Synaptic plasticity in the medial superior olive of hearing, deaf, and cochlear‐implanted cats

Abstract

The medial superior olive (MSO) is a key auditory brain-stem structure that receives binaural inputs and is implicated in processing interaural time disparities used for sound localization. The deaf white cat, a proven model of congenital deafness, was used to examine how deafness and cochlear implantation affected the synaptic organization at this binaural center in the ascending auditory pathway. The patterns of axosomatic and axodendritic organization were determined for principal neurons from the MSO of hearing, deaf, and deaf cats with cochlear implants. The nature of the synapses was evaluated through electron microscopy, ultrastructure analysis of the synaptic vesicles, and immunohistochemistry. The results show that the proportion of inhibitory axosomatic terminals was significantly smaller in deaf animals when compared with hearing animals. However, after a period of electrical stimulation via cochlear implants the proportion of inhibitory inputs resembled that of hearing animals. Additionally, the excitatory axodendritic boutons of hearing cats were found to be significantly larger than those of deaf cats. Boutons of stimulated cats were significantly larger than the boutons in deaf cats, although not as large as in the hearing cats, indicating a partial recovery of excitatory inputs to MSO dendrites after stimulation. These results exemplify dynamic plasticity in the auditory brainstem and reveal that electrical stimulation through cochlear implants has a restorative effect on synaptic organization in the MSO.

Congenital and Prolonged Adult-Onset Deafness Cause Distinct Degradations in Neural ITD Coding with Bilateral Cochlear Implants

“…Chronic diotic stimulation using clinical CI processors largely reverses these changes (O'Neil et al 2010;Tirko and Ryugo 2012). In the cat IC, neonatal deafening degrades pulse-locking limits to unilateral CI stimulation compared to acutely deafened cats (Snyder et al 1995;Vollmer et al 2005).…”

Feline Deafness

“…Reductions of cochlear nerve input to the brain have been produced by drugs, nerve section or cochlear ablation, and noise trauma. These measures produce dramatic changes in the structure and function of the central auditory pathway [81–90]. Are the pathologic changes due to the side effects of experimental manipulations, missing sensory receptors, absent cochlear nerve activity, or deafness regardless of cause?…”

“…Congenital deafness causes a bilateral disruption in the spatially segregated inputs to the MSO principal neurons such that inhibitory input at the cell body is significantly reduced compared to what is observed in hearing animals [90,111]. This change in axosomatic inhibition was manifest by a loss of staining for gephyrin, an anchoring protein for the glycine receptor [111] and the migration of terminals containing flattened and pleomorphic synaptic vesicles (indicative of inhibitory synapses) away from the cell body [90].…”

“…This change in axosomatic inhibition was manifest by a loss of staining for gephyrin, an anchoring protein for the glycine receptor [111] and the migration of terminals containing flattened and pleomorphic synaptic vesicles (indicative of inhibitory synapses) away from the cell body [90]. Excitatory inputs to the dendrites were severely shrunken [90] and the dendrites themselves atrophied [115]. …”

In VivoReversible Regulation of Dendritic Patterning by Afferent Input in Bipolar Auditory Neurons

“…Although afferent or sensory deprivation has been shown to slow dendritic growth or affect dendritic stability in a number of systems (e.g., Wong and Ghosh, 2002; Groc et al, 2002; Mizrahi and Katz, 2003), the current study provides the first in vivo observation that such changes in dendritic branch length can be reversed by recovery of normal afferent activity. Dynamic plasticity in the auditory brainstem has also been recently demonstrated in deaf cats in which electrical stimulation through cochlear implants has a restorative effect on synaptic organization in the medial superior olive, the mammalian analogues of the avian NL (Tirko and Ryugo, 2012). These forms of in vivo plasticity are consistent with studies demonstrating that enriched sensory inputs or electrical stimulation enhances dendritic growth (Sin et al, 2002; Faherty et al, 2003).…”