Regulation ofd-Aspartate Release and Uptake in Adult Brain Stem Auditory Nuclei after Unilateral Middle Ear Ossicle Removal and Cochlear Ablation

doi:10.1006/exnr.1997.6641

Experimental Neurology

Volume 148, Issue 1, November 1997, Pages 222-235

https://doi.org/10.1006/exnr.1997.6641 Get rights and content

Abstract

In young adult guinea pigs, the effects of unilateral ossicle removal and cochlear ablation were determined on transmitter release from glutamatergic presynaptic endings and glutamate inactivation via uptake. (i)d-[³H]Aspartate release and uptake were measured in subdivisions of the cochlear nucleus (CN) and in nuclei of the superior olive (SOC) and auditory midbrain (MB) up to 145 days after placing the lesions. Activities were compared to those from age-matched unlesioned controls. Fiber degeneration was visualized histologically. (ii) In the ipsilateral CN, changes in release and uptake were governed by the type of lesion. Ossicle removal produced sparse pruning of fibers only after 112 days and decreased release and uptake at 145 days, consistent with regulatory weakening of excitatory glutamatergic transmission. Cochlear ablation deafferented the CN, producing deficient release and uptake at 2 days and abundant fiber degeneration at 7 days. Subsequently, the residual release and uptake increased in magnitude, consistent with strengthening of excitatory glutamatergic transmission. (iii) In the contralateral CN, after either lesion, changes in release and uptake usually matched those in the ipsilateral CN. Thus, the auditory pathway associated with the lesioned ear probably provided cues for the regulation of synaptic strength in the contralateral CN. (iv) Both lesions increased release in the SOC and MB, and uptake in the SOC, consistent with strengthening of excitatory glutamatergic transmission. Sparse fiber degeneration, suggesting axonal pruning, appeared in the SOC and MB after cochlear ablation. (v) The strengthening of excitatory glutamatergic transmission may facilitate and maintain symptoms such as loudness recruitment and tinnitus which often accompany hearing loss.

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Acquired hearing loss results in an imbalance of the cochlear output across frequency. Central auditory system homeostatic processes responding to this result in frequency specific gain changes consequent to the emerging imbalance between excitation and inhibition. Several consequences thereof are increased spontaneous firing rates, increased neural synchrony, and (in adults) potentially restricted to the auditory thalamus and cortex a reorganization of tonotopic areas. It does not seem to matter much whether the hearing loss is acquired neonatally or in adulthood. In humans, no clear evidence of tonotopic map changes with hearing loss has so far been provided, but frequency specific gain changes are well documented. Unilateral hearing loss in addition makes brain activity across hemispheres more symmetrical and more synchronous. Molecular studies indicate that in the brainstem, after 2–5 days post trauma, the glutamatergic activity is reduced, whereas glycinergic and GABAergic activity is largely unchanged. At 2 months post trauma, excitatory activity remains decreased but the inhibitory one is significantly increased. In contrast protein assays related to inhibitory transmission are all decreased or unchanged in the brainstem, midbrain and auditory cortex. Comparison of neurophysiological data with the molecular findings during a time-line of changes following noise trauma suggests that increases in spontaneous firing rates are related to decreases in inhibition, and not to increases in excitation. Because noise-induced hearing loss in cats resulted in a loss of cortical temporal processing capabilities, this may also underlie speech understanding in humans.
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Similarities in the effects of cochlear ablation and carboplatin administration could reflect the destruction of inner hair cells that results from both procedures, whereas the differences in effects might reflect the destruction of outer hair cells by cochlear ablation, but not to any significant extent by carboplatin (Takeno et al., 1998; Ding et al., 1999; Li et al., 2002). Previous publications have described effects of cochlear ablation on uptake, release, and receptors for glutamate, glycine, and GABA neurotransmission in guinea pigs (Potashner et al., 1985, 1997, 2000; Suneja et al., 1998a,b, 2000) and rats (Li et al., 1997). Detailed comparisons between the results of these studies and those of our measurements of amino acid levels have been recently presented (Lee and Godfrey, 2014).
Inner ear damage can lead to hearing disorders, including tinnitus, hyperacusis, and hearing loss. We measured the effects of severe inner ear damage, produced by cochlear ablation, on the levels and distributions of amino acids in the first brain center of the auditory system, the cochlear nucleus. Measurements were also made for its projection pathways and the superior olivary nuclei. Cochlear ablation produces complete degeneration of the auditory nerve, which provides a baseline for interpreting the effects of partial damage to the inner ear, such as that from ototoxic drugs or intense sound. Amino acids play a critical role in neural function, including neurotransmission, neuromodulation, cellular metabolism, and protein construction. They include major neurotransmitters of the brain – glutamate, glycine, and γ-aminobutyrate (GABA) – as well as others closely related to their metabolism and/or functions – aspartate, glutamine, and taurine. Since the effects of inner ear damage develop over time, we measured the changes in amino acid levels at various survival times after cochlear ablation. Glutamate and aspartate levels decreased by 2 weeks in the ipsilateral ventral cochlear nucleus and deep layer of the dorsal cochlear nucleus, with the largest decreases in the posteroventral cochlear nucleus (PVCN): 66% for glutamate and 63% for aspartate. Aspartate levels also decreased in the lateral part of the ipsilateral trapezoid body, by as much as 50%, suggesting a transneuronal effect. GABA and glycine levels showed some bilateral decreases, especially in the PVCN. These results may represent the state of amino acid metabolism in the cochlear nucleus of humans after removal of eighth nerve tumors, which may adversely result in destruction of the auditory nerve. Measurement of chemical changes following inner ear damage may increase understanding of the pathogenesis of hearing impairments and enable improvements in their diagnosis and treatment.
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There are a few differences: the effects on aspartate and glutamate were similar in rat cochlear nucleus, whereas in guinea pig the effects on aspartate were generally larger than those on glutamate, and the effects on both amino acids in the DCN deep layer were larger and those on aspartate in the AVCN smaller in rat than in guinea pig. Our results for glutamate and aspartate are in some ways consistent with previous reports of changes in release and uptake of d-aspartate, as representative of synaptic release and uptake of glutamate, in guinea pigs (Potashner et al., 1997), in that decreases were found in AVCN, PVCN, and DCN after cochlear ablation. However, the release and uptake measurements showed more contralateral changes than our measurements of glutamate and aspartate levels and larger relative ipsilateral changes for release, especially at 2 days after cochlear ablation.
Amino acids have important roles in the chemistry of the auditory system, including communication among neurons. There is much evidence for glutamate as a neurotransmitter from auditory nerve fibers to cochlear nucleus neurons. Previous studies in rodents have examined effects of removal of auditory nerve input by cochlear ablation on levels, uptake and release of glutamate in cochlear nucleus subdivisions, as well as on glutamate receptors. Effects have also been reported on uptake and release of γ-aminobutyrate (GABA) and glycine, two other amino acids strongly implicated in cochlear nucleus synaptic transmission. We mapped the effects of cochlear ablation on the levels of amino acids, including glutamate, GABA, glycine, aspartate, glutamine, taurine, serine, threonine, and arginine, in microscopic subregions of the rat cochlear nucleus. Submicrogram-size samples microdissected from freeze-dried brainstem sections were assayed for amino acid levels by high performance liquid chromatography. After cochlear ablation, glutamate and aspartate levels decreased by 2 days in regions receiving relatively dense innervation from the auditory nerve, whereas the levels of most other amino acids increased. The results are consistent with a close association of glutamate and aspartate with auditory nerve fibers and of other amino acids with other neurons and glia in the cochlear nucleus. A consistent decrease of GABA level in the lateral superior olive could be consistent with a role in some lateral olivocochlear neurons. The results are compared with those obtained with the same methods for the rat vestibular nerve root and nuclei after vestibular ganglionectomy.
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The dynamics of synaptic transmission between neurons plays a major role in neural information processing. In the cochlear nucleus, auditory nerve synapses have a relatively high release probability and show pronounced synaptic depression that, in conjunction with the variability of interspike intervals, shapes the information transmitted to the postsynaptic cells. Cellular mechanisms have been best analyzed at the endbulb synapses, revealing that the recent history of presynaptic activity plays a complex, non-linear, role in regulating release. Emerging evidence suggests that the dynamics of synaptic function differs according to the target neuron within the cochlear nucleus. One consequence of hearing loss is changes in evoked release at surviving auditory nerve synapses, and in some situations spontaneous release is greatly enhanced. In contrast, even with cochlear ablation, postsynaptic excitability is less affected. The existing evidence suggests that different modes of hearing loss can result in different dynamic patterns of synaptic transmission between the auditory nerve and postsynaptic neurons. These changes in dynamics in turn will affect the efficacy with which different kinds of information about the acoustic environment can be processed by the parallel pathways in the cochlear nucleus.

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^☆: R. A. AltschulerR. P. BobbinB. M. CloptonD. W. Hoffmann, Eds.

¹: To whom correspondence should be addressed. Fax: (860)-679-1274. E-mail: [email protected].

²: Present address: Department of Neurobiology, Duke University Medical Center, Durham, NC 27710.

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Regular ArticleRegulation ofd-Aspartate Release and Uptake in Adult Brain Stem Auditory Nuclei after Unilateral Middle Ear Ossicle Removal and Cochlear Ablation☆

Abstract

Toxicon

Neuroscience

Exp. Neurol.

Brain Res.

Curr. Opin. Neurobiol.

Brain Res.

Hear. Res.

Hear. Res.

Neurosci. Lett.

Neurosci. Res.

Hear. Res.

Neuroscience

Neuroscience

J. Biol. Chem.

Am. J. Otolaryngol.

Brain Res.

Hear. Res.

Hear. Res.

Curr. Opin. Neurobiol.

Brain Res.

Brain Res.

Brain Res.

Neuroscience

The structural specificity of the high affinity uptake ofll

J. Neurochem.

Activation of protein kinase C augments peptide release from rat sensory neurons

J. Neurochem.

3d+

J. Neurosci. Res.

Retrograde transport of [3

J. Comp. Neurol.

Long-term effect of cochlear and middle ear lesions on synaptic transmitter release in the cochlear nucleus

Soc. Neurosci. Abstr.

Synaptophysin immunoreactivity in the cochlear nucleus after unilateral cochlear or ossicular removal

Synapse

Functional changes in the ventral cochlear nucleus following acute acoustic overstimulation

J. Acoust. Soc. Am.

Projections to the lateral and medial superior olivary nuclei from the spherical and globular bushy cells of the anteroventral cochlear nucleus

Neurobiology of Hearing: The Central Auditory System

Two populations of commissural projections connecting like regions of the inferior colliculus immunostain for different amino acid transmitters

Soc. Neurosci. Abstr.

Immunocytochemical and neurochemical evidence of age-related loss of GABA in the inferior colliculus: Implications for neural presbycusis

J. Neurosci.

Fluoroacetate and fluorocitrate: Mechanism of action

Neurochem. Res.

Attenuation and protection provided by ossicular removal

J. Acoust. Soc. Am.

Uptake and release ofdl

J. Neurochem.

Evidence for a glutamatergic pathway from the guinea pig auditory cortex to the inferior colliculus

J. Neurochem.

Direct projections from the rat primary auditory cortex to nucleus sagulum, paralemniscal regions, superior olivary complex and cochlear nuclei

Auditory Neurosci.

Relation between lateralization and loudness in asymmetrical hearing loss

J. Am. Audiol. Soc.

Central denervation hypersensitivity in the auditory system of the cat

J. Acoust. Soc. Am.

Neurotransmitter microchemistry of the cochlear nucleus and superior olivary complex

Regular Article
Regulation ofd-Aspartate Release and Uptake in Adult Brain Stem Auditory Nuclei after Unilateral Middle Ear Ossicle Removal and Cochlear Ablation☆

³d⁺

Retrograde transport of [³