Fine structure of degeneration in the cochlear nucleus of the chinchilla after acoustic overstimulation

Abstract

To study plastic changes in the cochlear nucleus after acoustic stimulation, adult chinchillas were exposed once to a 4-kHz octave-band noise at 108 dB SPL for 3 hr. After survival times of 1, 2, 4, 8, and 16 weeks, samples were taken for electron microscopy from a part of the cochlear nucleus, where cochlear nerve fibers degenerated after the noise exposure. Progressive changes in fine structure were characterized as early, intermediate, and late stages of degeneration. Freshly occurring synaptic degeneration appeared in each period from 1-16 weeks. Endings with large round vesicles, putative excitatory synapses of the cochlear nerve, displayed progressive increases in neurofilaments and enlarged synaptic vesicles. Compared to controls, synaptic vesicles seemed fewer, often in small clusters in the interior of endings, and smaller in the synaptic zone. These early changes progressed to mitochondrial disintegration and overt "watery" degeneration. Some surviving endings, however, were shrunken and displaced partially by enlarged spaces in the synaptic complex. Dense-cored vesicles gathered in these endings. In terminals with pleomorphic and flattened vesicles, presumed inhibitory endings, cytological changes appeared within 1 week and persisted for months. The synaptic endings darkened, some vesicles disintegrated, and many smaller flatter vesicles collapsed into heaps. Especially at the presynaptic membrane, vesicles were shriveled, but a few mitochondria were preserved. Without overt signs of synaptic degeneration, some of these cytological changes presumably reflect reduced synaptic activity in the inhibitory endings. These changes may contribute to a continuing process associated with abnormal auditory functions, including hyperacusis and tinnitus.

Fine structure of long‐term changes in the cochlear nucleus after acoustic overstimulation: Chronic degeneration and new growth of synaptic endings

“…Either the surviving ganglion cells or the central neurons and their processes, perhaps by changes in their activity, could play a role in initiating the newly occurring synaptic degeneration. All intermediate stages of change described previously for shorter survival times (Kim et al, 2004a) were seen in the longer survivals, including the early stages (less often) and the late stages (more often). There was increasing evidence of totally vacated synaptic sites in the longer survivors.…”

“…The normal fine structure of the anterior part of the ventral cochlear nucleus in the chinchilla is described in a companion study (Kim et al, 2004a). The basic structure was found to be unchanged in age-matched controls for the longest survival times, up to 8 months.…”

“…2), although shrinkage of globular bushy cells was readily apparent and many cells did display pathologic signs. The watery and dense modes of synaptic degeneration (described by Kim et al, 2004a) occurred in the T1A and T3A endings, respectively (Fig. 2).…”

“…Noise-induced hearing loss thus may progress as a neurodegenerative disease with the capacity for synaptic reorganization within the cochlear nucleus. Key words: auditory system; synaptic plasticity; neurodegenerative disease; deafness; noise; tinnitusThe rapid onset of synaptic degeneration in the cochlear nucleus after acoustic overstimulation has been described in a previous report on the fine structure of the cochlear nucleus in chinchillas (Kim et al, 2004a). That study showed that, after a single noise exposure, synaptic endings of a number of different types underwent cytological changes within a few days of noise damage to the cochlea.…”

“…The same protocols were followed as described in a companion study (Kim et al, 2004a). Cytocochleograms were prepared for both the exposed and unexposed cochleas in each animal.…”