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Monopolar Intracochlear Pulse Trains Selectively Activate the Inferior Colliculus

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Abstract

Previous cochlear implant studies using isolated electrical stimulus pulses in animal models have reported that intracochlear monopolar stimulus configurations elicit broad extents of neuronal activation within the central auditory system—much broader than the activation patterns produced by bipolar electrode pairs or acoustic tones. However, psychophysical and speech reception studies that use sustained pulse trains do not show clear performance differences for monopolar versus bipolar configurations. To test whether monopolar intracochlear stimulation can produce selective activation of the inferior colliculus, we measured activation widths along the tonotopic axis of the inferior colliculus for acoustic tones and 1,000-pulse/s electrical pulse trains in guinea pigs and cats. Electrical pulse trains were presented using an array of 6–12 stimulating electrodes distributed longitudinally on a space-filling silicone carrier positioned in the scala tympani of the cochlea. We found that for monopolar, bipolar, and acoustic stimuli, activation widths were significantly narrower for sustained responses than for the transient response to the stimulus onset. Furthermore, monopolar and bipolar stimuli elicited similar activation widths when compared at stimulus levels that produced similar peak spike rates. Surprisingly, we found that in guinea pigs, monopolar and bipolar stimuli produced narrower sustained activation than 60 dB sound pressure level acoustic tones when compared at stimulus levels that produced similar peak spike rates. Therefore, we conclude that intracochlear electrical stimulation using monopolar pulse trains can produce activation patterns that are at least as selective as bipolar or acoustic stimulation.

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Acknowledgments

The authors thank Alex Hetherington and Steve Rebscher for construction of intracochlear electrodes and for assisting with data collection. This work was funded by NIH Predoctoral Fellowship 1 F31 DC008940-01A1, NIH/NIDCD HHS-N-263-2007-00054-C, the Epstein Fund, and Hearing Research, Inc.

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Authors and Affiliations

  1. Department of Bioengineering, University of California San Francisco, San Francisco, CA, 94143-0526, USA

    Matthew C. Schoenecker

  2. Department of Otolaryngology–HNS, University of California San Francisco, San Francisco, CA, 94143-0526, USA

    Ben H. Bonham, Russell L. Snyder & Patricia A. Leake

  3. Department of Hearing & Speech Sciences, University of Maryland at College Park, College Park, MD, 94143-0526, USA

    Olga A. Stakhovskaya

  4. Department of Psychology, Utah State University, Logan, UT, 84322, USA

    Russell L. Snyder

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  1. Matthew C. Schoenecker
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  4. Russell L. Snyder
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  5. Patricia A. Leake
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Correspondence to Matthew C. Schoenecker.

Appendix: chronically deafened cats

Appendix: chronically deafened cats

Six of the eight cats in this study were deafened as neonates by daily subcutaneous injections of neomycin sulfate (60 mg/kg; Leake et al. 1999) and received varying electrical stimulation regimes and drug treatments (Table 2). For all six animals, neomycin injections were started at day 1 after birth; click-evoked auditory brainstem responses were used to monitor hearing loss beginning after 16 days of treatment, at 2–3 days intervals. Neomycin treatment was discontinued after 16–21 injections when absence of responses to clicks at 90 dB SPL indicated a profound hearing loss. All six cats were implanted unilaterally at 4–7 weeks of age with an intracochlear electrode with six to eight stimulating contacts. Four cats also received a subcutaneous mini osmotic pump (Rebscher et al. 2007) for direct infusion of brain-derived neurotrophic factor (BDNF, 94 μg/ml, three animals) or artificial perilymph (one animal) into the inner ear. One animal received systemic treatment with rasagiline (1 mg/kg daily). Five cats also chronic electrical stimulation for 4 h per day, 5 days a week, for a period of 13–23 weeks. Four of these five animals received electrical stimulation with biphasic pulse trains (90 μs/phase) delivered by a Clarion™ CII speech processor. Levels of stimulation were controlled by the loudness of environmental sounds with maximum stimulation levels set at 6 dB above electrically evoked ABR thresholds, but no more than 500 μA. The remaining animal was stimulated with continuous trains of charge-balanced biphasic pulses (200 μs/phase) delivered at 300 pulses/s with 30-Hz sinusoidal amplitude modulation (100 % modulation depth). In this animal peak stimulation levels were set at 2 dB above electrically evoked ABR thresholds. Chronically deafened cats were studied in acute physiological experiments immediately following completion of the electrical stimulation and drug treatment protocols. Because the effect of treatment group was not significant for any of the tests performed (p > 0.09), data from all the cats were pooled.

TABLE 2 Electrical stimulation and drug treatment histories for eight cats
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Schoenecker, M.C., Bonham, B.H., Stakhovskaya, O.A. et al. Monopolar Intracochlear Pulse Trains Selectively Activate the Inferior Colliculus. JARO 13, 655–672 (2012). https://doi.org/10.1007/s10162-012-0333-4

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