Cochlear implants traditionally have been used to treat individuals with bilateral profound sensorineural hearing loss. However, given the evolution of electrode and signal-processing technology and improved surgical techniques, individuals with low-frequency residual hearing also are able to experience benefit from a cochlear implant (Balkany et al., 2006; Fraysse et al., 2006). Moreover, by combining electrical and acoustic stimulation (EAS), benefit exceeds that of using a hearing aid or a cochlear implant alone (Von Ilberg et al., 1999; Turner et al., 2008).

In order to benefit optimally from EAS technologies, residual hearing in these subjects must be preserved. However, at least 50% of subjects lose their residual hearing after surgery (James et al., 2005; Balkany et al., 2006; Brown et al., 2010; Lenarz et al., 2013; Roland et al., 2016). The loss of residual hearing is attributed mainly to, direct trauma to the basilar membrane (Roland and Wright, 2006; Li et al., 2007) and not due to any potential interference produced by the presence of the electrode in the cochlea(Donnelly et al., 2009; Huber et al., 2010; Greene et al., 2015; Banakis et al., 2016). But several researchers have reported increased air-bone gaps (ABG) post-operatively in a subset of subjects after cochlear implantation despite using surgical techniques to reduce trauma (Attias et al., 2012; Chole et al., 2014; Raveh et al., 2014; Mattingly et al., 2016), thus suggesting that conductive components may be involved that can be attributed to the changes in middle ear mechanics and/or the presence of electrode in the cochlea.

Figure 1 shows an example audiogram from a CI recipient with residual hearing showing large ABGs. These ABGs are difficult to quantify because post-operative hearing sensitivity is exclusively measured with air-conduction (AC) thresholds because bone-conduction (BC) thresholds are technically difficult to assess in individuals with severe-to-profound hearing loss. Specifically, high levels of bone oscillator stimulation in the low frequencies can result in vibrotactile sensations mistakenly reported as audible, thereby contributing to a false increase in ABG. Also, due to smaller transcranial attenuation unmasked BC thresholds may be measured due to the stimulation of the cochlea in the non-test ear. Typically, the contralateral ear is masked with a band of noise to facilitate measurement of BC thresholds in the test ear. However, limited hearing in the contralateral ear may limit the ability to measure masked BC thresholds and lead to inaccurate ABG measurement. Also, it is not possible to accurately measure BC thresholds in patients and children who cannot provide accurate responses to BC stimulation.

Because of these technical barriers to evaluating behavioral BC thresholds, it would be helpful to have an objective method to measure AC and BC thresholds for estimating ABG in implant patients with residual hearing. Koka et al. (2016) and Abbas et al. (2017) used the intra-cochlear electrodes from the implant array to measure electrocochleography (ECochG) in patients with residual hearing. Different electrical potentials such as cochlear microphonics (CM), compound action potential (CAP), summating potential (SP), and auditory nerve neurophonics (ANN) together constitute ECochG responses. The CM represents the combination of transducer currents primarily through the outer hair cell stereocilia (Dallos, 1973) and is known to follow the fine structure of the stimulus waveform. The ANN is assumed to reflect the phase locking activity of the auditory nerve fibers (Snyder and Schreiner, 1984; Lichtenhan et al., 2013; Fitzpatrick et al., 2014; Forgues et al., 2014). The CAP is generated by the auditory nerve in response to the onset and offset of the acoustic stimulus, and the SP is the direct current part of the response with multiple generators. The present study focuses on the alternating current components of the ongoing, or steady state, response to tones. The difference response, which is the difference between alternating polarities, emphasizes responses at odd harmonics of the tone frequency, which are those components of the response that change with stimulus phase. Thus, the difference response is dominated by the CM, but also includes the largest part of the ANN that is periodic with the signal. Current study focused mainly on CM responses. The summation response, which is the summation of alternating polarities, emphasizes responses at even harmonics of the tone frequency, and include the components of the response that do not change with stimulus phase. Thus, the summation response includes the asymmetric distortions present in the CM and ANN. Because these distortions are greater in the ANN than the CM, the ongoing component of the summation response can be dominated by the ANN, when it is present. However, this part of the ANN is only the distortions, and so is smaller than the part that appears in the difference response. That there is some ANN present in the difference response was shown by Forgues et al. (2014), who demonstrated a decrease in difference response by introducing a neurotoxin used to suppress auditory nerve response.

This study extends the (Koka et al., 2016) study to evaluate whether CM (which is the difference response) can be used to estimate BC thresholds in implanted patients with residual hearing. Because CM necessarily rules out any vibrotactile responses and contributions from the contralateral ear, it may be applicable for estimating BC thresholds at low frequencies. Thus, this study assessed CM responses for AC and BC stimuli in cochlear implant recipients with residual hearing.

This study measured pure-tone audiometric thresholds and CM thresholds for AC and BC stimulation in four implanted individuals with residual hearing. Across the range of test frequencies, behavioral sensitivity and CM thresholds were highly correlated for both AC and BC stimulation. Moreover, the ABG estimated by the ECochG responses provided a reliable surrogate for behavioral ABG in these subjects.

These results are similar to Koka et al. (2016) for AC thresholds and to Abbas et al. (2017) who showed that CM thresholds approximated behavioral AC thresholds better than auditory nerve neurophonics or compound action potential thresholds. Unique to this study is the demonstration that ECochG responses to BC stimulation can provide an objective indicator of BC thresholds that are not corrupted by vibrotactile responses and does not require contralateral masking. One caveat is that care should be taken to limit BC vibrator output so as not to create electromagnetic artifacts at high stimulus levels. These results suggest that ECochG can be used as an objective tool to verify behavioral BC thresholds in CI patients with residual hearing and ABG. In implant patients, intra-cochlear electrode is used to measure ECochG which simplifies the measurement of evoked potentials especially in pediatric patients.

With the observation that ABG may exist after implantation of patients with residual hearing (Chole et al., 2014; Raveh et al., 2014; Mattingly et al., 2016) and in normal-hearing animals after implantation (Hod et al., 2016), this ECochG method can provide an objective tool to estimate reliable ABG without technical issues of measuring behavioral BC thresholds in CI subjects. The fact that this group of subjects had ABG in the presence of normal tympanometry suggests that the ABG originated in the inner ear rather than the middle ear. On the other hand acute studies looking at effect of electrode in the cochlea did show only less than 5 dB differences between air and bone conduction in temporal bones (Donnelly et al., 2009; Huber et al., 2010; Greene et al., 2015; Banakis et al., 2016). Quesnel et al. (2016) suggested that the changes in residual hearing after initial preservation may be due to intracochlear fibrosis and new bone formation changing the compliance of round window and not due to degeneration of hair cells. The current EcochG measurement may acts a tool to monitor ABG chronically and understand whether the increased ABG is due to chronic changes in the cochlea.

ECochG responses can provide an objective method for estimating ABG in cochlear implant recipients with residual hearing in the implanted ear.

Authors equally contributed to conception and design, drafting the article; and final approval of the version to be published and KK and AS contributed for acquisition of data, analysis and interpretation of data.