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Overcoming issues related to abnormally high neural synchrony in response to electrical stimulation is one aspect in improving hearing with a cochlear implant. Desynchronization of electrical stimuli have shown benefits in neural encoding of electrical signals and improvements in psychophysical tasks. In the present study, 10 participants with either CII or HiRes 90k Advanced Bionics devices were tested for the effects of desynchronizing constant-amplitude high-rate (5,000 Hz) pulse trains on electrode discrimination of sinusoidal stimuli (1,000 Hz). When averaged across the sinusoidal dynamic range, overall improvements in electrode discrimination with high-rate pulses were found for 8 of 10 participants. This effect was significant for the group (p = .003). Nonmonotonic patterns of electrode discrimination as a function of sinusoidal stimulation level were observed. By providing additional spectral channels, it is possible that clinical implementation of constant-amplitude high-rate pulse trains in a signal processing strategy may improve performance with the device.
Cochlear implants are a commonly implemented auditory intervention for individuals with significant hearing loss for whom hearing aids are inadequate. Cochlear implant design has evolved from using a single stimulating electrode to implementing arrays that include multiple electrodes. One key purpose of a multielectrode cochlear implant is to provide spectral (i.e., place-frequency) information in electrical hearing that is absent due to the loss of cochlear processing. Therefore, the ability to discriminate between electrodes is critical for optimizing spectral resolution and allowing a cochlear implant user to take full advantage of the multielectrode device. In turn, it may be expected that electrode discrimination is related to performance with a cochlear implant.
Individuals with good electrode discrimination tend to have higher speech perception scores (Collins, Zwolan, & Wakefield, 1997; Henry, McKay, McDermott, & Clark, 2000; Throckmorton & Collins, 1999), and greater numbers of independent channels are important for complex listening situations such as speech in noise and music perception (Carroll & Zeng, 2007; Dorman, Loizou, Fitzke, & Tu, 1998; Dorman, Loizou, Spahr, & Maloff, 2002; Friesen, Shannon, Baskent, & Wang, 2001; Fu, Chinchilla, & Galvin, 2004; Fu & Nogaki, 2005; Shannon, Fu, & Galvin, 2004; Smith, Delgutte, & Oxenham, 2002; Xu & Zheng, 2007). In children, the number of channels may be particularly important. Investigations have found that children require more stimulation channels to reach the same speech perception performance level as adults (Dorman, Loizou, Kemp, & Kirk, 2000; Eisenberg, Shannon, Martinez, Wygonski, & Boothroyd, 2000). Furthermore, Dawson, McKay, Busby, Grayden, & Clark (2000) determined that electrode discrimination ability was the primary predictor of speech perception performance in implanted children.
Currently, a given cochlear implant user is limited by his/her electrode discrimination abilities, which is, in part, due to the neural encoding of electrical stimuli. Electrical stimulation of auditory nerve fibers results in highly synchronized neural responses that are distorted compared with those seen with a normally functioning auditory system and acoustic stimulation. In comparing single-fiber responses with acoustic and electric stimuli, Kiang and Moxon (1972) illustrated the functional consequences of highly synchronous neural activity with electrical stimulation, including loss of frequency selectivity, abnormally narrow dynamic range, and poor temporal representation of sinusoidal stimuli (Kiang & Moxon, 1972). Similar results demonstrating highly synchronized neural responses with electrical stimulation have been found in several investigations (Hartmann, Topp, & Klinke, 1984; Miller, Abbas, Robinson, Rubinstein, & Matsuoka, 1999; Shepherd & Javel, 1997; van den Honert & Stypulkowski, 1987).
To address these issues, novel electrical stimulation paradigms designed to desynchronize neural responses to electrical signals by introducing random, or stochastic, response behaviors at the level of the nerve fiber are under investigation. Such desynchronizing stimuli include adding electrical Gaussian noise to a signal (Matsuoka, Abbas, Rubinstein, & Miller, 2000; Morse & Evans, 1996, 1999 a and b) or eliciting random neural responses with high-rate pulse trains (Litvak, Delgutte, & Eddington, 2001, 2003a, 2003b; Litvak, Smith, Delgutte, & Eddington, 2003; Matsuoka, Rubinstein, Abbas, & Miller, 2001; Miller, Hu, Zhang, Robinson, & Abbas, 2008; Rubinstein & Hong, 2003; Rubinstein, Wilson, Finley, & Abbas, 1999).
Using electrical high-rate pulse trains as desynchronizing stimuli was first proposed by Rubinstein and colleagues (1999), with the rationale that pulse trains presented at a rate sufficient to maintain relative refractoriness will take advantage of nerve fibers' intrinsic noise characteristics, thereby improving neural encoding of electrical signals. Supporting this hypothesis, subsequent investigations of auditory nerve fiber responses to high-rate pulse trains have reported discharge patterns indicative of desynchronizing effects (Litvak et al., 2001; Litvak et al., 2003a, 2003b; Miller et al., 2008). Litvak, Smith, et al. (2003) measured sustained random neural responses to high-rate pulse trains in the auditory nerve fibers of cats, which resembled spontaneous activity in the normal auditory system. In addition, responses to high-rate pulse trains recorded simultaneously from pairs of nerve fibers were uncorrelated, indicating independent responses across fibers. Improved neural representation of electrical signals with high-rate pulses has been observed with vowel and sinusoidal stimuli (Litvak et al., 2003a, 2003b), and high-rate pulses have also been associated with increases in neural (Runge-Samuelson, Abbas, Rubinstein, Miller, & Robinson, 2004) and psychophysical (Hong & Rubinstein, 2003) dynamic range. Given the evidence toward improved neural encoding of electrical signals and increased neural independence with high-rate electrical stimuli, this may be one approach for improving electrode discrimination within cochlear implant users. In the present study, constant-amplitude high-rate electrical pulse trains were investigated for their effects on electrode discrimination. It was hypothesized that increases in independent neural activity from high-rate pulse trains would result in improved encoding of channel independence as measured by electrode discrimination.
Ten adult cochlear implant users participated in this study. All participants used either the Clarion Bionic Ear CII or the HiRes 90k (Advanced Bionics Corp., Sylmar, CA) device with HiFocus electrodes; one participant (S8) also had a positioner. All participants had been programmed with the HiResolution speech processing strategy for daily use. Table 1 shows demographic information for the participants. This study was approved by the Froedtert Hospital/Medical College of Wisconsin Institutional Review Board.
The stimuli were all presented using a monopolar configuration. They consisted of 1,000 Hz electric sinusoid bursts (400 ms duration) and, when present, constant-amplitude high-rate pulse trains. The pulse trains were biphasic pulses of 11 μs/phase presented at 5,000 Hz. The stimuli were presented using hardware and software provided by Advanced Bionics Corp. (Sylmar, CA) and were implemented as follows. On one computer, Bionic Ear Programming System (BEPS) software ran a custom program designed using the Bionic Ear Data Collection System (BEDCS) software on the same computer. This computer was connected to a platinum speech processor via the Clarion Programming Interface, and the coil headpiece connected the participant to the speech processor. The custom program run through BEPS designates which electrodes are analog, for presentation of the sinusoid bursts, and which electrodes are pulsatile, for presentation of the high-rate pulses. The sinusoid bursts were generated by and presented from a second computer using MATLAB (Mathworks, Inc.), and were called within the BEDCS software on that computer. The sinusoid burst stimuli were output to an external sound card (Creative Sound Blaster Extigy, 24-bit 100 dB SNR), which was connected to the external input on the speech processor. Within the speech processor, the sound card output was processed according to the electrode parameters determined by BEPS, which stimulated the implant accordingly. The stimulation levels of the sinusoid bursts and high-rate pulses were controlled through both BEPS and BEDCS from both computers.
Dynamic range measures. Threshold and most comfortable level (MCL) were measured for the sinusoid bursts presented on Electrode 12 (1,000 Hz sinusoid bursts of 400 ms duration separated by 1 s); dynamic range was defined as the range of levels between threshold and MCL. Sinusoidal threshold was defined as the level that elicited three detectable responses using ascending stimuli. Sinusoidal MCL was measured by increasing sinusoidal level gradually until the participant judged it as most comfortable. The procedure was repeated at least three times, and the average of the trials was defined as MCL. Threshold and MCL of sinusoidal stimuli were first obtained without the presence of high-rate pulses; then they were remeasured with high-rate pulses, as described below.
Constant amplitude high-rate pulse trains were presented on electrodes 11 and 13 for eight participants and on all odd electrodes for two participants (S1 and S9). The pulses were presented for a minimum of 30 s prior to presentation of the sinusoidal stimuli and remained on until the end of each experimental condition. Often, the participants were unable to perceive the pulses; however, in cases when the pulses were audible, presentation of the sinusoidal stimuli was postponed until the perception of the pulses adapted. Sinusoidal threshold was measured at each high-rate pulse level from 100 to 900 μA (in 100 μA steps), and the high-rate pulse level that resulted in the largest decrease in sinusoidal threshold was determined. Sinusoidal MCL was measured using this high-rate pulse level, which was used to determine the sinusoidal dynamic range in the presence of high-rate pulses. The level of high-rate pulses resulting in the largest decrease in threshold was interpreted as the most effective level and was subsequently used for the electrode discrimination experiment.
Electrode discrimination measures. Electrode discrimination was measured by presenting sinusoid bursts on a “standard” electrode and a “comparison” electrode, which for all participants were Electrodes 12 and 10, respectively. For each participant, discrimination was tested for three to five sinusoidal levels that ranged in loudness from very quiet to most comfortable. Discrimination for each sinusoidal level was tested both with and without high-rate pulses. Prior to the electrode discrimination testing, loudness balancing between the standard and comparison electrodes was performed at each sinusoidal level using a bracketing procedure. Loudness balancing was performed at all sinusoidal levels under each listening condition, that is, with and without the presence of high-rate pulses.
This study used a same–different task. Participants were presented with a pair of sinusoid burst sets (a set was three 400 ms sinusoid bursts separated by 1 s) on either the same or different electrode and had to report whether the sounds were the same or different. A trial consisted of 52 sinusoid burst pairs presented at a single sinusoidal level. An entire trial was conducted either in the presence or absence of high-rate pulse trains. When present, the high-rate pulse trains were on for the duration of the trial. As for the dynamic range measures, participants were allowed to adapt to the high-rate pulse stimuli when necessary before electrode discrimination testing. For each trial, there was equal probability for same and different presentations and for the order of electrode stimulation within a pair.
All stimulation conditions were randomized. Specifically, across trials, the suprathreshold sinusoidal level and the presence or absence of high-rate pulses were randomized, and within each trial, the order of standard and comparison electrode stimulation and whether pairs were the same or different were randomized.
Electrode discrimination performance was measured for each trial by calculating d-prime based on the hit and false-alarm rates. A hit was defined as the participant responding “different” when the stimuli were different, and a false-alarm was defined as a “different” response when the stimuli were the same. The respective hit and false-alarm rates were calculated by dividing the number of occurrences of each by the total number of sinusoid-burst-pair presentations. d-Prime was calculated by subtracting the z score of the false-alarm rate from the z score of the hit rate.
When the high-rate pulses were presented, the participants reported having either no perception or hearing a soft “static” sound. When the high-rate pulses were perceived, the participants were allowed to adapt to the perception before obtaining any measurements; in each case, adaptation occurred in less than 1 to 2 min.
Table 2 shows the effects of high-rate pulse trains on sinusoidal threshold, MCL, and dynamic range for the high-rate pulse level that resulted in the maximum threshold decrease (HRmax) for all participants; the values reflect differences between the sinusoid alone and sinusoid with high-rate pulses conditions in decibels. Decreases in threshold ranged from 0.37 to 2.02 dB, with an average of −0.95 dB (1 standard deviation [SD] = 0.49). For MCL, four participants showed no change, three had an increase, and two a decrease (range −0.89 to +1.58 dB; average increase of 0.28 dB [1 SD = 0.64]). This relative stability of MCL is consistent with that reported by Hong and colleagues (2003). Dynamic range increased for all but one participant (S8), whose decrease in MCL surpassed the threshold decrease. The range of dynamic range changes was −0.52 to +3.6 dB, with an average overall increase of 1.14 dB (1 SD = 1.03).
Electrode discrimination performance with and without high-rate pulses for all participants are shown in Figure 1. d-Prime values were plotted as a function of sinusoidal stimulation level in percentage dynamic range of the sinusoid without high-rate pulses. Closed symbols represent discrimination without high-rate pulses, and open symbols represent discrimination with high-rate pulses. Larger d-prime values indicate better electrode discrimination performance, and a d-prime value of zero is chance. Across participants, there was variability in overall discrimination performance, effects of sinusoidal stimulus level on discrimination, and the effects of high-rate pulses. For 8 of 10 participants, electrode discrimination across sinusoidal levels with high-rate pulses tended to be either better or the same as performance in the absence of high-rate pulses. S7 and S10 showed no effect of high-rate pulses; however, the functions were repeatable for both conditions despite the trials being randomized, indicating test-retest reliability.
The effects of high-rate pulse trains on electrode discrimination across sinusoidal levels shown in Figure 1 often appeared nonmonotonic. To examine this further, d-prime without high-rate pulses was subtracted from d-prime with high-rate pulses for each sinusoidal level, with positive values indicating improved electrode discrimination performance with the addition of high-rate pulses. The d-prime difference functions for all participants are shown in Figure 2. For all participants, nonmonotonic functions were observed, and the shapes of the functions fell into two groups, resembling nonmonotonic electrode discrimination functions observed by Pfingst, Holloway, Zwolan, and Collins (1999). These were termed here as Type I and Type II, and they represent inverted U- and U-shaped functions, respectively. Further analysis of the participants in each group showed no systematic differences in speech perception performance or demographic variables such as length of deafness or cochlear implant use.
To characterize the overall effects of high-rate pulses on electrode discrimination for each participant, the d-prime values were averaged across sinusoidal stimulation levels for both conditions (Figure 3). In Figure 3, the average d-prime values for each participant are shown with high-rate pulses (grey bars) and without high-rate pulses (black bars); the group mean is shown with +1 SD. As observed in Figure 1, eight participants demonstrated an overall improvement in electrode discrimination with high-rate pulses, with S7 and S10 showing a slight overall decrement. The differences in performance with high-rate pulses ranged from a decrement of 0.08 (S7) to an improvement of 0.63 (S4). The d-prime values for group mean data were 1.84 (1 SD = 0.70) without high-rate pulses and 2.10 (1 SD = 0.62) with high-rate pulses, and the improvement observed with high-rate pulses was statistically significant (p = .003).
The results of this study showed that constant-amplitude high-rate pulse trains affect dynamic range and electrode discrimination of sinusoidal stimuli in cochlear implant users. The primary changes in dynamic range were due to decreases in threshold, although changes in MCL were observed. These results are similar to previous studies examining the effects of desynchronizing stimuli on electrical sinusoidal dynamic range measures, including high-rate pulses (Hong & Rubinstein, 2003; Hong, Rubinstein, Wehner, & Horn, 2003; Morse, Morse, Nunn, Archer, & Boyle, 2007; Zeng, Fu, & Morse, 2000) and added Gaussian noise (Morse et al., 2007; Zeng et al., 2000). The average maximum change in dynamic range for the current study was an increase of 1.14 ± 1.03 dB. This is smaller than that observed by Hong and colleagues (2003), who reported a mean maximum increase in sinusoidal dynamic range of 6.7 dB with high-rate pulses. It is unclear why the effect was smaller in the present study; however, one potential factor may have been the use of monopolar stimulation compared with bipolar stimulation by Hong and colleagues. Using a monopolar configuration, Morse and colleagues (2007) measured a mean change in 1,000 Hz sinusoidal dynamic range of less than 0.7 dB in the presence of electrical Gaussian noise. Although the desynchronizing stimulus used was different from that in the present study, the effects may be similar; however, this is speculative.
The results of this study showed that high-rate pulse trains can improve electrode discrimination at individual levels across the sinusoidal dynamic range. In the instances where high-rate pulse stimuli did not improve electrode discrimination, the presence of the pulses tended to have no effect and seldom induced a performance decrement. Therefore, addition of high-rate pulses may improve electrode discrimination at certain suprathreshold sinusoidal levels but may not have a detrimental effect at others. Electrode discrimination performance across sinusoidal levels varied across participants and was nonmonotonic in several cases, irrespective of the presence of high-rate pulse trains. These patterns have been noted in previous studies (McKay, O'Brien, & James, 1999; Pfingst et al., 1999). When testing electrode discrimination at 25%, 50%, and 75% of the dynamic range, Pfingst and colleagues (1999) characterized three types of functions: best electrode discrimination at low stimulus levels, best electrode discrimination at high stimulus levels, and functions that were U- or inverted U-shaped. All three patterns were represented in the data for the present study. In addition, the effects of high-rate pulses were nonmonotonic across sinusoidal level for all participants and fell into two groups of inverted U- and U-shaped, referred to here as Type I and Type II (Figure 2).
The mechanism behind these electrode discrimination functions and the nonmonotonic effects of high-rate pulses is unclear. One possibility may be interactions between the sinusoidal and high-rate pulse levels that result in optimal neural encoding of the sinusoidal stimuli. This may be an effect similar to the phenomenon of stochastic resonance, which refers to an amount of noise that results in the greatest amount of signal enhancement. Stochastic resonance has been observed in many studies using various electrical desynchronizing stimuli (Behnam & Zeng, 2003; Chatterjee & Oba, 2005; Chatterjee & Robert, 2001; Hong & Rubinstein, 2003; Hong et al., 2003; Morse & Evans, 1996; Rubinstein & Hong, 2003; Runge-Samuelson et al., 2004; Zeng et al., 2000). Stochastic resonance is typically characterized by changing the level of the desynchronizing stimulus and measuring the response to a given signal level; however, the present study used one high-rate pulse level and several sinusoidal levels for the electrode discrimination experiment. In measuring neural representation of vowel stimuli with and without Gaussian noise, Morse and Evans (1996) demonstrated that for each vowel stimulus level, there was an optimal noise level for formant enhancement, although nonmonotonic relationships were not observed (Morse & Evans, 1996). In a simple model of stochastic resonance for neural population responses, Runge-Samuelson and colleagues (2004) included interactions between sinusoid and high-rate pulse levels. In a separate analysis, implementation of this model with assigned values yielded nonmonotonic U- and inverted U-shaped functions across signal level for some high-rate pulse levels (Runge-Samuelson, 2002, p. 157), which may indicate the potential for nonmonotonic interactions between stimulus levels, although this is highly theoretical.
Another possibility is that the high-rate pulses affected the loudness of the sinusoid, essentially changing that sinusoidal loudness percept to reflect one that had different discrimination performance. However, if this were the case, it would be expected that at certain sinusoidal levels, the high-rate pulses would result in decrements in performance that were comparable in magnitude to the improvements, which were not observed in the data. Although the reasons for nonmonotonic electrode discrimination performance across levels are not known, the clinical implications suggest an approach that optimizes programming parameters based on psychophysical performance for a given electrode (Pfingst, Burkholder-Juhasz, Zwolan, & Xu, 2008).
The improvements in electrode discrimination, or channel selectivity, with high-rate pulses observed in this study may translate into improved speech perception performance, particularly in complex listening situations. This may be especially beneficial for individuals who are only able to use a few channels of their device. Investigations of cochlear implant users and cochlear implant simulations with normal-hearing individuals have shown that a minimum of three to four spectral channels are required to perform well with speech perception in quiet (Dorman et al., 1998; Friesen et al., 2001; Shannon et al., 2004). Friesen and colleagues (2001) showed that for cochlear implant users, speech perception performance in quiet and in noise generally improved as the number of channels increased up to seven or eight, above which performance tended to plateau. The normal-hearing participants continued to improve up to 20 channels, the maximum included in the study. Additional analyses of the cochlear implant users showed that participants who were limited to three to four spectral channels were the poorest performers, whereas those whose performance improved with increases in channel number up to seven to eight were the best performers, with their performance comparable with that of normal-hearing participants using the same number of channels. In a meta-analysis of several spectral channel studies representing a wide range of speech perception and music tasks, Shannon and colleagues (2004) found that across listening tasks, doubling the amount of spectral channels led to an improvement of 60 percentage points. Therefore, cochlear implant users with limited spectral channels may benefit from a signal processing paradigm that provides even a few additional independent channels.
In cases where high-rate pulse trains improved electrode discrimination performance, it calls to question why this might be. There is evidence that electrode discrimination performance is dependent on the ability to detect changes in the edges of neural excitation as opposed to the relative amount of excitation overlap (Laneau & Wouters, 2004; McKay et al., 1999). As the high-rate pulses were presented on electrodes adjacent to the electrodes used for sinusoidal stimulation, it is likely that the pulses elicited excitation from these neural populations and, specifically, may have produced refractory effects that altered the fiber threshold distribution (Miller, Abbas, & Robinson, 2001) and elicited independent response behaviors at the edges of excitation. This may have resulted in enhancements of the neural representation of the sinusoidal signals at certain suprathreshold levels, potentially improving electrode discrimination performance.
Constant-amplitude high-rate pulse trains can improve electrode discrimination with sinusoidal stimulation in cochlear implant users. The clinical utility of this may be that implementation of constant-amplitude high-rate pulse trains in a signal processing strategy may increase the number of spectral channels for a given user, which has the potential to improve performance with the device.
The author is grateful for the contributions of the following individuals to this project: Leo Litvak, PhD, performed software programming of BEPS and BEDCS; Maire Frazer, AuD, assisted in data collection; David Friedland, MD, PhD, gave helpful suggestions on the manuscript, and Bryan Pfingst, PhD, provided valuable input as a consultant on this project. The review of this manuscript by Monita Chatterjee contributed significantly to the final version.