Edited by: Martin Pienkowski, Salus University, United States
Reviewed by: Shuman He, Boys Town National Research Hospital, United States; Dan Zhang, Tsinghua University, China
*Correspondence: Kanthaiah Koka
This article was submitted to Auditory Cognitive Neuroscience, a section of the journal Frontiers in Neuroscience
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
Although cochlear implants (CI) traditionally have been used to treat individuals with bilateral profound sensorineural hearing loss, a recent trend is to implant individuals with residual low-frequency hearing. Patients who retain some residual acoustic hearing after surgery often can benefit from electro-acoustic stimulation (EAS) technologies, which combine conventional acoustic amplification with electrical stimulation. However, interactions between acoustic and electrical stimulation may affect outcomes adversely and are time-consuming and difficult to assess behaviorally. This study demonstrated the feasibility of using the Advanced Bionics HiRes90K Advantage implant electronics and HiFocus Mid Scala/1j electrode to measure electrocochleography (ECochG) responses in the presence of electrical stimulation to provide an objective estimate of peripheral physiologic EAS interactions. In general, electrical stimulation reduced ECochG response amplitudes to acoustic stimulation. The degree of peripheral EAS interaction varied as a function of acoustic pure tone frequency and the intra-cochlear location of the electrically stimulated electrode. Further development of this technique may serve to guide and optimize clinical EAS system fittings in the future.
Because of advances in electrode array technology and surgical technique, patients with low-frequency residual acoustic hearing could benefit from cochlear implants (CI) (Balkany et al.,
One of the challenges in optimizing EAS benefit in individual patients is understanding the interactions between acoustic and electrical hearing. Psychometric studies indicate that acoustic thresholds can be increased in the presence of electrical stimulation, thereby suggesting peripheral electro-acoustic interactions (Lin et al.,
Consequently, it would be valuable to take advantage of objective responses to help clinicians program EAS devices optimally. The electrically evoked compound action potential (ECAP) is a physiologic response that reflects auditory nerve activity and can serve as an objective measure of electro-acoustic interactions in the same ear (Abbas et al.,
Electrocochleography (ECochG) is a procedure that offers potential for assessing peripheral electro-acoustic interactions objectively. The ECochG response is comprised of electrical potentials generated by the hair cells and auditory nerve. The cochlear microphonic (CM) represents the combination of transducer currents primarily through the outer hair cell stereocilia (Dallos,
To date, the ability to measure ECochG responses in the presence of electrical stimulation in CI recipients has been limited by CI hardware capability due to stimulus artifacts. However, the back-telemetry capability and fast-recovery amplifier in the Advanced Bionics (AB) HiRes90K® cochlear implant offers the opportunity to measure ECochG responses reliably and to explore the feasibility of using ECochG to assess peripheral electro-acoustic interactions. the AB device can record ECochG responses to low frequency pure tones. By calculating the
This study explored the feasibility of using ECochG to assess electro-acoustic interactions objectively in implanted subjects with residual hearing in the presence of electrical stimulation. The study focused particularly on using the fast-recovery amplifier in the AB HiRes90K® cochlear implant to measure ECochG responses. The objective of the study was to show that it is feasible to record the
Two methods were used to explore the interaction between acoustic and electrical stimulation in CI recipients with residual hearing. Experiment 1 evaluated the feasibility of recording acoustic ECochG responses in the presence of electrical stimulation. Those responses then were used to estimate electro-acoustic interactions objectively. Experiment 2 assessed electro-acoustic interactions behaviorally by measuring changes in acoustic thresholds in presence of electrical stimulation. These behavioral interactions then were compared with the objective electro-acoustic interactions from Experiment 1.
The aim of this experiment was to show the feasibility of recording acoustic ECochG responses in the presence of electrical stimulation. The
Twelve CI recipients with Advanced Bionics HiRes90K® cochlear implants and HiFocus MidScala® and 1J electrode arrays participated in this phase of the study. Eleven subjects were unilaterally implanted and one subject was a bilateral implant user, thereby yielding a total of 13 experimental ears. Table
CI03 | HiRes90K Advantage | MidScala | 0.25 | yes | yes |
CI04L | HiRes90K Advantage | MidScala | 1 | yes | yes |
CI04R | HiRes90K Advantage | MidScala | 2 | yes | yes |
CI06 | HiRes90K Advantage | MidScala | 0.5 | yes | yes |
CI07 | HiRes90K Advantage | MidScala | 2 | yes | no |
CI08 | HiRes90K Advantage | MidScala | 1.67 | yes | yes |
CI09 | HiRes90K Advantage | MidScala | 1.5 | yes | no |
CI11 | HiRes90K | HiFocus 1J | 3 | yes | no |
CI12 | HiRes90K Advantage | MidScala | 1.5 | yes | no |
CI13 | HiRes90K Advantage | MidScala | 0.5 | yes | yes |
CI15 | HiRes90K Advantage | MidScala | 0.5 | yes | yes |
CI16 | HiRes90K Advantage | MidScala | 2 | yes | no |
CI19 | HiRes90K Advantage | MidScala | 1.5 | yes | no |
Pure tone audiograms for 12 study participants.
The stimulus delivery and measurement system for assessing ECochG responses was like that described in Koka et al. (
The acoustic stimulus for ECochG recording consisted of 50-ms tone bursts with a ramp duration of 5 ms (Hanning window) presented at each subject's most comfortable level (MCL) or at maximum stimulus level generated by test system at test frequency. ECochG responses were recorded using 240 presentations with alternating polarity (120 rarefaction and 120 condensation). From the responses to alternating polarities, the
The electrical stimulus consisted of a 50-ms biphasic pulse train with a phase duration of 36 μS. The inter-pulse gap was varied to produce pulse rates that ranged between 400 and 1,200 pulses per second (pps). The pulse trains were delivered at each subject's MCL. Electrical stimuli were delivered to either electrode 2 or electrode 3 in a monopolar manner using the case ground as the return electrode. Electrode 1 was used as the recording electrode. In some cases, electrode 2 was used as the recording electrode, and then either electrode 1 or 3 was used for stimulation. In the AB system, electrode 1 is the most apical electrode.
For recording, the ring electrode, located on the electrode lead outside of the cochlea, served as the reference electrode for the differential recording amplifier. The amplifier on the HiRes90K® Advantage implant was configured to have a gain of 1,000. Data were sampled at a rate of 9,280 sample/s, thus supporting a fast Fourier transform (FFT) up to 4,000 Hz. The response amplitudes were estimated as the peak value at stimulus frequency in the FFT spectrum. With these settings, the AB implant offers a relatively long recording window of 54.4 ms that can record ECochG waveforms for low-frequency stimuli down to 125 Hz.
The procedure used for electro-acoustic interaction was simultaneous presentation of electric and acoustic stimuli. The electrical pulse rates and acoustic frequencies were kept disparate so that the acoustic responses could be differentiated from electrical stimulus artifacts in the FFT spectrum. Figure
Experimental procedure used for estimating physiological electro-acoustic interactions for simultaneous stimulations.
The electric-only responses were subtracted from electro-acoustic responses. This subtracted response was defined as the
Different electrodes were used for electrical stimulation and recording of ECochG responses to minimize stimulus artifact contamination of the recordings. The fast-recovery property of the evoked potential recording amplifier designed into the HiRes90K® Advantage cochlear implant allowed the amplifier, when it encountered large saturating stimulus artifacts, to quickly return from saturation into linear operation. This capability permitted recording of responses immediately after the stimulus artifact ended. Thus, electrical pulse rates closer to clinical stimulation rates could be explored to determine the feasibility of using this ECochG technique to complement everyday clinical programming.
The aim of this experiment was to estimate electro-acoustic interactions using a behavioral masking technique, i.e., the elevation of acoustic thresholds in the presence of an electrical stimulus masker. These behavioral electro-acoustic interactions were compared with the objective electro-acoustic interactions estimated in Experiment 1.
A subset of the 6 subjects who participated in Experiment 1 took part in this phase of the study. Five were unilaterally implanted and one had two devices, resulting in a total of seven experimental ears. Table
The experiment was conducted in a quiet room. If required, a foam plug was introduced in the contralateral ear to avoid distraction. The acoustic probe stimuli consisted of tone bursts at 125, 250, 500, 750, 1,000, and 2,000 Hz. The tone duration was 200 ms with 10-ms on/off ramps.
The electrical masker consisted of 500-ms pulse train of (cathodic first) biphasic pulses with phase durations of approximately 36 μs. The pulse rate was kept constant at 421 pps. Electrical stimulation was delivered at the same MCLs used in Experiment 1. When the probe and masker were delivered simultaneously, the acoustic tone burst was centered temporally within the electrical pulse train. The experimental design was similar to Lin et al. (
Unmasked and masked acoustic thresholds were measured using a three-interval, forced-choice procedure with a three-down-one-up search rule. Initially within a run, the acoustic stimulus levels were varied in 8-dB steps. After three reversals, the step size was reduced to 2 dB. Thresholds were calculated by averaging six reversals with a step size of 2 dB. Thresholds were measured for each acoustic stimulus presented alone and with the electrical masker. The threshold track was aborted if the acoustic signal level exceeded the maximum stimulation limit. Any changes in acoustic thresholds in the presence of electrical stimulation from the unmasked condition were evidence of electro-acoustic interactions.
Figure
The time domain data show no visible residual stimulus artifacts after template subtraction. The frequency spectra show some stimulus artifacts around 1,160 Hz which appear to be harmonic or at the electrical stimulation rate. Nonetheless, these stimulus artifacts were clearly different from the
Figure
Figure
Comparison of
Figure
Behavioral threshold change vs. acoustic test frequency for a representative subject CI04L. An electrical masker of 421 pps was applied to either electrode 1 or electrode 3.
Figure
Behavioral threshold changes and
Figure
This study demonstrates the feasibility of measuring acoustic ECochG responses in the presence of electrical stimulation using the HiRes90K® Advantage cochlear implant. The fast-recovery amplifier enabled measurement of acoustic
Furthermore, this is the first study to demonstrate that ECochG can be used to evaluate electro-acoustic interactions in CI recipients with residual hearing. The degree of electro-acoustic interaction was dependent on location of the stimulation and recording electrode, as well as acoustic frequency (Figures
Decrease in acoustic responses due to electrical stimulation on electrode 1. The decrease in amplitudes (indicating presence of electro-acoustic interactions) were plotted with respect actual
Stronks et al. (
In summary, it is feasible to assess electro-acoustic interactions objectively in CI recipients with residual hearing. Further studies will explore stimulus-level-dependent electroacoustic interactions and whether these objective data can be used to guide fitting of EAS technology. Long-term, the goal is to be able to fit clinical EAS systems (1) without dependence on time-consuming psychometric methods and (2) in patients unable to undergo behavioral testing.
It is feasible to record ECochG responses in the presence of electrical stimulation in HiRes90® Advantage CI recipients with residual hearing, thus providing a method for objectively assessing electro-acoustic interactions.
The HiRes90K® Advantage fast-recovery recording amplifier allows electro-acoustic interactions to be measured at high electrical stimulation rates with minimal stimulus artifacts.
Future studies are required to understand the relationship between behavioral and objective electro-acoustic interactions.
Both authors contributed for conception and design, acquisition of data, or analysis and interpretation of data and drafting the article.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors would like to thank all the subjects who participated in the study and Lupe Navarro and Maria Holloway for organizing their visits.