Noise trauma alters D‐[³H]aspartate release and AMPA binding in chinchilla cochlear nucleus

Abstract

Exposure of adults to loud noise can overstimulate the auditory system, damage the cochlea, and destroy cochlear nerve axons and their synaptic endings in the brain. Cochlear nerve loss probably results from the death of cochlear inner hair cells (IHC). Additional degeneration in the cochlear nucleus (CN) is hypothesized to stem from overstimulation of the system, which may produce excitotoxicity. This study tested these predictions by exposing one ear of anesthetized adult chinchillas to a loud noise, which damaged the ipsilateral cochlea and induced degeneration in the glutamatergic cochlear nerve. During the first postexposure week, before cochlear nerve axons degenerated, glutamatergic synaptic release in the ipsilateral CN was elevated and uptake was depressed, consistent with hyperactivity of glutamatergic transmission and perhaps with the operation of an excitotoxic mechanism. By 14 days, when cochlear nerve fibers degenerated, glutamatergic synaptic release and uptake in the CN became deficient. By 90 days, a resurgence of transmitter release and an elevation of AMPA receptor binding suggested transmission upregulation through plasticity that resembled changes after mechanical cochlear damage. These changes may contribute to tinnitus and other pathologic symptoms that precede and accompany hearing loss. In contrast, the other ear, protected with a silicone plug during the noise exposure, exhibited virtually no damage in the cochlea or the cochlear nerve. Altered glutamatergic release and AMPA receptor binding activity in the CN suggested upregulatory plasticity driven by signals emanating from the CN on the noise-exposed side.

Can homeostatic plasticity in deafferented primary auditory cortex lead to travelling waves of excitation?

“…In particular, the intrinsic excitability of the pyramidal neurons in the deafferented region of A1 is shown to be enhanced (Kotak et al 2005). Moreover, the excitatory synapses targeted on the deafferented neurons are strengthened (Vale et al 2002;Muly et al 2004;Kotak et al 2005) while the inhibitory synapses are weakened (Suneja et al 1998a, b;Vale et al 2002;Kotak et al 2005). These synaptic regulations are consistent with homeostatic plasticity, previously observed in the hippocampus ) and the visual cortex (Desai et al 2002).…”

Noise-induced hyperactivity in the inferior colliculus: its relationship with hyperactivity in the dorsal cochlear nucleus

“…Finally, one cannot discount the possibility that homeostatic mechanisms, as described by Schaette and Kempter (2006), might have compensated for any acute loss of hyperactivity that DCN ablation might have caused. In line with this view, earlier works have shown that deafferentation of central auditory centers leads to long-term effects that are very different from those observed shortly after the deafferenting procedure Morest et al 1997;Muly et al 2004;Suneja et al 1998aSuneja et al , 1998b. Studies examining the time course of the effects of complete DCN ablation on IC or cortical activity or on tinnitus would be of great value in bringing clarity to these issues.…”

Dorsal cochlear nucleus response properties following acoustic trauma: Response maps and spontaneous activity

“…More relevant to the present work are studies in which acoustic trauma was used. Following trauma, degeneration of axons and cells in the cochlear nucleus occurs (Bilak et al, 1997;Muly et al, 2002;Kim et al, 2004b;Muly et al, 2004). The initial loss includes both excitatory and inhibitory synapses, but there is a return of excitatory synapses and of glutamate release and uptake, without a corresponding increase in inhibitory synapses.…”

“…Although the lesions produced by acoustic trauma are in the cochlea, secondary effects in the central nervous system may be important in determining the perceptual consequences of trauma (reviewed by Syka, 2002). Central effects of cochlear damage or ablation include degeneration of axons and neurons (Born and Rubel, 1988;Morest et al, 1998;Redd et al, 2000;Muly et al, 2002), formation of new synaptic connections (Kim et al, 2004a;Muly et al, 2004), rewiring of central circuits (Nordeen et al, 1983;Rajan et al, 1993;Leake et al, 2000), and changes in synaptic strength to favor excitation over inhibition (Suneja et al, 1998a;Abbott et al, 1999;Milbrandt et al, 2000;Mossop et al, 2000;Oleskevich and Walmsley, 2002;Vale and Sanes, 2002;Kim et al, 2004a). Each of these could influence substantially the central representation of sound.…”