢ed by presenting acoustic

lamina generates a periodic potential with period

(EP)

is

measured with

di¡erent

isofrequency laminae

Te = 1/

tones to the other ear. This method has some limita-

fe .

tions. First, if the laminae are polled by driving a single

with energy only at

recording electrode through various depths, then a new

other lamina generates a second periodic potential with

Because this signal is periodic, it has a line spectrum

Ts = 1/fs

fe

and its harmonics. Similarly the

fs

track through ICC is needed for each contacted AN

period

¢ber. In general this would not be practical if a large

and its harmonics. The aggregate potential recorded by

population of ¢bers is to be studied. However, we an-

a macroelectrode is the superposition of these two sig-

ticipate that this di¤culty can be addressed by using a

nals. Therefore its spectrum is the sum of the two orig-

whose spectrum has energy only at

¢xed multicontact array of recording microelectrodes

inal spectra, and will have energy only at

placed across the frequency axis of IC (see Section 4).

their harmonics.

Second, resolution of the place estimate is limited by the

spacing

between

recording

sites,

which

in

turn

would be ¢xed by the density of contacts in a multi-

fe

and

fs

and

In the case where volleys from the two ears converge upon the

same

isofrequency lamina within ICC, binau-

ral neurons within the lamina are in£uenced by inputs

fe

fs

contact recording array. Finally, the method depends

from both ears. We assume that

upon identi¢cation and quanti¢cation of a time domain

chosen to be inharmonic such that the least-common-

response (the EP) which is contaminated by electrical

multiple of their periods

stimulus

such

the master period. We further assume that the binaural

quanti¢cation can be problematic because the magni-

neurons are not perfectly linear (i.e. their outputs are

tude

can

not the simple summation or subtraction of their scaled

vary across preparations and recording sites. Automa-

inputs), which is inherently true of synaptic processes.

tion of this process is likely to be di¤cult. Method 2

The steady state response of the binaural neurons re-

avoids each of these limitations.

sponding to both inputs must be periodic at

and

artifact.

Even

morphology

with

of

visual

both

EP

inspection

and

artifact

TM

and

have been

is ¢nite. We refer to

TM

as

TM =1/fM .

Then the spectrum of that response will have energy

2.3. Method 2: binaural interactions in ICC Rather

than

polling

individual

laminae,

fM and its harmonics. Those harmonics include fs and their harmonics, but they also include intermodulation (IM) distortion products nfe þ mfs pro-

only at

fe

method

2

seeks to identify the responding lamina by measuring

and

duced by nonlinear

HEARES 2887 28-11-97

combination of the two periodic

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

143

1

inputs at the binaural neurons . The aggregate poten-

was titrated by skin pinch and maintained by periodic

tial recorded by a macroelectrode is the summation of

subcutaneous

¢elds

tion.

from

both

binaural

and

monaural

neurons,

ECG

injection

was

of

lactated

monitored

Ringer's

continuously.

solu-

The

animal

and its spectrum will include distortion products in ad-

was mounted in a stereotaxic frame using hollow ear

dition to harmonics of

bars.

fe

and

fs .

Thus convergence of

The

left

cerebellum

binaural inputs can be detected by examination of the

craniotomy.

Cerebellum

ICC gross potential spectrum for IM distortion prod-

and

nucleus

was

then

ucts.

lear

nucleus

was

gently

was

exposed

overlying gently

the

by

aspirated.

displaced

occipital

auditory The

medially

nerve coch-

by

in-

When an electrical stimulus is used to elicit volleys

sertion of small pieces of cotton between the nucleus

from the experimental ear, the gross potential recorded

and the skull to enhance the exposure of the auditory

by the macroelectrode represents the sum of both phys-

nerve.

iological signals described above and electrical stimulus

Stimulus waveforms were synthesized digitally with

artifact. A powerful advantage of this method is that in

two 16-bit digital-to-analog converters (DACs) clocked

the frequency domain the electrical stimulus artifact is

by

entirely segregated from the physiological signals of interest. This is true because the electrical stimulus artifact is perfectly periodic at fe and contributes energy to the gross potential spectrum only at fe and its harmon-

separate

Acoustic

4.5-digit

stimuli

phase-locked-loop

were generated with

synthesizers.

two Sennheiser

HD540 dynamic phones coupled to the hollow stereotaxic ear bars (Sokolich, 1981). A separate acoustic calibration was performed for each ear in each preparation

at

using a calibrated microphone positioned within 2 mm

these frequencies as well, they are not the components

of the tympanic membrane through a tube at the tip of

of interest. The spectral components of interest re£ect-

the ear bar. Electrical stimuli were generated by con-

ing binaural convergence are those distortion products

necting the output from one of the DACs to a custom,

at

optically isolated high-voltage stimulator.

ics.

Although

nfe þ mfs

there

are

physiological

components

which are distinct from the harmonics of

fe .

Single

These components can be readily resolved by spectral

unit

analysis even if they are 70 dB or more below the arti-

were

made

fact components.

(20^25 M

6

recordings

with

3

M

from

KCl

auditory

¢lled

glass

nerve

¢bers

micropipettes

). Tuning curves for AN ¢bers were meas-

These experiments were undertaken to evaluate the

ured with tone pips according to the paradigm of Liber-

two proposed methods. This required that actual CF of

man (1978). The same micropipette was used alternately

AN ¢bers be measured with standard acoustic tuning

to

curves for comparison with estimated CFs. Therefore

liver

all animals had normal hearing in both ears. The ani-

bundle. After a tuning curve was measured the wire

mals were not deafened, and were not implanted with

from the shank of the pipette was disconnected from

intracochlear electrodes. Only one of the two methods

the recording preampli¢er and connected instead to the

was studied in each preparation because they employed

output of the optically isolated constant-voltage stimu-

di¡erent IC recording electrodes. Care and use of these

lator. The recording site was stimulated with 0.5 ms

animals were approved by the Duke University Institu-

biphasic sinusoidal voltage pulses (1 cycle of a 2 kHz

tional Animal Care and Use Committee.

sine) to the shank of the pipette. Repetition rate varied

record single ¢ber action microstimulation at the

potentials and then to desame site within the nerve

between 19 Hz and 97 Hz. A subcutaneous needle in

2.4. Surgical preparation

one forelimb serve as a return electrode. The amplitude of the voltage pulse varied between 20 V and 80 V peak,

Experiments were conducted in 14 adult cats prean-

which produced

6

peak

currents

of

1^4

WA

through

a

esthetized by i.m. injection of ketamine hydrochloride

typical 20 M

(30 mg/kg) and acepromazine (1.7 mg/kg). Surgical level

pipette was a regulated voltage, the high series resist-

anesthesia was maintained with i.v. doses of diallyl-bar-

ance

bituric acid, urethane and monoethyl urea (20, 40, and

constant current to the tissue. In several preparations

40 mg respectively per bolus). A tracheal cannula was

the

placed through a tracheotomy. Atropine sulfate (0.05

instrumentation ampli¢er which measured the voltage

mg/kg i.m.) and dexamethasone (1.0 mg/kg i.v.) were

drop across a 100 k

administered at 12-h intervals to reduce secretions and

return electrode. Current waveforms showed no £uctu-

edema. Core temperature was maintained between 37

ations during stimulation with 80 V pulses at 97 Hz.

and 39³C with a warm-water heating pad. Hydration

Pipette impedances and noise levels measured with the

of

the

actual

pipette. Although the stimulus to the

pipette e¡ectively

current

waveform

6

resulted

was

in

delivery

monitored

with

of

an

resistor placed in series with the

recording ampli¢er were unchanged even after lengthy 1

In fact it can be shown that every harmonic of

in¢nite where

n

set and

of

m

intermodulation

frequencies

of

fM

the

sessions of such stimulation, and subsequent recordings represents an

form

nfe þ mfs

are nonzero integers. Conversely, every such IM fre-

quency can also be shown to be a harmonic of

fM .

from other AN ¢bers were normal in all respects. Thus there was no evidence that stimulation altered the properties of the pipette in any way.

HEARES 2887 28-11-97

144

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

2.5. Method 1: evoked potential vs. ICC depth

During microstimulation of the AN EPs were recorded at various depths within the contralateral ICC using a stereotaxically positioned tungsten microelectrode (1^4 M6). The microelectrode was driven along a track in the sagittal plane 20^30³ from the vertical (dorso-rostral to ventro-caudal). The track was calibrated to enter ICC at its rostro-dorsal boundary. EPs were recorded at intervals of 0.1^0.5 mm by averaging responses to 200^500 pulses at each depth. At each depth best collicular frequency (BCF) was determined from single or multi unit tuning curves. (For clarity we use the term best collicular frequency when referring to cells within the ICC, and reserve the term CF to indicate characteristic frequency of auditory nerve ¢bers.) IC tuning curves were measured with both ipsilateral and contralateral tone pips. EP magnitude was measured from baseline to peak on the leading edge of the positive wave between 2 and 3.5 ms latency. EP magnitude was plotted as a function of BCF, and the peak of this function was compared with the CF measured directly from the AN ¢ber tuning curve. 2.6. Method 2: binaural interactions in ICC

Gross potentials were recorded within the ICC using similar tungsten needles except that 0.5^1.5 mm of insulation was removed from the tip of the needle to form a macroelectrode. The electrode tip was either positioned immediately rostro-dorsal to the boundary of ICC, or driven into ICC (in most cases to a depth which maximized the EP elicited by 100 Ws long, 80 dB peak SPL rarefaction clicks). The ampli¢ed gross potential was lowpass ¢ltered at 2 kHz and connected to a spectrum analyzer. In most experiments the signal was also digitized and averaged for subsequent o¡-line analysis. Current records of the ¢ltered IC potential were also collected using a separate computer. The search stimulus presented to the non-experimental ear was a sinusoidally amplitude-modulated (SAM) tone. Its carrier frequency Cs was varied between 200 Hz and 30 kHz in order to activate di¡erent tonotopic pathways. Periodicity was established by 100% modulation at frequency fs which was ¢xed at 101.875 Hz. Carrier intensity was varied but was generally limited to 70 dB SPL in order to limit spread along the basilar membrane and consequent broadening of the activated pathway. Experiments were ¢rst undertaken to test the basic methodology using a second SAM tone (rather than microstimulation) presented to the experimental ear to elicit periodic volleys in the AN. This second carrier at frequency Ce was modulated at ¢xed fre-

quency fe =96.875 Hz. The modulation frequencies fe and fs were selected to be near 100 Hz, inharmonic to one another, and not multiples of the 60 Hz power line frequency. In addition, these two frequencies produce IM products which fall exactly at the analysis frequencies of the spectrum analyzer which was used in initial experiments to measure the intermodulation energy. Intermodulation components nfe þ mfs in the spectrum of the IC gross potential were measured as carrier frequencies Cs and Ce were varied. Carrier tone frequencies Cs and Ce were selected to produce an integer number of carrier cycles within one period of their respective modulators. In cases where it was desired to deliver bilateral SAM tones with equal carrier frequencies the closest integer multiples of the modulators were used. For example, if matching bilateral 5 kHz carriers were desired the actual carrier frequencies used were Ce = 52fe = 5.037500 kHz and Cs = 49fs = 4.991875 kHz. Although their frequencies are not identical, such approximately equivalent carrier pairs are referred to below as `matched carriers', and the term `near' is used to identify the corresponding target frequency. Carrier intensities are speci¢ed in dB SPL RMS at modulation maxima. In two preparations the experimental ear received microstimulation of AN through the recording pipette to generate the periodic volleys. In initial experiments the spectrum of the IC gross potential was measured with the spectrum analyzer. Spectra were stored on disk for subsequent o¡-line analysis. In a few cases the frequency zoom capability of the analyzer was utilized to lower the noise £oor around speci¢c distortion products (generally fe + fs). In this mode a longer time record was collected resulting in more closely spaced analysis lines, each with a smaller noise component. Because of the narrowed frequency window, however, fewer distortion products were available for analysis. In later experiments this limitation was removed by storing time records of the IC gross potential and computing spectra o¡ line using custom analysis software. Time records were collected and stored in two forms, termed `short' and `long'. In the short form the IC potential was sampled at 10.24 kHz, and 10 cycles of the master period TM were averaged (16 s total). Time zero represented the common zero crossing of both modulators fe and fs . Spectra of the short form records were computed by discrete Fourier transform. The long form consisted of a raw 16 s epoch sampled by a separate computer with 12-bit resolution at a 10 kHz rate (160 000 samples total) beginning at an arbitrary point within the master period. Spectra of long form records were computed by Chirp-z

HEARES 2887 28-11-97

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

145

Fig. 1. EP data collected at successive depths along one track through ICC with microstimulation of AN. CF at stimulus site was 9.3 kHz.

3

Stimulus was 1 cycle of a 2 kHz sine wave applied to the pipette. a : EP magnitude (leading edge baseline

peak) vs. depth. Depth 0 represents

the dorso-caudal boundary of ICC 2.5 mm posterior, 4.5 mm dorsal, and 4.5 mm lateral to stereotaxic zero. Legend indicates stimulus intensity in peak volts. b : BCF vs. depth. Dashed curve represents ¢tted function

y = axb .

Dotted line shows CF of AN ¢ber contacted at the stimulus

site. c : Magnitude replotted against BCF at corresponding depths. Inset shows tuning curve measured from the AN ¢ber prior to microstimulation. d : EP waveforms for 70 V data of panels a and c.

transform (Rabiner and Gold, 1975) after application

3. Results

of a hanning window. Both short and long form records were

collected

concurrently

over

approximately

the

3.1. Method 1: evoked potential vs. ICC depth

same 16 s interval, although they did not have identical starting points. Data collection began approximately 1 s

Evoked potential data were collected from 12 tracks

after onset of the stimuli. Excellent correspondence was

through ICC in six animals. Along each track EPs were

observed between corresponding long and short form

recorded at depth intervals ranging from 0.1 to 0.5 mm.

spectra.

At each depth an averaged EP was recorded with mi-

HEARES 2887 28-11-97

146

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

Fig. 2. EP data from a single track through ICC with microstimulation of AN. CF at stimulus site 710 Hz. Format of panels a^c as in Fig. 1. d : EP magnitude replotted against interpolated BCF derived from the ¢tted curve (dashed line) of panel b.

crostimulation to the AN at each of several pulse in-

depth data are replotted against BCF on the abscissa.

tensities ranging from 10 V to 80 V peak. Data from a

For comparison a tuning curve measured from an AN

representative track are shown in Fig. 1. Panel 1d

¢ber at the site of microstimulation is inset in panel 1c.

shows the sequence of evoked potentials recorded at

BCFs at the maxima slightly overestimate CF of the

successive depths within the IC using a 70 V stimulus

AN ¢ber, but there is generally a good correspondence.

to the pipette. The magnitudes of these EPs and others

The relatively smooth and monotonic BCF vs. depth

measured with lower stimulus intensities are plotted

relationship of Fig. 1b is representative of most data

against relative depth in panel 1a. All of the curves

from this study. However, in four cases the BCF/depth

exhibit a maximum in the vicinity of 3.3 mm relative

curves exhibited moderate discontinuities or non-mon-

depth. BCFs at corresponding depths along the same

otonicity at low frequencies. These e¡ects were an arti-

track are shown in panel 1b. In panel 1c the EP vs.

factual result of the de¢nition of BCF adopted here,

HEARES 2887 28-11-97

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

147

Fig. 3. EP data from a single track through ICC with microstimulation of AN. CF at stimulus site 3.7 kHz.

viz. the absolute minimum of the multiunit tuning

the AN ¢ber at the site of microstimulation corre-

curve. Although this de¢nition is simple and conven-

sponded to the single maximum observed at lower in-

ient, it can introduce variability at low frequencies

tensities. It was hypothesized that the divergence into a

where the curves are broadly tuned. A relatively noisy

bimodal curve at high intensities re£ected spread of the

tuning curve may demonstrate several local minima

microstimulation into an adjacent AN fascicle contain-

within a broadly tuned tip, and the deepest of those

ing ¢bers with lower CFs.

de¢nes the BCF. In order to reduce the e¡ects of

Fig. 4 compares actual and estimated CFs for all

such variability, BCF vs. depth data from each track were ¢tted with a power function of the form

y = axb

as

illustrated in panel 1b. These ¢ts provided smooth monotonic functions which could be used to interpolate an estimated BCF for each depth. EP data were plotted against both raw BCFs and interpolated BCFs. Fig. 2 illustrates such a comparison. In this case microstimulation in the AN was delivered at the site of a low frequency ¢ber with a CF of 710 Hz. As in Fig. 1, the EP vs. depth data demonstrate a well de¢ned maximum, in this case near 0.5 mm. But the non-monotonicities

introduced

by

the

transformation

from

depth to BCF (panel 2b) result in the relatively noisy EP vs. BCF plot (panel 2c). The EP data are replotted in panel 2d against interpolated BCF computed from the best ¢t function of Fig. 2b. As in Fig. 1 there is a good correspondence between BCF at the maxima and the CF of the ¢ber. For 11 of 12 tracks the EP vs. depth data demonstrated an unambiguous maximum which was consistent across intensities. Data from the remaining track are shown in Fig. 3. EP magnitude exhibited a single maximum at 1 mm relative depth for stimulus intensities up to 40 V (panel 3a). As the intensity was further increased to 80 V two separate maxima in the EP vs. depth curve emerged. As shown in panel 3b, the CF of

Fig. 4. Estimated vs. measured CF of AN ¢bers. Each symbol represents one AN ¢ber and one track through ICC. Solid represents perfect estimation (not a regression line).

HEARES 2887 28-11-97

x=y

line

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

148

Fig. 5. Excerpts of magnitude spectra computed from short form records of ICC potential with unilateral and bilateral SAM tones near 10 kHz. Both carrier intensities 70 dB SPL. Solid line indicates ipsilateral to IC. Carrier frequency

Ce = 103fe = 9.978125

3

150 dB re : 1 V rms. Carrier frequency

Cs = 98fs = 9.98375

kHz presented to ear

kHz presented to contralateral ear. Solid diamonds indicate harmonics of the 60 Hz

power line frequency.

studied

AN

¢bers.

Estimates

were

made

from

both

quency (198.75 Hz) also appeared. In this case an addi-

fe +fs

measured BCF and interpolated BCF at the each site

tional IM product at 2

of maximum EP. For the ¢ber shown in Fig. 3, CF was

fe + fs

estimated from the 40 V EP data because it was the

entation of matched carriers between 500 Hz and 20

was observed as well. The

product was similarly observed with bilateral pres-

kHz. In general

fe +fs

For all other tracks the highest intensity studied was

and

IM

employed (60^80 V). Estimates from measured BCFs

animals

show

cases of bilateral stimulation with matched carriers.

highest

intensity

slightly

r2 = 0.94) 2 (r = 0.90). (

which

higher

than

produced

a

correlation

those

from

single

with

maximum.

actual

interpolated

CF

BCFs

prominent

fe +fs

was the most reliably measurable product

in

the

spectrum.

Across

was measurable in the great majority of

Fig. 6 illustrates the e¡ect of stimulus intensity on the magnitude of the

fe +fs

M fe + f s M )

distortion product (

generated by bilateral SAM tones with matched car-

3.2. Method 2: binaural interactions in ICC

riers. Each panel presents data collected at one of ¢ve di¡erent depths along two di¡erent tracks within ICC.

Measures of binaural interaction were made in eight

In each panel

Mfe +fs M

is plotted against stimulus inten-

fe +fs

animals. Most experiments reported here used bilateral

sity for various carrier frequencies. In general the

acoustic stimuli in order to assess the feasibility of de-

product was resolved above the noise £oor with inten-

tecting binaural interaction with spectral analysis. Un-

sities above 50 or 60 dB SPL. Its magnitude rose with

less otherwise speci¢ed, the stimulus to the experimental

increasing intensity, tending to plateau at higher inten-

ear was a SAM tone modulated at

fe = 96.875

Hz, and

the search stimulus to the contralateral ear was a SAM

fs = 101.875

tone modulated at

Hz. Fig. 5 shows exem-

sities. The magnitude of frequency.

Four

of

the

fe +fs ¢ve

also varied with carrier

sites

exhibited

particular

sensitivity to one of the tested carrier frequencies. At

fe +fs

plary magnitude spectra computed from short form re-

these `preferred' frequencies the

cords measured with unilateral and bilateral SAM tones

above the noise £oor at intensities as low as 10^30 dB

with carriers near 10 kHz. Both stimuli were generated

SPL. As a consequence of the saturating tendency in

in

the curves, the spread in

all

three

produce

cases,

but

unilateral

one

attenuator

stimulation.

As

was

muted

illustrated

in

to the

top two traces unilateral presentation of either stimulus produced prominent spectral components at harmonics of the modulator (

fe

or

fs ).

With bilateral stimulation a

prominent component at the

fe +fs

IM distortion fre-

Mfe +fs M

product remained

across frequencies gen-

erally decreased as intensity increased. The rationale for inferring the locus of activity in the experimental that

the

ear

binaural

from

ICC

gross

interaction

when the binaural inputs are

HEARES 2887 28-11-97

in

potentials

the

ICC

is

assumes greatest

tonotopically coincident,

C. van den Honert et al. / Hearing Research 113 (1997) 140^154 maximum in

Mfe +fs M

149

Cs

was observed for

Ce .

at or near

The maxima became broader as intensity was increased, and in two cases (Fig. 7a,b) a second maximum near

Cs = 1.5 kHz emerged at high intensities. In one of those cases

(Fig.

7a)

this

second

`spurious'

maximum

ex-

ceeded the original matched carrier maximum when intensity was raised to 60 and 70 dB SPL. Nevertheless, in

Ce

each of these cases a good estimate of

(the frequency

region of activity in the experimental ear) could be inferred from the behavior of the

Mfe +fs M

Cs

vs.

curves.

For brevity we will adopt the abbreviation IMTC (for `intermodulation

Mfe +fs M

vs.

Cs

tuning

curve')

to

refer

to

plots

of

below.

The data of Fig. 7 argue for the use of low or moderate intensities to preserve selectivity of the measure. However, this presents a practical problem. At any particular ICC recording site, low intensity stimuli generally generated a measurable

fe +fs

component over only

a limited range of preferred matched carrier frequencies (e.g. Fig. 6a^d). The question remains whether, at a single recording site, adequate selectivity can be maintained with higher

intensities needed

to resolve

fe +fs

across a wide range of frequencies. Data addressing this question are mixed. Each panel of Fig. 8 shows IMTCs from one site collected using bilateral intensities of 70 dB SPL. Fig. 8a illustrates a case where two experimental ear carriers almost three octaves

apart

were

readily

distinguished.

IMTCs were measured with ¢xed

Ce

The

two

near 1 kHz and

7 kHz respectively. Although both curves are broad, the maxima are well de¢ned and correspond to

Ce

w

in both

cases. In the case shown in Fig. 8b, IMTCs exhibit well de¢ned maxima corresponding to

Ce

for

Ce

500 Hz,

10 kHz and 20 kHz, but the maximum of the 2 kHz

Ce and that of the 5 kHz Ce . The poorest observed in Fig. 8c. Except for Ce 20

curve is 1.5 octaves below

w

curve is two octaves above correspondence is shown Fig. 6. Intermodulation energy vs. intensity measured with bilateral

kHz the IMTCs are broad with poorly de¢ned maxima

w

Ce . Further, three of these

matched carriers at various frequencies. Each panel represents a dif-

which generally do not fall at

ferent ICC recording site in the same animal. Legend inset in panel

curves

e applies to all panels. Hatched area represents the noise £oor.

`spurious' maximum at 1.5 kHz, similar to that in the

(

Ce

500,

5

kHz

and

10

kHz)

also

exhibit

a

70 dB curve of Fig. 7a. Across all animals, no single site

wC

fe +fs

i.e. the matched carrier case. Thus the should be strongest when progressively frequency.

In

Ce

weaker

as

the

order

to

test

carriers

Ce

product

s and should become

this

are

separated

assumption

Cs

in

demonstrated appropriate IMTC maxima for the entire range of

Ce

Several

values when 70 dB SPL stimuli were used.

observations

suggested

that

high

intensity

Mfe +fs M

1 kHz SAM tones (70 dB SPL) were singularly e¡ective

was systemati-

in generating intermodulation products when compared

cally varied. Fig. 7 shows results measured at each of

to equally intense SAM tones at other carrier frequen-

the four ICC recording sites from Fig. 6 which exhib-

cies. The ¢rst was the phenomenon of `spurious' peaks

ited particular sensitivity to one of the matched carrier

such as those in Fig. 7a,c. These were frequently ob-

was measured with a ¢xed

while

fe +fs is plotted as a function of the search carrier frequency Cs . In each case the experimental ear carrier Ce was ¢xed at the preferred frequency (indicated by the vertical line), and Cs was varpairs. The magnitude of

served in IMTCs with 70 dB SPL carriers, and were

W

consistently

Cs Ce .

located

around

search

frequencies

of

1 kHz regardless of recording site or the value of

In addition, bilateral matched carrier 1 kHz SAM

ied. Carrier intensity was the same for both ears, and

tones at 70 dB consistently elicited a strong response

was varied between 20 and 70 dB SPL. In each case a

with

a

HEARES 2887 28-11-97

distinctive

spectrum

characterized

by

a

rich

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

150

Fig. 7. Intermodulation tuning curves measured at the same four sites illustrated in Fig. 6a^d. Carrier intensities to the two ears were equal. Legend inset in panel d applies to all panels. In each case 6 for which the

structure

of

fe +fs IM

Ce

(indicated by vertical line) was ¢xed at the `preferred' carrier frequency from Fig.

product remained above the noise at 30 dB. Hatched areas represent the noise £oor.

products

and

modulator

harmonics

with a repetition rate of 96.875 Hz. The non-experimen-

fs

clustered at 50 Hz intervals. These features were gener-

tal ear received SAM tones modulated at

ally not observed with other matched carrier frequen-

Prior to microstimulation the pipette was used to record

cies at 70 dB. In addition the

fe +fs

product at 1 kHz

as usual.

a standard tuning curve from a single AN ¢ber. In the

fe +fs

was sometimes 15^20 dB higher than that observed with

¢rst case the

other matched carrier frequencies. One further observa-

the noise £oor. In the second animal the

tion regarding these stimuli is noteworthy. In one ex-

nent

periment a platinum ball recording electrode was placed

quency

on the cortical surface. With 1 kHz matched carriers the

shows the IMTC and corresponding single ¢ber tuning

fe +fs

curve. The peak in the IMTC corresponds well with the

product

was

clearly

resolved

at

the

cortex

for

stimuli of 60 dB SPL or greater, whereas with 5 kHz and 20 kHz carriers up to 80 dB no

fe + fs

was

component was not resolved above

successfully

resolution

of

resolved the

by

fe +fs

increasing

spectrum

analyzer.

compothe

fre-

Fig.

9

tuning curve tip.

component

was ever resolved above the noise £oor. All of the intermodulation measures described above

4. Discussion

were performed with acoustic stimulation of both ears. In two animals periodic microstimulation was used to

4.1. Microstimulation of auditory nerve

excite the auditory nerve through a micropipette. The stimulus was an 80 V-peak 500

Ws/phase

biphasic pulse

Microstimulation

HEARES 2887 28-11-97

of

the

auditory

nerve

through

a

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

151

recording pipette forms the cornerstone of both proposed methods of CF inference. Perhaps the most important result of these experiments is the demonstration that such microstimulation is practical. Two possible di¤culties with such microstimulation were anticipated. The ¢rst was that adequate stimulation might not be achievable through the high impedance of a micropipette. Results from the EP vs. depth measures (e.g. Fig.

Fig. 9. Intermodulation tuning curve measured with microstimulation of AN in the experimental ear. CF at stimulation site 1.26 kHz. Inset shows tuning curve measured from AN ¢ber prior to microstimulation. Stimulus was a biphasic pulse (80 V peak, 500

Ws/

phase) repeated at 96.875 Hz. Hatched area represents the noise £oor.

1) clearly demonstrate that adequate stimulation can be e¡ectively delivered through these recording electrodes. The second anticipated di¤culty was that stimulation adequate to elicit a measurable response in the ICC might excite a substantial population of ¢bers whose CFs were dissimilar to that of the recorded ¢ber. This might occur if (1) the stimulus were to spread across a fascicular boundary ; or (2) the CFs of the recorded ¢ber were dissimilar to those of its neighbors. With respect to the former, the curves of Fig. 3 do suggest that cross-fascicular spread may occur at high intensities. But the phenomenon is recognizable by the transition from a narrow unimodal pro¢le to a broad bimodal one at high intensity. The latter issue hinges on the local homogeneity of CF in comparison to the size of the stimulated region of the AN. We are not aware of any detailed maps in the literature which describe the microscopic details of tonotopy within the cross-section of cat AN at the intracranial boundary. In our experience it is not uncommon to observe a one octave change in CF with a 25^50

Wm

advance of the pipette.

On the other hand, contact with one ¢ber is occasionally maintained over a comparable distance and then lost precipitously, which suggests that the tip of the pipette may not always advance smoothly through the tissue. Observed CF discontinuities may therefore be at least partially due to tissue distortion and relaxation as the pipette is advanced, rather than local variability of Fig. 8. Intermodulation tuning curves at various

Ce

frequencies with

bilateral 70 dB carriers. Each panel represents a di¡erent ICC recording site. Legend inset in panel a applies to all panels. Hatched area represents the noise £oor.

CF. The size of the microstimulation region is also dif¢cult to estimate with con¢dence. Notwithstanding these quantitative questions, the excellent correlation demonstrated in Fig. 4 suggests that

HEARES 2887 28-11-97

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

152

local tonotopy is su¤cient to permit a reasonably ac-

curve could likely be interpolated and/or extrapolated

curate inference of CF. In this context it is worth reit-

from even a handful of measured points. Such extra-

erating that even an imperfect estimate of cochlear lo-

polation might be needed for very high BCF sites where

cation would permit, for the ¢rst time, study of spatial

sensitivity to ipsilateral tones is lower (Schreiner and

selectivity of intracochlear electrode geometries in deaf

Langner, 1988). Even in a bilaterally deafened prepara-

ears. Such studies must generally be carried out in large

tion, where acoustic responses cannot be measured at

¢ber populations where an occasional estimation error

all, IC depth alone can still be used to determine

(even much larger than those observed here) would in-

tive

troduce outliers in the population data, but would not

et al. (1990) used IC depth in this way as an analog of

preclude

the frequency axis to measure spatial tuning of IC re-

nally,

reasonable

the

spatial

data

interpretation

presented

speci¢city

of

here

of

also

results.

demonstrate

microstimulation

after

the

is

Fithat

adequate

rela-

cochlear place among recorded AN ¢bers. Snyder

sponses to intracochlear stimulation.

to

A clear limitation of the method as implemented in

contact with a ¢ber has been

these experiments is the need to perform a new pene-

lost. This is particularly important, because it means

tration of IC for every CF estimate. Each penetration is

that valuable recording time need not be devoted to

time consuming and unavoidably imparts some damage

the CF estimation procedure.

to the IC. A more practical implementation would uti-

estimate CF even

One caveat is in order regarding frequency-speci¢c microstimulation.

In

a

chronically

deafened

auditory

lize a ¢xed linear array of recording electrodes with 100

Wm

spacing (Hetke et al., 1992). The array could be

system, central reorganization may broaden or distort

driven into the IC to span the tonotopic axis of the

cochleotopic projections. In this case binaural inputs to

ICC. Since the recording sites would be ¢xed, BCFs

an

similar

could be measured (or interpolated) just once for each

cochlear places in both ears (Snyder et al., 1990). In a

electrode at the outset of the experiment. With appro-

unilaterally deafened animal reorganization on one side

priate

might lead to an error in estimating the physical coch-

could be recorded simultaneously from all electrodes,

lear place of the stimulation presuming a normal fre-

such that data collection for each CF estimate would

quency map. Further experiments are needed to deter-

require only tens of seconds.

IC

mine

lamina

the

may

e¡ects

of

not

necessarily

chronic

represent

deafening

on

the

EP

multichannel

recording

instrumentation,

EPs

vs.

depth pro¢les. In any case this is not an issue in acutely

4.3. Method 2: binaural interactions in ICC

deafened preparations which can be pro¢tably used to study a variety of basic issues regarding spatial selectiv-

Method 1 seeks to identify the IC lamina receiving

ity of intracochlear electrode con¢gurations and stimu-

volleys from the experimental ear essentially by polling

lation methods.

the individual laminae. In contrast, method 2 seeks to identify it on the basis of phenomena detectable at a

4.2. Method 1: EP vs. depth

distance, without requiring a separate, spatially discrete measurement from each candidate lamina. Prospects for

It is evident from Fig. 5 that CF of an auditory nerve

success of this method are still uncertain. The data of

¢ber can be estimated well from the EP vs. depth pro¢le

Fig. 7 suggest that the desired information exists within

using microstimulation. Recordings with a spatial reso-

the activity of IC, but it is also clear that at this point

lution

no turnkey method for extracting it is in hand. The

of

100

Wm

(and

sometimes

coarser)

yielded

a

correlation coe¤cient of 0.94 between actual and esti-

objective

mated CF values. Errors might have been smaller in

these experiments was to derive a spatially generalized

some cases if EP data had been available from inter-

aggregate measure of activity within ICC. The fact that

mediate depths (in ¢ve of 12 tracks only 500

reso-

some sites exhibited particular sensitivity to one of the

While ¢ne spatial resolution might

matched carrier frequencies (Fig. 6) suggests that some

lution was used). provide

greater

accuracy,

the

demonstrated

Wm

accuracy

spatial

in

using

speci¢city

relatively

large

remained.

It

might

such

the

BCF

range spanned by the macroelectrode surface included

cochlear electrode arrays.

one

the

test

apparent mm)

was

frequencies. selectivity,

perimental ear need not depend upon single or multi

(4

unit tuning curves. Acoustic BCF could likely be deter-

resulting attenuation of

used

in

mined with good accuracy by maximizing the gross po-

urable.

In a

one

fe +fs

an very

where

that

tial excitation and interaction patterns of existing intra-

of

locations

be

sensitivity

this

at

in

is more than adequate for fruitful investigation of spa-

In practice determination of BCF from the non-ex-

occurred

macroelectrodes

attempt large

preparation.

to

avoid

electrode But

the

made it generally unmeas-

tential evoked by tone pips. In addition, it would prob-

Focusing for the moment on the optimal recording

ably not be essential to measure BCF at every depth,

circumstance where the volleys from the experimental

because BCF vs. depth curves are strongly monotonic

ear are in the electrode's preferred frequency region, it

and reproducible (Merzenich and Reid, 1974). A usable

is evident that 70 dB SPL SAM tones are not optimal

HEARES 2887 28-11-97

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

153

search stimuli for our purpose. While elevation of in-

the pivotal issue which must be resolved for practical

tensity is e¡ective in strengthening the intermodulation

use of the interaction method is the elimination of spa-

components, this comes at the expense of broadening,

tial selectivity in the recording. The analysis must detect

and sometimes distorting the IMTC. Another disad-

convergent inputs to

vantage of higher intensities is the appearance of spu-

proximately equal sensitivity. Two simple methods for

rious maxima in the IMTC in the vicinity of 1 kHz.

accomplishing this were attempted brie£y in these ex-

This is apparently due to the singular e¡ectiveness of

periments : (1) removal of the recording electrode to a

high level 1 kHz SAM tones in generating intermodu-

distance which is large compared to the dimensions of

lation products. The origin of this phenomenon is un-

ICC (surface of the cortex) ; and (2) increasing the re-

known, but it may well arise from an extracollicular

cording electrode surface to a size comparable to the

source. This would explain why it is equally prominent

dimensions of the ICC (4 mm). Unfortunately both of

at all ICC recording sites. It could also explain the fact

these have the disadvantage of attenuating an already

fe +fs

all

isofrequency laminae with ap-

is detectable even at the cortical surface with

small signal. A better alternative may be to combine

these stimuli but not with other matched carriers. Fur-

signals from an array of smaller electrodes implanted

ther experiments are needed to identify the source of

throughout the ICC, such as the one envisioned above

this phenomenon, and to determine whether electrical

for parallel EP measurements. An aggregate measure of

microstimulation of auditory nerve at the 1 kHz place

intermodulation might be derived by combining infor-

produces a similar e¡ect. From a practical standpoint

mation from all electrodes in the array. With simple

both

of

summation of their signals, corresponding IM products

IMTCs can be avoided by use of search intensities no

from multiple electrodes might interfere destructively if

greater than 50 dB SPL.

they were not all in phase. In that case individual IM

that

the

spurious

maxima

and

the

broadening

The binaural interaction method is empirical. It presumes nothing about the nature of the underlying bin-

products could be computed for each electrode, and their scalar magnitudes summed.

aural processing except that it is nonlinear and achieves a steady state with steady inputs. As such it is subject to

4.4. Conclusion

the limitations of any empirical method. Validation is needed to con¢rm its reliability across experimental

Data presented here demonstrate that the cochlear

conditions which might a¡ect the processing, such as

place of an AN ¢ber can be estimated without acoustic

depth of anesthesia. The optimum stimuli for generat-

responses, using electrical microstimulation through a

ing intermodulation can be determined only by thor-

recording pipette in the AN bundle. Microstimulation

ough exploration of the stimulus space. For these initial

excites a small group of ¢bers neighboring the recorded

studies we chose low frequency sinusoidal modulators

¢ber, generating centrally propagated volleys along a

for three reasons : (1) the resulting narrowband stimuli

frequency-speci¢c pathway. Two methods have been

excite small frequency regions ; (2) they allow search

described for identifying the locus of that pathway in

carrier frequencies down to a few hundred Hz ; and

the ICC.

(3) temporal representation (which is essential to the

Method 1 is simple and proven, and can be useful

method) is good for low rate modulators. A few pre-

even in bilaterally deafened animals. There are no con-

liminary measures with other modulation frequencies

ceptual barriers to its implementation, although adap-

did not show them to have any obvious advantages.

tation to a multielectrode recording array will no doubt

Nevertheless, the ICC is known to have a highly organ-

require some methodological re¢nements. Method 2 re-

ized topographic distribution of best modulation fre-

mains an unproven but intriguing possibility. If the is-

quencies (BMFs). BMFs are organized into concentric

sue of spatial selectivity can be successfully resolved,

contours in each isofrequency lamina, ranging from

method 2 o¡ers very signi¢cant advantages over meth-

400^600 Hz at the center to 100 Hz at the periphery

od 1 in frequency resolution, artifact immunity, and

(Schreiner

modulator

ease of automation. It holds su¤cient promise as a

combinations may be more e¡ective for our purpose.

potentially rapid and accurate tool for CF estimation

And other distortion products or combinations of prod-

to justify continued e¡ort towards its implementation.

ucts may provide a more robust overall measure of

Finally it is worth noting that a combination of the two

and

Langner,

intermodulation than

fe +fs

fe +fs

1988).

Other

alone. Our focus on the

product derived from early experiments where

methods, using the same recording array, may o¡er the advantages of each.

this product seemed to be most robust across conditions, but it is also true that many other products have been observed,

fe +fs

some of which have exceeded

Acknowledgments

on occasion.

Although better search stimuli or intermodulation

Dr. Norman Herzberg provided invaluable insight

metrics may be identi¢ed by further experimentation,

into the number theory underlying the relationships

HEARES 2887 28-11-97

C. van den Honert et al. / Hearing Research 113 (1997) 140^154

154

among modulators and distortion product frequencies. Ms. in

Ramona data

Miller

collection

supported

in

provided

and

part

technical

analysis.

by

NIH

This

Grants

assistance work

was

P01-DC00036

and R55-DC01381. Data were collected at the Hearing Research Laboratory of Duke University Medical Cen-

stimulation of the auditory nerve in the profoundly deaf ; interfacing electrode arrays with the auditory nerve. Acta Otolaryngol. 87, 196^203. Moxon, E.C.,

the

cat's cochlea :

A

MIT, Cambridge, MA. Oliver, D.L., 1984. Dorsal cochlear nucleus projections to the inferior colliculus

ter.

1965. Electrical stimulation of

study of discharge rates of single auditory nerve ¢bers. MS Thesis,

of

the

cat :

A

light

and

electron

the

inferior

microscopic

study.

J. Comp. Neurol. 224, 155^172. Oliver,

D.L.,

1978.

Projections

to

colliculus

from

the

anteroventral cochlear nucleus in the cat : Possible substrates for

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