Elsevier

Neuroscience

Volume 154, Issue 1, 12 June 2008, Pages 304-314
Neuroscience

The changing auditory system: Development, learning, aging and disease
Effects of cochlear ablation on amino acid concentrations in the chinchilla posteroventral cochlear nucleus, as compared to rat

https://doi.org/10.1016/j.neuroscience.2007.12.031Get rights and content

Abstract

Using a microchemical approach, we measured changes of amino acid concentrations in the chinchilla caudal posteroventral cochlear nucleus (PVCN) after cochlear ablation to determine to what extent slow decreases of glutamate and aspartate concentrations after carboplatin treatment resulted from slower effects of cochlear damage in chinchillas than in rats and guinea pigs, as opposed to effects of carboplatin treatment being slower than those of cochlear ablation. Our results indicate that both factors are involved: decreases of glutamate and aspartate concentrations after cochlear ablation are much slower in chinchillas than in rats and guinea pigs, but they are much faster than the decreases after carboplatin treatment. Further, aspartate and glutamate concentrations in the chinchilla caudal PVCN decreased by larger amounts after cochlear ablation than in rats or guinea pigs, and there was a transient increase of aspartate concentration at short survival times. Detailed mapping of amino acid concentrations in the PVCN of a chinchilla with 1 month survival after cochlear ablation and a rat with 7 days' survival indicated that the reductions of glutamate and aspartate occurred throughout the PVCN but were somewhat larger in ventral and caudal parts in chinchilla. Any decreases in the adjacent granular region were very small. There were also sustained bilateral decreases in concentrations of other amino acids, notably GABA and glycine, in the caudal PVCN of cochlea-ablated chinchillas but not rats. The effects of cochlear ablation on the concentrations of most of these other amino acids in chinchilla caudal PVCN differed from those of carboplatin treatment. Thus, although a major effect of auditory nerve damage on the cochlear nucleus—decreases of glutamate and aspartate concentrations—occurs across species and types of lesions, the details of timing and magnitude and the effects on other amino acids can vary greatly.

Section snippets

Experimental procedures

Most of the procedures used in this study have been described previously (Godfrey and Matschinsky 1976, Ross et al 1995, Godfrey et al 2000, Godfrey et al 2005).

Effects of cochlear ablation on PVCN structural parameters

The volume of the PVCN on the lesioned side appeared to decrease by 84 days after unilateral cochlear ablation (Table 1). Because of the small numbers of measurements (one per cochlear nucleus) and sizable variation in PVCN volume even among sham animals, analysis of variance indicated no significant differences among the groups, even though the average at 84 days was significantly different from the sham average by t-test (P=0.002). The consistency of the volume reduction at 84 days for the

Considerations in interpreting the results

Although the most prominent changes in amino acid concentrations should be closely associated with the degeneration of auditory nerve fibers, the spatial resolution of the microchemical approach as applied here does not enable determination of which other neurons or glia may also be the sites of changes. However, previous measurements have suggested that concentrations of aspartate, glutamate, and serine are at least twice as high in neurons and GABA more than 10 times as high; glutamine and

Conclusions

Our results indicate that the slowness of the decreases of glutamate and aspartate concentrations in the chinchilla PVCN after carboplatin treatment relates partially to a slower loss of these amino acids from the central terminal regions of auditory nerve fibers during their degeneration in chinchillas than in rats or guinea pigs and partially to slower deterioration of the central terminal regions of auditory nerve fibers after carboplatin treatment than after cochlear ablation.

Our findings

Acknowledgments

We are grateful to Brent Martin, D.V.M., and his staff of the Division of Laboratory Animal Medicine of the University of Toledo Health Science Campus for assistance and advice at various stages of this project. Support for this research was received from the American Tinnitus Association and the University of Toledo Foundation.

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      However, the average thickness of the AudCtx was measured in several sections of each rat as the distance from its surface to the underlying external capsule. Free amino acid concentrations were measured by an HPLC assay (Hill et al., 1979; Ross et al., 1995; Godfrey et al., 2000, 2008, 2012, 2014, 2015). To each sample tube and some empty blank tubes were added 16 μL of 50% (vol/vol) methanol, containing an internal standard amino acid not present in the tissue (β-[2-thienly]-DL-serine) to correct for variations in injection volume.

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      The procedures used in this study were the same as used in our report on the chinchilla PVCN (Godfrey et al., 2008) and have been described previously (Godfrey and Matschinsky, 1976; Godfrey et al., 1977, 2000, 2008, 2014; Ross et al., 1995). The results are from the same chinchillas as used in our previous report on the PVCN (Godfrey et al., 2008). Eighteen adult chinchillas, one female and 17 male, obtained from Jarr Chinchilla, Hubbard, Ohio, USA, were divided into several cochlear-ablated and sham-lesioned groups (Table 1).

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      A preliminary report of results from this study has been presented (Godfrey et al., 2004a). Some of the results for the PVCN were included in a previous publication (Godfrey et al., 2008a), but they are also included here for completeness. The results are compared to those obtained previously for the other eighth cranial nerve system, the vestibular nuclear complex and its vestibular nerve root, after removal of its inner ear input by vestibular ganglionectomy (Li et al., 1996; Godfrey et al., 2004b).

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    Present address: K. Chen, Hough Ear Institute, Oklahoma City, OK, USA; Y.-M. Jin, Department of Neurosciences, Lerner Research Institute, Cleveland Clinic, Cleveland, OH, USA.

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