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Cochlear Damage Affects Neurotransmitter Chemistry in the Central Auditory System

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      Abstract

      Tinnitus, the perception of a monotonous sound not actually present in the environment, affects nearly 20% of the population of the United States. Although there has been great progress in tinnitus research over the past 25 years, the neurochemical basis of tinnitus is still poorly understood. We review current research about the effects of various types of cochlear damage on the neurotransmitter chemistry in the central auditory system and document evidence that different changes in this chemistry can underlie similar behaviorally measured tinnitus symptoms. Most available data have been obtained from rodents following cochlear damage produced by cochlear ablation, intense sound, or ototoxic drugs. Effects on neurotransmitter systems have been measured as changes in neurotransmitter level, synthesis, release, uptake, and receptors. In this review, magnitudes of changes are presented for neurotransmitter-related amino acids, acetylcholine, and serotonin. A variety of effects have been found in these studies that may be related to animal model, survival time, type and/or magnitude of cochlear damage, or methodology. The overall impression from the evidence presented is that any imbalance of neurotransmitter-related chemistry could disrupt auditory processing in such a way as to produce tinnitus.

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      Most cited references 106

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      General review of tinnitus: prevalence, mechanisms, effects, and management.

      Tinnitus is an increasing health concern across all strata of the general population. Although an abundant amount of literature has addressed the many facets of tinnitus, wide-ranging differences in professional beliefs and attitudes persist concerning its clinical management. These differences are detrimental to tinnitus patients because the management they receive is based primarily on individual opinion (which can be biased) rather than on medical consensus. It is thus vitally important for the tinnitus professional community to work together to achieve consensus. To that end, this article provides a broad-based review of what is presently known about tinnitus, including prevalence, associated factors, theories of pathophysiology, psychological effects, effects on disability and handicap, workers' compensation issues, clinical assessment, and various forms of treatment. This summary of fundamental information has relevance to both clinical and research arenas.
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        Homeostatic plasticity drives tinnitus perception in an animal model.

        Hearing loss often results in tinnitus and auditory cortical map changes, leading to the prevailing view that the phantom perception is associated with cortical reorganization. However, we show here that tinnitus is mediated by a cortical area lacking map reorganization. High-frequency hearing loss results in two distinct cortical regions: a sensory-deprived region characterized by a decrease in inhibitory synaptic transmission and a normal hearing region showing increases in inhibitory and excitatory transmission and map reorganization. Hearing-lesioned animals displayed tinnitus with a pitch in the hearing loss range. Furthermore, drugs that enhance inhibition, but not those that reduce excitation, reversibly eliminated the tinnitus behavior. These results suggest that sensory deprivation-induced homeostatic down-regulation of inhibitory synapses may contribute to tinnitus perception. Enhancing sensory input through map reorganization may plausibly alleviate phantom sensation.
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          Elevated fusiform cell activity in the dorsal cochlear nucleus of chinchillas with psychophysical evidence of tinnitus.

          Chinchillas with psychophysical evidence of chronic tinnitus were shown to have significantly elevated spontaneous activity and stimulus-evoked responses in putative fusiform cells of the dorsal cochlear nuclei (DCN). Chinchillas were psychophysically trained and tested before and after exposure to a traumatic unilateral 80 dB (sound pressure level) 4 kHz tone. Before exposure, two groups were matched in terms of auditory discrimination performance (noise, and 1, 4, 6, and 10 kHz tones). After exposure, a single psychophysical difference emerged between groups. The exposed group displayed enhanced discrimination of 1 kHz tones (p = 0.00027). Postexposure discrimination of other stimuli was unaffected. It was hypothesized that exposed animals experienced a chronic subjective tone (i.e., tinnitus), resulting from their trauma, and that features of this subjective tone were similar enough to 1 kHz to affect discrimination of 1 kHz objective signals. After psychophysical testing, single-unit recordings were obtained from each animal's DCN fusiform cell layer. Putative fusiform cells of exposed animals showed significantly (p = 0.0136) elevated spontaneous activity, compared with cells of unexposed animals. Putative fusiform cells of exposed animals showed a greater stimulus-evoked response to tones at 1 kHz (p = 0.0000006) and at characteristic-frequency (p = 0.0000009). This increased activity was more pronounced on the exposed side. No increase in stimulus-evoked responses was observed to other frequencies or noise. These parallel psychophysical and electrophysiological results are consistent with the hypothesis that chronic tonal tinnitus is associated with, and may result from, trauma-induced elevation of activity of DCN fusiform cells.
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            Author and article information

            Affiliations
            1Department of Neurology, University of Toledo College of Medicine , Toledo, OH, USA
            2Division of Otolaryngology and Dentistry, Department of Surgery, University of Toledo College of Medicine , Toledo, OH, USA
            Author notes

            Edited by: Jinsheng Zhang, Wayne State University, USA

            Reviewed by: Richard Altschuler, University of Michigan, USA; James A. Kaltenbach, Cleveland Clinic, USA; Rui Cai, Southern Illinois University School of Medicine, USA

            *Correspondence: Donald A. Godfrey, Department of Neurology, University of Toledo Health Science Campus, Mail Stop 1195, 3000 Arlington Avenue, Toledo, OH 43610, USA e-mail: donald.godfrey@ 123456utoledo.edu

            This article was submitted to Neuro-otology, a section of the journal Frontiers in Neurology.

            Contributors
            URI : http://frontiersin.org/people/u/176505
            URI : http://frontiersin.org/people/u/176509
            Journal
            Front Neurol
            Front Neurol
            Front. Neurol.
            Frontiers in Neurology
            Frontiers Media S.A.
            1664-2295
            08 September 2014
            19 November 2014
            2014
            : 5
            25477858 4237057 10.3389/fneur.2014.00227
            Copyright © 2014 Lee and Godfrey.

            This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

            Counts
            Figures: 2, Tables: 7, Equations: 0, References: 116, Pages: 16, Words: 11331
            Categories
            Neuroscience
            Review Article

            Neurology

            acetylcholine, tinnitus, taurine, glycine, glutamate, gaba, carboplatin, aspartate

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