The development of innervation patterns in the avian cochlea.

The sequence of developmental events leading to the innervation of the cochlea and the differentiation of its receptor cells has been studied in chick embryos with Golgi methods. We describe the morphogenesis of cochlear ganglion cell peripheral processes from their appearance in early embryos to the formation of their mature endings on hair cells in the basilar papilla (organ of Corti) of prehatching chicks. In the stage of peripheral fiber outgrowth, embryonic days 3-5, the fibers emerge from the ganglion cell bodies and grow, in a uniform fashion, toward the undifferentiated receptor epithelium of the otocyst. In the stage of the invasion of the otocyst by the peripheral fibers, embryonic days 6-7, some fibers enter the epithelium directly after reaching it, others enter after traveling some distance longitudinally beneath its basal lamina. The invading fibers appear to encounter resistance at the basal lamina, but, once within the epithelium, at embryonic days 8-9, they form a surfeit of branches in columnar zones oriented radially toward the surface. In early synaptogenesis (embryonic days 8-9) hair cells first become apparent. They differentiate from primitive epithelial cells. These cells withdraw their basal processes, which appear to accompany the growing fibers into the superficial epithelium. At embryonic days 11-13, the stage of mid-synaptogenesis, the fibers develop large, bulbous, preterminal and terminal swellings, which are located below the bases of the hair cells; the surplus branches atrophy or withdraw. Efferent axons are first seen in the epithelium at this time. In late synaptogenesis (embryonic days 14-17), the preterminal swellings disappear and the endings transform into mature foot-shapes at the bases of the hair cells. These morphological changes during the development of the peripheral endings are comparable to those of cochlear axons in nucleus magnocellularis (cochlear nucleus). During mid-synaptogenesis, when the ganglion cells develop swellings in the periphery, their central axons ramify extensively. Late in synaptogenesis, while the peripheral swellings disappear, there is a corresponding condensation of the central terminals to form the end-bulbs of Held. Thus, specific connections of the cochlear ganglion cells and their target cells in the ear and brain may result from two sequential developmental phases: (1) loosely organized and overabundant initial growth of branches from the fibers entering their target tissue; (2) reorganization of these fibers with the disappearance or resorption of the surplus branches during the transformation of their endings into mature synaptic arrangements.(ABSTRACT TRUNCATED AT 400 WORDS)