Research paperEffects of stimulus manipulation on electrophysiological responses in pediatric cochlear implant users. Part I: Duration effects☆
Introduction
In cochlear implant users, the sense of audition is typically lost as a consequence of cochlear dysfunction. Perception of sound can be realized by bypassing the cochlea and directly stimulating the auditory nerve with trains of electrical pulses delivered by a cochlear implant. Although the effects of electrical stimulus intensity on the auditory pathways have been well documented (van den Honert and Stypulkowski, 1986, Stephan et al., 1990, Abbas and Brown, 1991, Gallego et al., 1999, Firszt et al., 2002, Eisen and Franck, 2005), effects of pulse train duration or rate of pulse presentation are less clear. Moreover, stimulus effects on auditory activity could depend on the area of the auditory pathway being measured and may or may not be perceived. In the present study, we focused on the duration of electrical pulse train presentation and asked: Does increasing pulse train duration affect evoked auditory activity in children using cochlear implants as measured by (a) behavioral thresholds; and (b) electrophysiological responses of the auditory brainstem and thalamo-cortex?
We are specifically interested in the effects of stimulus changes in children as electrophysiological measures in this population could help to predict behavioral responses which are used for cochlear implant fitting. For each cochlear implant user, stimulation parameters must be customized for each stimulating electrode along the implanted array. Behavioral measures are typically used to establish threshold (T) levels of current (the lowest levels of current required to elicit a response) as well as maximum comfort (C) levels (loudest sound that the subject would be willing to listen to for an extended period of time). However, behavioral testing is not always possible particularly in very young children and alternative measures of threshold determination are required. One such alternative is the use of electrophysiological measures to determine threshold levels. Electrophysiological responses most commonly used to evaluate hearing thresholds include the electrically evoked auditory brainstem response (EABR) which reflects activity in the auditory nerve and brainstem (van den Honert and Stypulkowski, 1986) and the electrically evoked middle latency response (EMLR) which reflects activity in the auditory thalamus and cortex (Kraus and McGee, 1993, Kraus and McGee, 1995, Gordon et al., 2005). The benefits of these electrophysiological measures include their ability to be performed at any age and for any level of patient capacity.
Electrophysiological and behavioral thresholds have been correlated in the literature in both animal and human models. Comparison of EABR thresholds with behavioral thresholds using identical low-rate, short duration stimuli was demonstrated with excellent correlation in cats (Smith et al., 1994). In human studies, behavioral and electrophysiological thresholds have typically not been evoked by the same stimuli; electrophysiological responses of the auditory nerve and brainstem are evoked by a single pulse stimulus while behavioral testing employs longer duration pulse trains of approximately 500 ms. Although the two measures are significantly correlated, EABR thresholds were found to consistently fall at levels higher than behavioral thresholds and closer to the maximum comfort levels (Shallop et al., 1991, Abbas and Brown, 1993, Brown et al., 1994, Brown et al., 1999, Brown et al., 2000, Firszt et al., 1999; Gordon et al., 2004).
It has been suggested that the difference between electrophysiological and behavioral thresholds is a result of temporal integration evoked by the increased number of electrical pulses presented by higher rate and longer duration stimuli used to elicit behavioral responses (Shallop et al., 1991, Brown, 2003). Temporal integration is thought to occur either because the auditory system acts as a long-term integrator of stimulus energy (Plomp and Bouman, 1959, Zwislocki, 1960) or, as the result of multiple “looks” at the signal over a short time (<10 ms), that is, multiple short samples of processed signal stored in short-term memory to help the listener detect the signal (Viemeister and Wakefield, 1991). This increase in neural activity due to differences in stimulus rate and duration could explain, at least in part, why behavioral thresholds are typically lower than electrophysiological thresholds. We address the issue of duration effects in the present paper and effects of stimulus rate in our companion paper (Davids et al., 2008).
It is plausible that by altering stimulus properties such as duration and rate of stimulation for electrophysiological recordings, we could take advantage of the properties of temporal integration and promote decreases in response thresholds thereby improving the ability to predict behavioral thresholds using electrophysiological responses. To do this, we must first prove that short latency electrophysiological measures can be effectively recorded using long duration pulse trains.
The electrical pulses from a cochlear implant can be 2 orders of magnitude larger in amplitude than the evoked auditory response and can therefore, obscure short latency responses such as the electrically evoked auditory nerve potential (EAP) (Miller et al., 2000) and early EABR latencies such as waves eI to eIII (van den Honert and Stypulkowski, 1986, Miller et al., 1993a, Miller et al., 1993b). Whereas random sources of artifact can be minimized by averaging multiple recording sweeps, this approach will not reduce stimulus artifact in cochlear implant users. A number of methods have been used to decrease the electrical stimulus artifact from electrophysiological responses including the use of a forward masking paradigm (Brown and Abbas, 1990, Miller et al., 2000). This approach is available in the telemetry systems of some cochlear implants which can measure the EAP but not later latency responses. Tri-phasic pulses could better limit the temporal spread of the stimulus artifact (Schoesser et al., 2001), however, these are not used in current cochlear implant devices. Alternating the polarity of the pulse stimulation might also reduce the stimulus artifact in averaged responses (Eisen and Franck, 2004, Alvarez et al., 2007) but there is evidence that neural responses to cathodic pulses are different from those to anodic pulses (Shepherd and Javel, 1999) thus potentially compromising the averaged response. Without using these strategies, we hypothesized that an increase in pulse train duration would: (1) obscure neural responses over an increasing latency range and (2) result in decreased thresholds of responses still visible beyond the stimulus artifact.
Section snippets
Subjects
Ten cochlear implant users, aged 6.2–17.9 (mean 10.9) years at activation, with 0.3–6.1 (mean 1.2) years of implant experience voluntarily enrolled in the study. Consent was obtained from the parent/caregiver and participant prior to testing. The characteristics of the participants are listed in Table 1. User devices included the Nucleus 24RE (n = 8) and the Nucleus 24RCS (n = 2). Onset of hearing loss was pre-lingual in 5 children, peri-lingual in 4 children and post-lingual in 1 child. No
Results
Behavioral threshold responses were obtained for five subjects in response to 2 and 40 ms pulse bursts at 500 pps. Fig. 2 plots mean (±1 SE) thresholds evoked by both the basal and apical implant electrodes. There was a statistically significant reduction in thresholds as duration was increased from 2 to 40 ms for responses evoked by both the basal (t(4) = 2.75, p = 0.01) and apical (t(4) = 6.00, p < 0.0001) electrodes. There was no electrode effect (basal versus apical) on thresholds as duration was
Discussion
It would be of great benefit, particularly to the pediatric population, to be able to rely on electrophysiological threshold determination to predict behavioral thresholds when programming cochlear implants. Unfortunately electrophysiological thresholds tend to be higher than behavioral comfort levels by 30–40 clinical current units (Pfingst, 1988, Smith et al., 1994, Brown, 2003, Hughes et al., 2001, Gordon et al., 2004a). Two stimulus parameters that may contribute to this discrepancy
Conclusion
Our behavioral data demonstrated that as duration of electrical stimulation increased, threshold responses decreased, thereby, supporting the notion of temporal integration of electrical pulses delivered by a cochlear implant. Electrophysiological data were collected to pulse trains ranging in duration from 2 to 10 ms and unique effects were found on responses from the auditory brainstem versus thalamo-cortical areas.
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This research is supported by the Hospital for Sick Children Research Institute; there are no conflicts of interest.