Olivocochlear innervation of inner and outer hair cells during postnatal maturation: Evidence for a waiting period

Abstract

Reconstructions of the efferent innervation of the hamster (Mesocricetus auratus) cochlea were done during postnatal development. Efferent neurons were labeled via injections of biocytin and horseradish peroxidase into the crossed olivocochlear (OC) bundles using an in vitro brainstem technique. Such injections retrogradely labeled cell bodies in ventral periolivary regions of the superior olive consistent with their being medial OC neurons. Anterogradely labeled axons were traced to the cochlea, where they terminated on or below inner hair cells (IHCs) prior to postnatal day 5 (P5). After P5, labeled axons terminated on IHCs and outer hair cells (OHCs) and after P10, the majority of labeled axons terminated on the OHCs. In the electron microscope, small labeled terminals containing densely packed synaptic vesicles were found both adjacent to IHCs (axosomatic) as well as apposed to afferent and efferent fibers below IHCs prior to P5. By P10, large labeled terminals were axosomatic to OHCs and no longer found on IHCs. Consistent with previous reports, these data suggest that medial OC axons form part of an early primary innervation on and below IHCs before terminating on OHCs. This raises the possibility that OC neurons demonstrate a period of waiting below an intermediate target similar to that described in the development of thalamocortical projections.

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.…”

The Final Stage of Cholinergic Differentiation Occurs Below Inner Hair Cells During Development of the Rodent Cochlea

“…In either case, our findings are consistent with the idea that efferent axons arrive below inner hair cells, and undergo some further differentiation, such as ChT1 expression, prior to contacting OHCs. We have previously termed this period of differentiation below IHCs a developmental waiting period, which occurs prior to OHCs efferent terminations (Simmons et al 1996a;Simmons 2002).…”

Developmental Regulation of Nicotinic Synapses on Cochlear Inner Hair Cells

“…In particular, IHCs initially are contacted by olivocochlear efferent fibers that "wait" under the IHC region before targeting OHCs (Simmons et al, 1996b). This transition occurs around the onset of hearing, and adult IHCs are innervated mainly by afferent fibers, having few if any remaining efferent contacts (Liberman et al, 1990).…”