Research PaperImpact of stimulus frequency and recording electrode on electrocochleography in Hybrid cochlear implant users
Introduction
Traditionally, cochlear implant (CI) candidates had bilateral, severe-to-profound sensorineural hearing loss. However, recent advancements in electrode array design and changes in surgical techniques have made preservation of acoustic hearing in the implanted ear a reality. Today, patients with good low-frequency hearing but high-frequency hearing loss can be implanted using an electrode array designed to preserve their acoustic hearing. These CI users are able to combine acoustic low-frequency information and electric high-frequency information from the same ear (electric-acoustic stimulation, EAS). While hearing preservation post-implant is possible for many patients, a percentage experience some loss of acoustic hearing immediately post-op and others experience a delayed onset hearing loss, typically within the first year post-implant (Kopelovich et al., 2015; Scheperle et al., 2017). This unfortunate outcome led several researchers to consider novel ways to assess cochlear health.
The neural telemetry systems of all three major CI manufacturers (Cochlear Ltd., Advanced Bionics, and MED-EL) have traditionally been used to record electrically evoked compound action potentials from an intracochlear electrode (Brown et al., 1998; Abbas et al., 1999). For patients with residual acoustic hearing post-implant, the telemetry system can be adapted to record acoustically evoked electrocochleograms (ECoG) from an intracochlear electrode (Acharya et al., 2016; Campbell et al., 2015; Campbell et al., 2016; Abbas et al., 2017; Koka et al., 2017; Kim et al., 2018; Tejani et al., 2019). The ECoG is a complex response that includes contributions from cochlear hair cells as well as neural components [Cochlear Microphonic (CM), Summating Potential (SP), Compound Action Potential (CAP) and Auditory Nerve Neurophonic (ANN)]. Because it can be recorded non-invasively post-implant, the ECoG is increasingly viewed as a measure that may help characterize and monitor the status of the peripheral auditory system over time and potentially provide clues as to the underlying cause of delayed onset hearing loss that some EAS CI listeners experience.
Typically, the ECoG is recorded from the most apical intracochlear electrode in the array. The assumption is that ECoG response magnitudes will be largest for this recording electrode given its proximity to the region of the basilar membrane where there are more functional hair cells and where residual acoustic hearing is best. However, previous studies have shown that is not always the case (Dalbert et al., 2015; Campbell et al., 2015; Campbell et al., 2016; Bester et al., 2017; Harris et al., 2017). For example, Campbell et al. (2015) performed ECoG recordings post-operatively and reported CM amplitudes increased for most individuals as the recording electrode was moved apically across the array. For other subjects, larger CM and ANN amplitudes were recorded from the most basal electrode. Dalbert et al. (2015) reported finding minimal changes in post-operative ECoG magnitude regardless of the intracochlear recording electrode that was used. Intraoperative data, obtained during electrode array insertion (Campbell et al., 2016; Harris et al., 2017) or immediately post-insertion (Bester et al., 2017), has shown CM amplitudes that increase as the recording electrode is inserted toward the apex for some subjects, a maximum response for others occurs at a point midway into the insertion for other subjects, and in some individuals no change is observed with insertion. Most studies used a single stimulus frequency and focused primarily on the CM response. The magnitude of the hearing losses also varied significantly across these studies.
Changes in CM phase as a function of place along the cochlea has also recently received attention in intracochlear ECoG for its potential applications in intraoperative monitoring of cochlear trauma during CI surgeries (Campbell et al., 2017; Koka et al., 2018; Giardina et al., 2019). Preliminary studies have proposed real-time monitoring of CM amplitudes as the electrode array is inserted, as drops in CM amplitude may be indicative of cochlear trauma, leading to partial or complete loss of the patient’s acoustic hearing post-operatively (Campbell et al., 2016; Dalbert et al., 2018; but see Adunka et al., 2016; O’Connell et al., 2017). However, Koka et al. (2018) and Giardina et al. (2019) proposed incorporating CM phase information when interpreting CM magnitude changes. Specifically, they hypothesized that drops in CM magnitudes concurring with large shifts in the starting phase of the ongoing CM response may not be indicative of cochlear trauma, while drops in CM magnitudes with minimum shifts in phase may be indicative of cochlear trauma (e.g. loss of acoustic hearing or scalar translocation of the electrode array). Similarly, normal-hearing animal literature has also shown some evidence of phase shifts for apical recording sites relative to basal recording sites (Tasaki et al., 1952; Pfeiffer and Molnar, 1970; Kohllöffel, 1970; Kim et al., 1980).
In the present study we describe the effect that recording electrode position and stimulus frequency have on both CM and ANN responses for a group of six Cochlear Nucleus L24 Hybrid CI users with good low-frequency acoustic hearing (e.g. thresholds in the mild to moderate range). These are typical EAS CI candidates and patients likely to be interested in preserving acoustic hearing post implant. Our goal is to more fully characterize the impact of recording electrode and stimulus frequency on both CM and ANN response amplitude and to use our data to suggest optimal recording parameters. We hypothesize that for a given frequency tone burst, moving the recording electrode basally should result in reduced CM and ANN amplitudes. Similarly, because these subjects have a sloping audiometric configuration, we hypothesize that for a fixed recording electrode, decreasing the tone burst frequency should result in larger CM and ANN response amplitudes. As a secondary aim, we also explored the effect of recording electrode location on phase of the CM and ANN responses.
Section snippets
Participants
Six adults (age = 55–84 years) participated in this study. All used the Cochlear Nucleus Hybrid L24 electrode array (insertion depth = 16 mm; Roland et al., 2016), and were implanted at the University of Iowa Hospitals and Clinics between 2016 and 2017. Fig. 1 shows individual preoperative and postoperative unaided audiograms from the implanted ear. Postoperative audiograms were obtained at the time of testing. Table 1 details subject demographics. The electrode arrays were implanted via the
Results
Fig. 2 shows results obtained using a 500 Hz tone burst from recording electrode 22 for subject L68R. The left panel shows raw condensation and rarefaction recordings, the middle shows the resulting CM/DIF and ANN/SUM potentials and the right shows their FFTs. Higher harmonics are also occasionally present in the FFT. For the CM/DIF FFT, a small peak at 1500 Hz was noted in addition to the 500 Hz peak. The 1500 Hz peak may reflect distortion caused by saturation in hair cell transduction at
Discussion
The goal of this study was to systematically explore the effect of recording electrode location and stimulus frequency on ECoG recordings. Consistent with our hypothesis, results showed that when stimulus frequency was held constant, moving the recording electrode basally resulted in a decrease in response amplitude (Fig. 3A). This trend was most apparent when a low frequency tone burst was used (e.g. 250 Hz and 500 Hz) and is consistent with ECoG studies where an apical peak was observed (
Declaration of competing interest
The authors declare that there is no conflict of interest in relation to this work.
Acknowledgements
This study was supported by NIH/NIDCD (P50 DC000242). We are grateful to all participants for their time and to the University of Iowa Cochlear Implant team for their clinical care of our study participants.
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