Afferent reorganisation within the superior olivary complex of the gerbil: development and induction by neonatal, unilateral cochlear removal.

Cochlear removal in young animals has been shown to produce a variety of degenerative and generative effects within the auditory brainstem. A primary target for axons of neurons in the anteroventral cochlear nucleus (AVCN) is the superior olivary complex (SOC). Following unilateral cochlear removal in neonatal gerbils, AVCN neurons on the side of the removal die, and axons deriving from the AVCN on the unlesioned side produce new endings that innervate previously inappropriate target zones within the ipsilateral medial nucleus of the trapezoid body, both medial superior olives, and the contralateral lateral superior olive. In this study, we have used the anterograde transport of DiI and HRP from the AVCN to relate the formation of these endings to the time course of normal development in the gerbil brainstem. We have also examined the effects of cochlear removal at different ages, and survival to various ages after the removal, to define the time course for these generative phenomena. The results show that, while the major projection pathways from the AVCN to the SOC are in place at the time of birth, further and subtle development of AVCN terminal arbors occurs during the first postnatal week. This overlaps with the time during which cochlear removal produces the formation of exuberant afferents to the SOC from the intact AVCN. The exuberant afferents form through axon sprouting rather than through a suppression of normal, developmental regression. They appear to innervate tonotopically appropriate target regions within the SOC. The formation of the novel afferents begins within 3 days of the removal and appears to be complete within a further 5-7 days. By postnatal day (P) 10, both the normal development of the AVCN to SOC projection and the potential for alteration of that projection by removal of the contralateral cochlea appear to be over. These results suggest that the potential for forming novel projections in the gerbil auditory brainstem is lost before the onset of functional hearing (at P12) and is, therefore, unlikely to result from changes in auditory experience.