Effects of acoustic noise on the auditory nerve compound action potentials evoked by electric pulse trains
Introduction
Electric stimulation of the auditory nerve by a cochlear implant is the method of choice for the treatment of severe and profound hearing loss. Clinical criteria for cochlear implantation have become more relaxed over the last decade, and many patients with residual hearing have been receiving cochlear implants (NIH Consensus Statement, 1995). Studies by Turner and Gantz, 2001, Turner et al., 2003 and Gstoettner et al. (2004) have demonstrated that hair cells can remain functional in patients following cochlear implantation. Therefore, there is a possibility that residual acoustic sensitivity can influence responses of the auditory nerve fibers to electric stimuli delivered by the cochlear implant. A systematic understanding of possible interactions between acoustic and electric stimuli at the level of the auditory nerve may facilitate improvements of stimulation paradigms in individuals with residual hearing.
Previous work in our laboratory addressed the effects of functional hair cells on the response properties of the electrically stimulated auditory nerve. It was found that presence of functional hair cells – even without acoustic stimulation – could affect the response of the auditory nerve to electric stimuli (Hu et al., 2003). Specifically, electrically evoked compound action potential (ECAP) growth functions in response to single electric pulses had smaller saturation (maximum) amplitudes and more shallow slopes in acoustically sensitive ears compared with deafened ears. In addition, it was demonstrated that viable hair cells could affect the adaptation and refractory properties of the auditory nerve, as evidenced by compound action potential recordings in response to electric pulse trains. The observed effects were attributed to increased stochastic activity of the auditory nerve fibers associated with spontaneous release of neurotransmitter by functionally active hair cells.
Preliminary studies in our laboratory have investigated effects of acoustic stimuli on the auditory nerve response to simultaneous electric stimulation. This interaction has been addressed using measures based both on ECAP (Miller et al., 2000) and single fiber (Miller et al., 2003a) responses. When presented simultaneously, wideband acoustic noise can decrease the amplitude of ECAP response to single electric pulses. Analysis of single-fiber data showed that this effect was associated with an increase of fiber discharge rate, an increase in spike jitter, a decrease in vector strength, and reductions in amplitude of individual spikes (Miller et al., 2003a). Based on these results, it was hypothesized that ECAP decrements can indicate an acoustically driven desynchronization of responses of the auditory nerve fibers to pulsatile electric stimuli.
While the aforementioned studies demonstrated acoustic–electric interactions, they provided little information about the time course of the observed effects of acoustic stimuli. As most cochlear implants present information to the auditory nerve as trains of amplitude modulated electric pulses, it is important to consider the temporal properties of acoustic–electric interaction.
Studies of electric pulse train responses in deafened animals have demonstrated that the auditory nerve response can undergo significant changes over the course of the pulse-train stimulus. Short-term adaptation to electric pulse trains that occurred over tens of milliseconds (Javel, 1990, Haenggeli et al., 1998, Matsuoka et al., 2000) as well as long-term cumulative effects that spanned over seconds (Haenggeli et al., 1998, Abkes et al., 2003) have been described. Furthermore, the magnitude and time course of adaptation to electric pulse trains can be affected by the presence of viable hair cells (Haenggeli et al., 1998, Hu et al., 2003). Response of the auditory nerve fibers to an acoustic stimulus may also undergo changes over time (Westerman and Smith, 1984).
The major goal of the present study was to provide a detailed description of the time course of changes in the auditory nerve compound action potential in response to electric pulse trains in the presence of broadband acoustic noise. Changes in ECAP amplitude observed during stimulation with acoustic noise (simultaneous effects) and following cessation of the noise stimulus (post-stimulatory effects) are described across different stimulus parameters. Level, duration and rate of stimulation may all affect response adaptation of the auditory nerve fibers to these stimuli (Haenggeli et al., 1998, Matsuoka et al., 2000). As adaptation may affect the time course of acoustic–electric interaction, we examined it by varying the levels of acoustic and electric stimuli, as well as the duration of acoustic and the rate of electric stimulation.
Portions of this study have appeared previously in abstract form (Miller et al., 2003b, Nourski et al., 2003a, Nourski et al., 2003b).
Section snippets
Animal preparation
Twelve adult guinea pigs (weight range 450–620 g) free from middle ear infection were used in acute experimental sessions. Initial anesthesia was accomplished with a combination of ketamine (40 mg/kg), xylazine (7.5 mg/kg) and acepromazine (0.5 mg/kg), administered intramuscularly. A single dose of atropine sulphate (0.05 mg/kg) was given subcutaneously to reduce musocal secretion. After anesthesia was induced, the right external jugular vein was surgically exposed and a catheter was inserted
General characteristics
Fig. 2 demonstrates an example of ECAP amplitudes in response to electric pulse trains presented at a 4 ms IPI with or without simultaneous acoustic noise. In the upper panel (Fig. 2(a)), response amplitudes to individual pulses of the train are plotted as a function of time after the onset of the acoustic stimulus. Responses to the electric pulse train presented alone (filled circles) provide a control condition for evaluating effects of the acoustic noise. It can be seen that the response
Effects of acoustic noise across stimulus parameters
The results presented in this paper provide evidence that electric and acoustic stimuli, when presented simultaneously, can functionally interact at the level of the auditory nerve. Acoustic noise can produce simultaneous as well as post-stimulatory effects on the auditory nerve responses to electric pulses. The principal result of this interaction is a decrease in the ECAP response amplitude in the presence of the acoustic stimulus (wideband noise). This is consistent with our previous
Acknowledgement
This work was supported by NIH contract N01-DC-2-1005.
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