Distribution of synaptic ribbons in the developing organ of Corti

Abstract

Studies of synaptogenesis in the developing organ of Corti in the intact mouse and in culture indicate that the inner and outer hair cells contain three populations of synaptic ribbons, i.e. ribbons adjacent to nerve fibres, free intracellular ribbons and misplaced ribbons apposed to non-neuronal elements. Ribbons adjacent to nerve fibres can be further classified into: ribbons synaptically engaged, ribbons participating in formation of presynaptic complexes only and ribbons that are not engaged to the hair cell membrane. In the developing innervated cultures the ribbon distributions are similar to those in the normal animal. Inner and outer hair cells differ in distribution of the ribbons. In the inner hair cells the ribbons adjacent to the nerve fibres are dominant (over 90%) and most of them (88%) are synaptically engaged. In the outer hair cells the presynaptic ribbons dominate the population (up to 60%) during the first postnatal week when the cells acquire afferent synaptic connections. This stage is followed by a marked reduction in the number of all ribbons. In the intact animal the rapid decrease results in a relative increase of misplaced and free ribbons. These changes are presumably due to the loss of some of the afferents. In the denervated hair cells the distribution of ribbons indicated the presence of conspicuous scatter. In the areas of incomplete denervation, however, the ribbons are apposed to the preserved fibres. Despite denervation, most of the ribbons develop the entire presynaptic complex in apposition to non-neuronal structures. The different populations of synaptic ribbons appear to reflect different stages in synapse formation. Possibly, the synaptic body originates in the interior of the hair cell and subsequently migrates to the cell membrane. In any case, a nerve fibre appears critical in influencing the location of the synaptic ribbon. At the apposition of the ribbon to the hair cell membrane, presynaptic densities are formed and the ribbon appears to become anchored. Typically, the nerve fibre membrane apposed to the presynaptic complex responds with the formation of postsynaptic densities.

Tyrosine Hydroxylase Expression in Type II Cochlear Afferents in Mice

“…The presence of ribbon-associated and ribbon-free afferent synapses was also seen in 3D reconstructions from serial section TEM of mouse OHCs. These showed that half of all afferent contacts were ribbon-free, reminiscent of earlier reports of ribbon-less contacts in various species (Dunn and Morest 1975;Francis and Nadol 1993;Liberman et al 1990;Nadol 1983;Sobkowicz et al 1986). Pre-and postsynaptic immunolabeling in rat showed that only half of the postsynaptic densities in type II boutons were associated with ribbons in OHCs (Martinez-Monedero 2016).…”

Relationship between the Development of Outer Hair Cell Electromotility and Efferent Innervation: A Study in Cultured Organ of Corti of Neonatal Gerbils

“…However, this study at least demonstrates that removal of afferent innervation at birth does not hinder further development of OHCs. A similar conclusion was also reached by Sobkowicz et al (1986), who demonstrated that removal of afferent innervation at birth did not hinder further morphological development of hair cells or cause any degeneration of the organ of Corti in tissue culture.…”

“…A number of investigations were also targeted to the question of how the presence of neuronal elements or the pattern of innervation exert influence on the cytodifferentiation of sensory cells (Knowlton, 1967;Orr, 1968;Sher, 1971;Thornhill, 1972;Van de Water, 1976, 1986, 1988Van de Water et al, 1984Pirvola et al, 1991). No attempt has been made to test directly the hypothesis that efferent innervation regulates the maturation of OHCs.…”

Alternative Splicing of the CaV1.3 Channel IQ Domain, a Molecular Switch for Ca2+-Dependent Inactivation within Auditory Hair Cells

“…Second, weak CDI could help prolong Ca 2ϩ entry that would sustain activity-dependent transcription underlying outer hair cell development (Platzer et al, 2000;Brandt et al, 2003;Glueckert et al, 2003). During the development of hearing, cochlear hair cells undergo major changes in potassium (Kros et al, 1998;Marcotti et al, 2003) and calcium channel expression (Beutner and Moser, 2001;Michna et al, 2003), as well as dramatic rearrangement of efferent and afferent innervation (Liberman and Simmons, 1985;Sobkowicz et al, 1986Sobkowicz et al, , 2004Simmons and Liberman, 1988a,b;Simmons et al, 1992Simmons et al, , 1996Simmons, 1994Simmons, , 2002Fuchs et al, 2003;Bergeron et al, 2005). Hence, the early presence of Ca V 1.3 IQ⌬ channels, as well as the loss of OHCs shortly after the onset of hearing in Ca V 1.3 knock-out mice (Platzer et al, 2000), cohere with a contribution of these channels to activity-dependent gene expression underlying development.…”