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Discharge properties of identified cochlear nucleus neurons and auditory nerve fibers in response to repetitive electrical stimulation of the auditory nerve

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Abstract

Using the in vitro isolated whole brain preparation of the guinea pig maintained at 29°C, we intracellularly recorded and stained cochlear nucleus (CN) neurons and auditory nerve (AN) fibers. Discharge properties of CN cells and AN axons were tested in response to 50-ms trains of electrical pulses delivered to the AN at rates ranging from 100 to 1000 pulses per second (pps). At low stimulation rates (200–300 pps), the discharges of AN fibers and a large proportion of principal cells (bushy, octopus, stellate) in the ventral cochlear nucleus (VCN) followed with high probability each pulse in the train, resulting in synchronization of discharges within large populations of AN fibers and CN cells. In contrast, at high stimulation rates (500 pps and higher), AN fibers and many VCN cells exhibited "primary-like", "onset" and some other discharge patterns resembling those produced by natural sound stimuli. Unlike cells in the VCN, principal cells (pyramidal, giant) of the dorsal CN did not follow the stimulating pulses even at low rates. Instead, they often showed "pauser" and "build-up" patterns of activity, characteristic for these cells in conditions of normal hearing. We hypothesize that, at low stimulation rates, the response behavior of AN fibers and VCN cells is different from the patterns of neuronal activity related to normal auditory processing, whereas high stimulation rates produce more physiologically meaningful discharge patterns. The observed differences in discharge properties of AN fibers and CN cells at different stimulation rates can contribute to significant advantages of high- versus low-rate electrical stimulation of the AN used for coding sounds in modern cochlear implants.

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Acknowledgements

This work was supported by Swiss National Science Foundation grants 31-55836.98 and 31-66731.01, NIH/NIDCD grant DC00232, and the Swiss national center for competence in research (NCCR) "Neural plasticity and repair."

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Authors and Affiliations

  1. Division of Physiology, Department of Medicine, University of Fribourg, Rue du Musée 5, CH-1700, Fribourg, Switzerland

    Alexander L. Babalian & Eric M. Rouiller

  2. Departments of Otolaryngology-HNS and Neuroscience, Johns Hopkins University, Baltimore, MD, USA

    David K. Ryugo

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  1. Alexander L. Babalian
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  2. David K. Ryugo
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Correspondence to Alexander L. Babalian.

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Babalian, A.L., Ryugo, D.K. & Rouiller, E.M. Discharge properties of identified cochlear nucleus neurons and auditory nerve fibers in response to repetitive electrical stimulation of the auditory nerve. Exp Brain Res 153, 452–460 (2003). https://doi.org/10.1007/s00221-003-1619-x

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