Neonatal sensorineural hearing loss affects synaptic density in the auditory midbrain

Abstract

We examined the effect of neonatal sensorineural hearing loss on synaptic density in the central nucleus of the inferior colliculus (ICC) of adult cats to evaluate the role of auditory experience in synaptogenesis. Three groups of animals were used: bilaterally deafened, unilaterally deafened and normal hearing controls. Synaptic density in bilaterally deafened animals was significantly lower than in normal hearing animals. By contrast, there was no significant difference in synaptic density between normal hearing animals and unilaterally deaf animals. These results demonstrate, for the first time, that a sensorineural hearing loss during development can affect synaptogenesis in the auditory midbrain.

Spatial Selectivity to Intracochlear Electrical Stimulation in the Inferior Colliculus is Degraded After Long-Term Deafness in Cats

“…Also deafnessinduced changes in the central auditory system may contribute to the decreased spatial selectivity after long-term deafness. Such changes include alterations in the balance between excitatory and inhibitory inputs to the ICC (Raggio and Schreiner 1999;Schreiner and Raggio 1996) and decreases in the synaptic density in the IC of neonatally deafened animals (Hardie et al 1998). In contrast to the present findings, Shepherd and colleagues (Shepherd and Javel 1997;Shepherd et al 1999) observed increased dynamic ranges following long-term deafness, although it must be noted that this result was obtained from only one experimental animal that was deafened as a juvenile.…”

“…Among the possible explanations are the loss of myelin and partial neural degeneration that not only lead to a larger distance between the stimulating contacts and the population of excitable neural targets but also to prolonged refractory periods and an increased vulnerability of the propagating spike. In the central auditory system, a weakening of individual excitatory synapses (Kotak and Sanes 1997), a decrease in excitatory neurotransmitter release (Vale and Sanes 2002), a reduction in the volume of the cochlear nuclei, reduced size and/or loss of auditory brain stem neurons and a decrease in synaptic density in the IC (Hardie et al 1998;Nadol et al 1989;Nishiyama et al 2000;Otte et al 1978;Saada et al 1996) may contribute to an overall reduction in conduction, synaptic efficacy, and synchrony of afferent connections along the ascending central auditory system and thus to increased response thresholds.…”

“…Animal studies have shown that hearing loss induced during the early postnatal period results in progressive and more profound anatomical degeneration in the central auditory system (e.g., Lustig et al 1994;Moore 1990;Nishiyama et al 2000;Nordeen et al 1983) and functional degradation or reorganization as compared with changes observed following auditory deprivation later in life (e.g., Hardie et al 1998;Moore et al 2002;Raggio and Schreiner 1999;Shepherd and Javel 1997;Shepherd et al 1999;Silverman and Clopton 1977;Trune 1982). At the University of California San Francisco (UCSF), we have developed an animal model of neonatal or very early acquired profound hearing loss to evaluate the effects of early auditory deprivation and duration of deafness on signal processing in the central auditory system.…”

Degradation of Temporal Resolution in the Auditory Midbrain After Prolonged Deafness Is Reversed by Electrical Stimulation of the Cochlea

“…Within the cochlea the changes include progressive demyelination of spiral ganglion neurons, loss of their peripheral processes, and degeneration of their somata. Within the central auditory system, the changes include reduction in the volume of the cochlear nuclei, shrinkage or loss of auditory brain stem neurons, a reduction in the synaptic density within the central nucleus of the inferior colliculus (ICC), and a degradation in the temporal resolution and spatial selectivity of physiological responses (Hardie et al 1998;Nadol et al 1989;Nishiyama et al 2000;Otte et al 1978;Snyder et al 1995;Vollmer et al 1999Vollmer et al , 2000. The age at onset of deafness is an important factor determining the extent of these pathological changes, suggesting a critical period for normal development of the auditory system (human studies: Eggermont and Bock 1986;Ruben and Rapin 1980;animal studies: Silverman and Clopton 1977;Webster 1983Webster , 1988.…”

Cochlear Implants in Children: A Review

“…These could include the anatomical structure and physiology of the ears, effects of the pathology that caused the hearing loss, and in the case of children who receive two cochlear implants separated in time (sequential implantation), the duration of deafness will differ between the ears. A further reason for bilateral cochlear implantation is to prevent the neural degeneration that has been documented in humans and animal studies as a result of auditory deprivation (Hardie, 1998;Sharma et al, 2002;Shepherd, 1997). Bilateral implantation also ensures that children still have hearing in the case of speech processor or device failure in one ear, which can significantly reduce stress for children and their families if these events occur.…”