Intracochlear and extracochlear ECAPs suggest antidromic action potentials
Introduction
With the establishment of clinical systems such as “neural responses telemetry” (NRT), the ability to obtain electrically evoked auditory nerve potentials from cochlear-implant users has become commonplace. Several research groups have characterized the electrically evoked compound action potential (ECAP) as a response occurring within the first millisecond after stimulus onset, dominated by a relatively large-amplitude negative peak followed by a smaller positive peak (Brown et al., 1990; Abbas et al., 1999; Dillier et al., 2002; Frijns et al., 2002). Multiple groups have been investigating the clinical utility of ECAP measures, including possible application to adjusting device parameters to individual users, predicting nerve survival, and using repeated measures for longitudinal monitoring of nerve status (Hughes et al., 2000, Hughes et al., 2001; Franck and Norton, 2001; Smoorenburg et al., 2002; Zimmerling and Hochmair, 2002; Cohen et al., 2003).
Useful interpretations of intracochlear ECAPs require a firm understanding of the neural excitation process and the propagation of neural potentials through cochlear and extracochlear tissues. Perhaps an ultimate goal is the development of a computational model of the implanted cochlea with sufficient accuracy to account for electrophysiological measures from humans and animals and a variety of stimulation conditions. Animal model data provide the critical means of validating computational model predictions, as cochlear and nerve status can be controlled and a wide variety of parameters explored. There have been impressive gains in computational modeling of the electrically stimulated cochlea (e.g., Finley et al., 1990; Frijns et al., 1995, Frijns et al., 2001; Rubinstein, 1995), however, no model yet exists that can accurately predict most of the fundamental aspects of ECAPs reported from animal studies.
Several properties of the ECAP have been explored using animal models. Although some have been obtained using intracochlear recording sites (Brown and Abbas, 1990; Haenggeli et al., 1998), most animal data have been collected using sites on or near the surgically exposed nerve trunk (Nagel, 1974; Prijs, 1980; Stypulkowski and van den Honert, 1984; Miller et al., 1998). While a nerve-trunk recording site is preferred for its superior isolation from stimulus artifacts, it is not optimal for approximating the human ECAPs recorded from intracochlear sites. No within-subject comparisons of potentials from the two sites have been made. However, across-study comparisons of cat ECAPs indicate that the latency of the main negative peak of the intracochlear ECAP is short (i.e., 0.26 ms, Brown and Abbas, 1990) compared to latencies of 0.25–0.55 ms measured at the nerve trunk (Stypulkowski and van den Honert, 1984; Miller et al., 1998). Furthermore, nerve-trunk ECAP latencies are strongly dependent upon stimulus polarity (Miller et al., 1998), suggesting that stimulus polarity affects the site of action potential initiation on the peripheral-to-central dimension of the nerve fibers.
ECAP recordings from humans and animals reveal significant differences. One fundamental difference is ECAP morphology. Animal studies often report ECAPs consisting of three peaks, including a positive (“P1”) peak that precedes the dominant negative peak. This triphasic morphology is rarely, if ever, observed in human ECAPs recorded by NRT systems or other protocols (Brown et al., 1990; Wilson et al., 1994; Abbas et al., 1999). Related to this morphology difference is the fact that the negative (“N1”) potential from humans has a shorter latency than that observed in most animal studies. It is not known to what extent these differences arise from species-specific anatomy, cochlear pathologies of implant patients, or the site of the recording electrodes. Other differences between human and animal ECAPs arise from limitations of clinical stimulation. For example, the strong stimulus-polarity effects recorded from animals (Miller et al., 1998) have not been observed in humans, presumably because monophasic stimuli are not used with the latter group. It is not known how such polarity effects would influence animal ECAPs recorded at intracochlear sites.
Given these issues, it is clear that within-subject comparisons of ECAPs recorded at intracochlear and nerve-trunk sites are needed. Such comparisons could include many experimental variables, including intracochlear electrode design and relative and absolute position of intracochlear electrode sites. For this study, however, we focused on three parameters that have been shown to strongly influence the site of action potential initiation: (1) electrode configuration; (2) stimulus polarity, and; (3) stimulus level. Monophasic stimulus pulses were used to explore polarity effects and a feline-scaled version of the Nucleus banded electrode array was used for intracochlear stimulation and recording.
Section snippets
Surgical preparation
Four adult cats free of visible middle ear pathology were used in acute experiments, with all procedures conducted while the subject was under a surgical level of anesthesia. Procedural details are described in Miller et al. (2003). Briefly, after induction of anesthesia, the cat’s head was immobilized by a bite bar. The nerve was accessed by the posterior fossa approach to allow placement of a linear array of recording electrodes above the nerve trunk. The bulla was opened and the round window
Results
Examples of feline ECAPs recorded from both intracochlear and nerve-trunk sites are shown in Fig. 1, Fig. 2 for both cathodic and anodic stimulus pulses. Fig. 1 shows responses obtained at several stimulus levels for monopolar (electrode I8 to ground) stimulation, while Fig. 2 shows responses to several bipolar (I8–I7) stimuli. Residual stimulus artifacts can be seen at −0.5 and 0.0 ms, corresponding to the imperfect subtraction of the masker and probe stimulus artifacts, respectively. Most
Main findings
This paper presents direct comparisons of ECAPs obtained from both intracochlear and nerve-trunk recording sites. As human ECAPs are recorded using intracochlear recording sites, this comparison has been needed in order to define differences between findings from humans and animal model studies. The data demonstrate several differences between intracochlear and nerve-trunk ECAPs. First, typical intracochlear amplitudes were almost an order of magnitude greater than the nerve-trunk amplitudes.
Acknowledgement
The feline research was supported by NIH Contract N01-DC-9-2107. Studies with human participants were supported by NIH/NIDCD Grant P50 DC 00242 and the Iowa Sight and Hearing Foundation.
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