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Developmental segregation in the efferent projections to auditory hair cells in the gerbil

The auditory receptor epithelium of mammals receives efferent innervation from neurons within and surrounding the superior olivary complex of the brainstem (Warr [1975] J. Comp. Neurol. 161:159–181). Disruption of this pathway during early postnatal life, when olivocochlear axons are forming their final connections with auditory hair cells and nerve fibers, can lead to profound and permanent hearing impairments (Walsh et al. [1998] J. Neurosci. 18:3859–3869). Identification of the possible causes for this deterioration in auditory function requires a better understanding of the normal developmental interactions that occur between efferent axons and their target cells within the cochlea. To provide such information, we labeled developing efferent fibers at a constant location within the gerbil cochlea by using the fluorescent carbocyanine dye 1,1′‐dioctadecyl‐3,3,3′,3′‐tetramethylindo‐carbocyanine perchlorate (DiI). The terminal arbors of these neurons were then reconstructed by using digital confocal microscopy. By postnatal day (P) 2, the efferent arbors associated with inner hair cells (IHCs) and outer hair cells (OHCs) displayed distinctly different morphologies closely resembling those described for adult animals (Brown [1987] J. Comp. Neurol. 260:605–619). Unlike their mature counterparts, however, P2 efferent axons frequently branched to contact both types of auditory hair cells. Unexpectedly, between P4 and P6, both IHC and OHC efferent axons produced additional branches that crossed the tunnel of Corti to invade the OHC zone. By P8, all of these supernumerary connections were eliminated, yielding completely segregated efferent pathways to IHCs and OHCs. J. Comp. Neurol. 467:509–520, 2003. © 2003 Wiley‐Liss, Inc.