Cochlear-implant spatial selectivity with monopolar, bipolar and tripolar stimulation

Abstract

Sharp spatial selectivity is critical to auditory performance, particularly in pitch-related tasks. Most contemporary cochlear implants have employed monopolar stimulation that produces broad electric fields, which presumably contribute to poor pitch and pitch-related performance by implant users. Bipolar or tripolar stimulation can generate focused electric fields but requires higher current to reach threshold and, more interestingly, has not produced any apparent improvement in cochlear-implant performance. The present study addressed this dilemma by measuring psychophysical and physiological spatial selectivity with both broad and focused stimulations in the same cohort of subjects. Different current levels were adjusted by systematically measuring loudness growth for each stimulus, each stimulation mode, and in each subject. Both psychophysical and physiological measures showed that, although focused stimulation produced significantly sharper spatial tuning than monopolar stimulation, it could shift the tuning position or even split the tuning tips. The altered tuning with focused stimulation is interpreted as a result of poor electrode-to-neuron interface in the cochlea, and is suggested to be mainly responsible for the lack of consistent improvement in implant performance. A linear model could satisfactorily quantify the psychophysical and physiological data and derive the tuning width. Significant correlation was found between the individual physiological and psychophysical tuning widths, and the correlation was improved by log-linearly transforming the physiological data to predict the psychophysical data. Because the physiological measure took only one-tenth of the time of the psychophysical measure, the present model is of high clinical significance in terms of predicting and improving cochlear-implant performance.

Introduction

Spatial selectivity, or frequency tuning in acoustic hearing, has played a pivotal role in auditory research and practice for over 100 years (Helmholtz, 1877). The concept of spatial selectivity has been used to explain a wide range of auditory phenomena from loudness, pitch and masking to music and speech perception (e.g., Fletcher, 1935, Plomp, 1964). Spatial selectivity can be characterized either directly by physiological means (e.g., Bekesy, 1952, Tasaki, 1954) or indirectly by psychophysical means (e.g., Chistovich, 1957, Small, 1959, Zwicker, 1974). There is generally good correspondence between physiologically and psychophysically measured spatial selectivity, as sharp tuning is observed with normal hearing whereas broad tuning is observed with sensorineural hearing loss (e.g., Liberman and Dodds, 1984, Moore and Glasberg, 1986).

Spatial selectivity has also played an important role in the development of modern multichannel cochlear implants (CI), which can restore significant functional hearing to deaf people by conveying acoustic spectral information to different places in the cochlea. However, compared with 3000 tonotopically-organized inner hair cells and their sharp tuning (e.g., Ruggero, 1992), the amount of spectral information in a cochlear implant is severely limited by not only the small number of intracochlear electrodes but also the wide spread of electrical stimulation and nerve survival (e.g., Finley et al., 2008, Khan et al., 2005, Shannon, 1983, Wilson et al., 1991, Zeng, 2004). As a result, the actual number of independent channels is significantly smaller than the number of physical electrodes in a cochlear implant (e.g., Fishman et al., 1997, Friesen et al., 2001); the CI users’ ability to resolve spectral contrast is also highly variable and can be directly correlated to their speech performance in quiet and in noise (Henry and Turner, 2003, Litvak et al., 2007b, Won et al., 2007).

The need to increase the number of functional channels in cochlear implants has spurred extensive research from new electrode designs to advanced signal processing (e.g., Koch et al., 2004, Tykocinski et al., 2001). Recent attention has been paid to manipulating electrode configuration and stimulation delivery to steer or focus the electrical field (for a review, see Bonham and Litvak, 2008). In particular, different electrode configurations have shown successively more focused electrical fields from monopolar, bipolar, to tripolar stimulation (e.g., Jolly et al., 1996, Kral et al., 1998, Zhu et al., 2010). The increased spatial selectivity with bipolar and tripolar stimulation modes is also supported by physiological studies in the auditory nerve (Kral et al., 1998, Miller et al., 2003, van den Honert and Stypulkowski, 1987), the inferior Colliculus (Bierer et al., 2010, Bonham and Litvak, 2008, Snyder et al., 2008), and the auditory cortex (Bierer and Middlebrooks, 2002, Middlebrooks and Bierer, 2002, Raggio and Schreiner, 1994). Therefore, it seems reasonable to hypothesize that focused stimulation such as bipolar and tripolar configurations will increase functional spatial selectivity and hopefully improve the overall cochlear-implant performance.

Unfortunately, this hypothesis has not been established functionally as recent studies showed little or no improvement in cochlear-implant performance using focused electric stimulation (Berenstein et al., 2008, Donaldson et al., 2011; e.g., Mens and Berenstein, 2005, Pfingst et al., 2001). There are several explanations for this lack of correspondence between physical and functional measures of focused stimulation. First, focused stimulation requires a higher current level than monopolar stimulation to reach behavioral threshold and comfortable loudness, so the benefit of focused stimulation may be reduced with the increased level of input (e.g., Berenstein et al., 2010, Chua et al., 2011, Kwon and van den Honert, 2006, Pfingst and Xu, 2004). Second, there are significant differences in physiological and psychophysical methods in addition to differences in animal and human studies of spatial selectivity. For example, psychophysical methods usually employed longer stimulation duration than physiological methods, which typically used single pulses (e.g., Abbas et al., 2004, Hughes and Stille, 2008, Lim et al., 1989). Animal studies typically used acute preparations with relatively good nerve survival while human studies usually involved patients with longer duration of deafness, which is a likely indication of poor nerve survival, both of which could significantly influence spatial selectivity (e.g., Goldwyn et al., 2010, Linthicum et al., 1991, Nadol et al., 2001, Vollmer et al., 2007). Third, there is a great deal of individual variability from etiology to performance that often renders direct comparison of psychophysical and physiological spatial selectivity difficult, if not impossible. For example, the first study of psychophysical spatial tuning curve used Nucleus users in bipolar mode and Clarion users in monopolar mode, with different electrode arrays, electrode-to-electrode spacing, and reference electrodes (Nelson et al., 2008). Most notably, reliable psychophysical measures are usually not obtainable in the growing population of pediatric cochlear-implant users, requiring physiological measures that can accurately and reliably predict corresponding pediatric psychophysical and functional performance. An ideal study would obtain comparable physiological, psychophysical and speech measures using the same electric stimulation parameters in the same cohort of subjects so that the hypothetic link between cochlear-implant performance and physiological or psychophysical spatial selectivity can be directly addressed.

As a first goal, the present study directly compared psychophysical and physiological spatial selectivity under a controlled paradigm. To reduce variability between subjects, all measures were conducted in the same subjects using the same device. To control procedural differences, both psychophysical and physiological measures used a similar forward-masking paradigm, except for the use of pulse trains for psychophysical measurement and the use of single pulses for the physiological measurement. To control stimulus differences, all pulses had the same, but relatively long, pulse duration to achieve sufficient loudness in focused stimulation. In addition, loudness growth was measured for both pulse trains and single pulses to assure presentation of probe and masker at a proper level within their respective dynamic ranges. The second goal was to test whether, under these stringent conditions, there were significant differences in spatial selectivity between broad and focused electric stimulation modes. The final goal was to test whether the psychophysical spatial tuning could be predicted from the physiological spatial masking curve.