Behavioral frequency discrimination ability of partially deafened cats using cochlear implants
Yuri B. Benovitski
1,2
, Peter J. Blamey
1,3,4
Graeme D. Rathbone
1,2
and James B. Fallon
1,3,4
1
Bionics Institute,
2
Department of Electronic Engineering, La Trobe University,
3
Department of Medical
Bionics University of Melbourne, and
4
Department of Otolaryngology, University of Melbourne.
Correspondence concerning this article should be addressed to James B. Fallon, Bionics Institute, 384-388
Albert St, East Melbourne, VIC – 3002, Australia. Tel.: +61 3 9288 3686; fax: +61 3 9288 2998
Email: jfallon@bionicsinstitute.org
Abstract
The aim of this study was to determine the effects of cochlear implant (CI) use on behavioral frequency
discrimination ability in partially deafened cats. We hypothesized that the additional information provided
by the CI would allow subjects to perform better on a frequency discrimination task.
Four cats with a high frequency hearing loss induced by ototoxic drugs were first trained on a go/no-go,
positive reinforcement, frequency discrimination task and reached asymptotic performance (measured by d’
- detection theory). Reference frequencies (1, 4, and 7 kHz) were systematically rotated (Block design) every
9 to 11 days to cover the hearing range of the cats while avoiding bias arising from the order of testing.
Animals were then implanted with an intracochlear electrode array connected to a CI and speech processor.
They then underwent 6 months of continuous performance measurement with the CI turned on, except for
one month when the stimulator was turned off.
Overall, subjects performed the frequency discrimination task significantly better with their CI turned on
than in the CI-off condition (3-way ANOVA, p<0.001). The analysis showed no dependence on subject (3-
way ANOVA, subject x on-off condition, p>0.5); however, the CI only significantly improved performance
for two (1 and 7 kHz) of the three reference frequencies.
In this study we were able to show, for the first time, that cats can utilize information provided by a CI in
performing a behavioral frequency discrimination task.
Abbreviations: ICES, intracochlear electrical stimulation; CI, cochlear implant; EAS, electric and acoustic
stimulation; FA, false alarm; CR, correct rejection; ∆f/f, ratio between frequency difference and reference
frequency; SPL, sound pressure level; d’, d-prime.
Keywords: Partial hearing loss, cochlear implant, behavioral frequency discrimination.
1. Introduction
Profound sensorineural hearing loss is successfully treated by intracochlear electrical stimulation (ICES) of
the auditory nerve via a cochlear implant (CI). Improvement in the speech perception ability of cochlear
implantees over the post-implantation period has been shown in various clinical studies (Blamey et al., 2012,
Blamey et al., 1996a, e.g., Wilson and Dorman, 2008). Initial perceptual quality and rate of improvement
over time largely depend on the amount of pre-implantation hearing experience and auditory training.
As selection criteria for CI recipients have eased, more patients with preserved low frequency hearing have
received CIs (for review see Turner et al., 2008). Several clinical studies report improvement of overall
hearing performance of subjects with residual hearing in one ear (possibly with a hearing aid) in addition to
ICES in the other, sometimes referred to as bimodal hearing (Von Ilberg et al., 2011, Mok et al., 2006, Firszt
et al., 2008, Ching et al., 2006). For example, Dorman et al. (2007) showed an increase of 20% in
performance of patients with CI in one ear and a hearing aid in another on word and sentence recognition
tasks when electric stimulation was added (EAS). Other studies report very little or no bimodal benefit (Mok
et al., 2006, Tyler et al., 2002). The latter findings might be at least partially explained by the finding that
pitch percepts evoked by ICES can correspond to tones up to 3 octaves lower than those predicted from the
place of stimulation (Blamey et al., 1996b). The mechanisms that underlie auditory perception in response to
combined electric and acoustic stimulation (EAS) remain unclear. Although the residual hearing of partially
deaf subjects is usually in the low frequency region, whereas the CI usually stimulates the high-frequency
region, the degree of overlap between the regions is variable and significant overlap in this region could
cause electric and acoustic perception interference.
Frequency discrimination ability is a factor in determining how well human subjects can recognize pitch,
and separate auditory streams, which in turn affects speech recognition ability (Rose and Moore, 2005). To
study the effects of interactions between electric and acoustic stimulation on frequency discrimination, we
developed a novel behavioral task (Benovitski et al., 2014) to test frequency discrimination in the partially
deaf cat model. We have previously shown that using this task, cats can learn a frequency discrimination
task and demonstrate stable and repeatable performance (Benovitski et al., 2014). The use of a partial
hearing, chronically stimulated animal model allows us to determine performance changes on a behavioral
frequency discrimination task by adding and removing ICES in the same animal. While other studies have
used conditioning to provide animals with behaviorally relevant auditory experience (Kral et al., 2006,
Klinke et al., 1999), these studies did not allow performance to be measured. Others have used avoidance
conditioning to train cats to detect stimulation thresholds (Vollmer et al., 2001, Beitel et al., 2000, Vollmer
and Beitel, 2011) and discriminate changes in modulation frequency (Vollmer et al., 2001). In those
experiments individual electrodes were tested one at a time and subjects received only electric but not
acoustic stimulation.
The aim of this experiment was to determine whether CI use affects the ability of partially deaf animals to
perform a frequency discrimination task. We hypothesized that additional information provided by the CI
would allow partially deafened animals to perform better on a frequency discrimination task. To our
knowledge, this is the first study to test frequency discrimination in partially hearing animals implanted with
a CI.
2. Method
2.1 Subjects
Four healthy cats with otoscopically normal tympanic membranes were used in the present study. All
procedures were in accordance with Australian Code of Practice for the Care and Use of Animals for
Scientific Purposes and with the guidelines laid down by the National Institutes of Health in the US
regarding the care and use of animals for experimental procedures, and were approved by the Royal
Victorian Eye and Ear Hospital Animal Research and Ethics Committee. Subjects were partially deafened
between 7.4 to 8.3 months of age by daily subcutaneous injections of Kanamycin (200 mg/kg; kanamycin
monosulphate, Sigma, USA). After 17 days, hearing condition was checked via tone-specific auditory brain
response (ABR) recordings (Coco et al., 2007) and injections continued until a partial high frequency
hearing loss was achieved to model an EAS CI recipient (Irving et al., 2014). High frequency hearing loss
(normal hearing up to 2 kHz, figure 1) was confirmed using a standard ABR. The difference in thresholds
between two ears was not significant (4-way ANOVA, ear side x cat x pre/post CI x frequency, p> 0.9).
Subjects were implanted unilaterally (left side) with a Hybrid L 14-electrode intra-cochlear array between
13.3 to 14.4 months of age. The tip of electrode array was approximately 10.5 mm from the round window,
resulting in the most apical electrode being located at approximately the 4-kHz place as represented in figure
1 (for details about the Hybrid L array and implantation procedure see Shepherd et al., 2011).
Each subject was chronically stimulated using a clinical stimulator and speech processor (Cochlear Limited)
carried in a harness worn by the animals which did not limit the animal’s ability to move (Fallon et al.,
2009). A standard stimulation strategy (SPEAK; McDermott, 1989) with a clinical electrode-frequency
allocation map was used. The 14 electrodes from apex to base were allocated to the following frequencies
187, 312, 562, 812, 1062, 1312, 1562, 1937, 2312, 2812, 3437, 4187, 5187, 6312, and 7937 Hz. The
stimulation rate was 500 pulses per second per electrode. During the stimulator-on phases of the behavioral
task, the following electrode pairs were preferentially activated by the acoustic stimulus: electrodes 13 and
10 (pair 1), 8 and 4 (pair 2), 5 and 1 (pair 3). The frequency-place map was not optimized to match the
characteristic frequencies of the electrode locations in the cochlea, thus overlap of electric and acoustic
cochlear stimulation can be expected, as shown in figure 1. After the unilateral CI implantation, acoustic
signals were not blocked from the implanted nor the contralateral ear meaning that cats were acoustically
stimulated in both ears and electrically stimulated in one ear only resulting in a combination of hybrid-
bimodal stimulation.
2.2 Behavioral procedure
After deafening, cats were trained on a go/no-go, positive reinforcement, frequency discrimination task
developed in our laboratory (For details regarding stability, repeatability and other aspects of the behavioural
method, please see Benovitski et al., 2014). Testing was carried out in the animals’ regular housing facility
where they were required to respond to pairs of tones by moving toward and away from the device
depending on whether the members of a tone pair were different or the same in frequency. A hit (animal
approached during a different frequency stimulus pair) was followed by food reward. A correct rejection
(CR) was recorded if same-frequency tone pairs were presented without an approach from the animal, after
which a new trial could be activated with no delay. A false alarm (FA) (approaching the food source after
presentation of a same-frequency tone pair) was followed by a 20 second penalty timeout, during which a
green light was presented and a new trial could not be initiated. A miss (failing to approach after
presentation of a different-frequency pair) was followed by 0 to 6 seconds of penalty time out without any
light indication. Tone pips of 195 ms with 4.3 ms rising edge and 49 ms falling edge were used. The interval
between the two tones within a pair was 750 ms, and that between two pairs was 2350 ms.
To minimize any response biases, after the end of the first week of procedural training on a different
frequency to the test stimuli, presentation of different (target) and same (non-target) frequency tone pairs
was randomized and the proportion set to 50% target and 50% non-target. The ratio between the frequency
of the tones (∆f/f) was fixed at 0.6 during the entire experiment where the three pairs of tones were (1, 0.4
kHz), (4, 1.6 kHz), and (7, 2.8 kHz). Sound pressure level (SPL) was set at 80 dB and the intensity of the
tones was roved by ±5 dB to minimize loudness cues. All cats reached asymptotic performance within the
first 1.5 (±0.5) months (see figure 2 for example). The training periods of 2 cats were before implantation
and the training period of the other 2 cats was interrupted by the implantation.
Experimental data was collected throughout a 4.3 to 5.5 month period of continuous performance
measurement after the conclusion of the training period. The CI stimulator was turned off for a period of one
month during this period (Table 1). Reference frequencies (1, 4, and 7 kHz) were systematically rotated
(Block design) every 9 to 11 days to cover the hearing range of the cats while balancing the order of testing
across both cats and reference frequencies.
2.3 Data analysis
Hit and FA rates (see figures 2 and 3A for example) were analyzed in 100-trial bins. Performance was
measured using detection theory by calculating d’ (d-prime); d' = z(hit rate) - z(FA rate), where z is the
inverse cumulative normal distribution with a mean of 0 and standard deviation of 1 (Heeger, 1997). To help
eliminate trials during which animals were possibly not fully engaged in the discrimination task, a test
session was defined as more than 5 consecutive trials that were less than 5 minutes apart (Benovitski et al.,
2014). Trials outside of sessions did not contribute to performance calculation. A repeated measures 3-way
analysis of variance with the variables stimulator condition (on and off), subjects (n=4), and reference
frequencies (1, 4, and 7 kHz), was conducted to determine the effect of an EAS on frequency discrimination
ability.
3. Results
Overall cats’ performance on the frequency discrimination task was stable over long periods of time (20
days, Figure 2) and repeatable after 2 months (FA rate, figure 3). This is in accordance with data collected
during the method validation (Benovitski et al., 2014). Subjects had a drop in performance, resulting from an
increase in the FA rate, after turning off the stimulator, which did not recover over time; while performance
returned to baseline after the stimulation was turned back on (e.g. solid lines in figure 3B).
Figure 4A shows behavioral performance for each cat, reference frequency (pair number) and stimulation
condition (On/Off). As can be seen, performance was variable among individual animals. C2’s performance
on Pair 1 with the stimulator off, was the worst, but showed a 0.6 increase in d’ with the stimulator on. A
similar increase in performance was seen for C3 for Pair 1 and C4 Pair 3. In contrast, C5 exhibited generally
high performance, with no clear effect of stimulation, possibly due to performance hitting a ceiling level (see
Discussion). Figure 4B shows the behavioral performance at each of the three reference frequencies,
averaged across cats, when the CI was turned on and off. Subjects performed the frequency discrimination
task significantly better (d’ = 2.64 with standard error of means of 0.34, averaged across 3 reference
frequencies) with the CI on compared to the off condition (d’ = 2.32 with standard error of means of 0.11; 3-
way ANOVA, p<0.001). This result was not significantly different among subjects (3-way ANOVA, subject
x on-off condition, p>0.5). However, there was a significant dependence on the reference frequency used (3-
way ANOVA, reference frequency x on-off condition, p<0.03). For reference frequencies 1 and 7 kHz, d’
increased by 0.6 and 0.36 respectively while reduced by 0.01 for 4 kHz. Post hoc t-tests considering on-off
condition for the 1, 4, and 7 kHz reference frequencies were p=0.0015, p=0.4725, and p=0.0041
respectively.
4. Discussion
Partial hearing animals were used to model a clinical condition of CI use in subjects with residual hearing.
This study shows, for the first time, that partially deafened cats can use the information provided by a CI to
improve performance on a frequency discrimination task compared to using their residual hearing alone.
The increase in frequency discrimination performance is despite the fact that the use of a clinical CI system
meant that frequencies represented by the CI were also represented by the residual hearing at different place
along the cochlea (i.e. significant disruption to the normal tonotopic representation). This dual representation
might have caused the ICES to interfere with the acoustic stimulation resulting in a performance drop after
adding ICES. Additionally, previous studies have reported a marked suppression of the acoustic evoked
auditory nerve compound action potential by ICES in guinea pigs (Von Ilberg et al., 1999), which again may
have been expected to result in decreased performance.
Multiple clinical studies have assessed speech recognition performance of partially hearing subjects who
received bimodal EAS (e.g. a CI and a hearing aid in the contralateral ear). The general trend is that patients
with bimodal EAS perform better on speech recognition tasks (for review see Von Ilberg et al., 2011, Firszt
et al., 2008, Ching et al., 2006); however, subject variability is large and some individuals do not benefit
from bimodal EAS. For example, a study by Mok et al. (2006) showed that less than half of their 14 patients
had a significant bimodal benefit. Another study by Tyler et al. (2002) showed a bimodal EAS advantage for
only one of the three patients for words and none for sentences. In fact, in some rare cases hearing
performance can even deteriorate (Hamzavi et al., 2004, Armstrong et al., 1997). These studies conclude that
perceptual ability can be heavily influenced by the amount and quality of residual hearing while bimodal
interaction might be a secondary factor. The animal model used in this experiment is somewhat different
from the usual bimodal clinical case. The residual hearing is similar in the two ears, and there is no
amplification in the non-implanted ear. In the clinical studies, patients have a hearing aid in one ear, usually
that with the better hearing thus direct comparison in performance is impracticable. Nevertheless this animal
model allows direct, within animal, assessment of CI use under conditions where deafening method and
time, as well as previous acoustic experience and environment, are well controlled.
To our knowledge there have been no previous studies of behavioral frequency discrimination performance
of partial hearing animals receiving ICES. There have been multiple studies which assessed ICES in animal
behavioral models (Vollmer et al., 2001, Vollmer and Beitel, 2011, Kral et al., 2006, Klinke et al., 1999,
Beitel et al., 2000). However, results from these studies are not comparable with results from the present
experiment due to: 1) effects of electrical stimulation differ significantly between partially and profoundly
deaf cochlea (Von Ilberg et al., 2011); 2) none of the above studies used a partial hearing, ICES behavioral
model; and 3) conditioning and detection tasks are different from discrimination tasks in terms of their
objectives.
Behavioral performance during the current experiment was measured while presenting EAS or acoustic
stimulation only. As performance on electrode discrimination alone was not available, we can only speculate
about the performance on the same task with only electric stimulation being provided to the animals. Worse
performance could be expected with electric stimulation alone, especially if delivered through a clinical
speech processor with multiple electrodes activated at the same time. One study on which we base this
assumption compared performance of normal hearing, hearing impaired, and CI subjects on a spectral shape
discrimination task and concluded that even hearing impaired subjects are doing better than CI users (Henry
et al., 2005). In another study, three EAS patients with residual hearing, implanted with the Iowa/Nucleus
Hybrid 10-mm short-electrode array performed significantly better compared to standard CI (electric
stimulation only) (Turner et al., 2004).
One limitation of the present study is the possibility of a behavioral measurement ceiling effect which could
partially explain the lack of EAS benefit at 4 kHz (Pair 2). This is evident from figure 4A where it is clear
that the performance of cats C2, C3, and C5 was already high (d’>2.5) for Pair 2 before turning the CI on,
although it must be noted that this does not hold for C3. The hit rate was saturated for all the subjects so the
d’ differences were primarily due to variations in FA rate. The maximum d’ for 100 trials (ideal observer: 49
hits, 1 miss, 49 CRs, and 1 FA) is 4.1; however, in practice a d’ of 4 is rarely achieved (see figure 3). In an
attempt to stay within the usable range of d’, the difficulty level (
∆f/f) was set to 0.6 as in pilot experiments
it generated a d’ level of 2. Nevertheless, it is possible that elevation in d’ at 4 kHz could not be observed
due to the superior performance in the stimulator off condition resulting in a performance ceiling effect.
Another limitation is that the SPL roving used to minimize loudness cues was probably not sufficient,
especially with the 7 kHz reference frequency. The difference between hearing thresholds for 7 and 2.8 kHz
was around 50dB post implantation. The 80 dB SPL tones may have been almost inaudible to cat C5 at 7kHz
but 40 dB above threshold at 2.8kHz; therefore it is possible that some animals may have been able to
perform some part of the auditory only task using just a loudness cue. However, that CI use improved
performance was also seen with the lowest frequency reference, where the auditory threshold was the most
similar, for which the loudness roving should have been sufficient. Finally, it is worth noting that the ICES
levels were set relatively to the electrically evoked ABR thresholds, and therefore should not have contained
any residual loudness cues.
Several studies of partial deafness suggest that frequencies closer to the lesion edge are over-represented in
the cortex (Robertson and Irvine, 1989, Harrison et al., 1991, for review see Pienkowski and Eggermont,
2011). This over-representation has been proposed to underlie the better frequency discrimination
performance in that frequency region seen in some patients (as shown by McDermott et al., 1998). However,
it is clear from figure 4B that performance at 7 kHz was not greater than for the other 2 reference
frequencies. Close examination of cortical activity will be necessary in future experiments to examine
possibility that having a larger area of cortex representing given frequencies does not necessarily mean better
frequency discrimination.
Most human bimodal clinical studies suggest that patients with residual hearing who receive bimodal
auditory input (e.g. CI in one ear and a hearing aid in the other) perform better compared to patients
receiving either acoustic or electric input alone. While the low-frequency hearing of the animals in the
current study is better than the majority of patients in those studies, there is a growing trend towards
implanting patients with increasing amounts of low-frequency hearing. Using this animal model also allows
testing of hearing loss treatments such as neurotrophins (Pettingill et al., 2007) and novel electric stimulation
strategies (e.g. Focused Multipolar Stimulation (van den Honert and Kelsall, 2007)) in ways not possible in
human subjects.
Acknowledgments
This work was funded by the National Institutes of Health (HHS-N-263-2007-00053-C), the National Health
and Medical Research Council of Australia and The Department of Electronic Engineering, La-Trobe
University. The Bionics Institute acknowledges the support it receives from the Victorian Government
through its Operational Infrastructure Support Program. The authors are grateful to Andrew Wise for implant
surgeries; Alison Neil, Nicole Critch and Amy Morley for technical assistance; Sam Irvine for advice; Sue
Pierce for veterinary advice; Sue Mckay for animal maintenance; and Dexter Irvine for comments on the
earlier versions of the manuscript.
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Figures and Tables:
Table 1. Animal details
Cat
Age at
deafening
Age at
implantation
Age at
EAS start
Age at
stimulator
turn off
Age of
stimulator
turn on
Age at
EAS end
C2
7.4
14.3
15.7
17.8
18.8
20
C3
7.4
14.4
15.7
17.8
18.8
20.3
C4
8.3
13.3
15.77
19
20
21.3
C5
8.3
13.3
15.77
19
20
21
All ages are in months and EAS stands for electric and acoustic stimulation.
Figure 1. ABR audiograms of cat C5 before and after bilateral deafening. Values are means (n = 8) of
thresholds for monaural stimulation of the left and right ears, and error bars represent standard deviation.
The inset represents unilateral electrode array placement relative to the characteristic frequencies of the
electrode locations in the cochlea. P1, P2, and P3 represent the different pairs’ frequencies and electrodes
activated during the psychophysical experiment.
0
20
40
60
80
100
120
0.1
1
10
A
BR
T
h
res
h
o
ld
(d
B
SPL
)
Frequency (kHz)
Pre-deafening
Post-deafening
Post-implantation
40
4
P1
P1
P2
P2
P3
P3
7 kHz
250 Hz
Hybrid L (14)
P1
P1
P2
P2
P3
P3
7
Figure 2. Behavioral performance represented in hit and false alarm (FA) rates (plus and cross signs) for cat
C4 before starting reference frequency rotations. The frequencies presented during training were 2 and 0.5
kHz. Each point was calculated over a window of 100 trials. The two lines are linear approximations for hit
and FA rates over the last 45 and 20 days respectively. Hit rate is stable (slope=2E-06; R
2
= 3E-07) at 0.92
throughout 45 days and FA stabilized (slope= -4E-04; R
2
= 1E-03) at 0.23 over the final 20 days indicating
good frequency discrimination ability.
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Day Number
Hit Rate
FA Rate
Figure 3. Example of stimulator turn-off effect on performance of cat C4. A: Experimental time-line. Each
block (P1, P2, and P3) represent 9 to 11 days of different pairs of tones (1, 4, and 7 kHz reference) presented
throughout the experiment. B: Hit and FA rates for 3 different periods of testing at 7 kHz reference
frequency (pair 3, 2.8 & 7 kHz) which was presented at times marked in A. Each point is cumulative
calculation of 100-trial window. Solid lines represent FA average of each period. C: Performance
represented by d’, calculated from hit and FA rates in B. Increase in FA causes reduction of d’ which means
reduction in frequency discrimination ability.
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d'
Stimulator ON | Stimulator OFF | Stimulator ON
0.03125
0.0625
0.125
0.25
0.5
1
0 1 2 3 4 5 6 7 8 9101112131415161718192021222324252627282930313233343536373839404142434445464748495051525354555657585960616263646566676869707172737475
Fa
ls
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Al
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it
Ra
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Pair 3 Hit Rate
Pair 3 FA Rate
(B)
(C)
(A)
Figure 4. A: Behavioral performance with cochlear stimulator on and off for 3 different frequency pairs. B:
Averaged performance across 4 subjects. Performance is measured in d’ calculated from the last 5, 100-trial
sessions (e.g. last 5 data points of each period in figure 3). Error bars represent standard error of the means.
Color is matched to the arrows in figure 1. Asterisks mark reference frequencies for which performance is
significantly better (Bonferroni correction) when the stimulator is turned on (Post hoc t-tests considering on-
off condition for the 1, 4, and 7 kHz reference frequencies were p=0.0015, p=0.4725, and p=0.0041
respectively).
Minerva Access is the Institutional Repository of The University of Melbourne
Author/s:
Benovitski, YB; Blamey, PJ; Rathbone, GD; Fallon, JB
Title:
Behavioral frequency discrimination ability of partially deafened cats using cochlear implants
Date:
2014-09-01
Citation:
Benovitski, YB; Blamey, PJ; Rathbone, GD; Fallon, JB, Behavioral frequency discrimination
ability of partially deafened cats using cochlear implants, HEARING RESEARCH, 2014, 315
pp. 61 - 66 (6)
Persistent Link:
http://hdl.handle.net/11343/43089
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