Postnatal development of the afferent innervation of the mammalian cochlea

The adult mammalian cochlea receives dual afferent innervation: the inner hair cells (IHCs) are innervated exclusively by type I spiral ganglion neurons (SGNs), whereas the outer hair cells (OHCs) are innervated by type II SGNs. We have characterized the reorganization and morphology of this dual afferent innervation pattern as it is established in the developing rat cochlea. Before the cochlear afferent innervation reaches a mature configuration, there is an initial mismatch, where both populations of SGNs innervate both types of sensory hair cells: during the first postnatal week in the rat cochlea, type I SGN innervation is eliminated from the OHC and type II SGN innervation is eliminated from the IHC. This reorganization occurs during the first two postnatal weeks just before the onset of hearing. Our data reveal distinct phases in the development of the afferent innervation of the organ of Corti: neurite refinement, with a formation of the outer spiral bundles innervating outer hair cells; neurite retraction and synaptic pruning to eliminate type I SGN innervation of OHCs, while retaining their supply to IHCs. Such a reorganization also makes the cochlea a model system for studying CNS synapse development, plasticity and elimination. The present article summarizes the recent progress in our understanding of the afferent innervation of the cochlea. Biomedical Reviews 2012; 23: 37-52.