DEVELOPMENT OF ECTOPIC PROJECTIONS FROM THE VENTRAL COCHLEAR NUCLEUS TO THE SUPERIOR OLIVARY COMPLEX-INDUCED BY NEONATAL ABLATION OF THE CONTRALATERAL COCHLEA

The ability of an animal to localize a sound in space requires the pre cise innervation of the superior olivary complex by the ventral cochle ar nuclei on each side of the lower brainstem. This precise pattern of innervation could require an immutable recognition of appropriate tar gets by afferent processes arising from these nuclei. This possibility was investigated by destroying one cochlea of gerbil pups (Meriones u nguiculatus) on the second postnatal day and assessing the projections from the ventral cochlear nucleus (VCN) on the unablated side to the superior olivary complex during the subsequent 2 weeks and after the a nimals had reached maturity. A crystal of -dioctadecyl-3,3,3',3'-tetra methylindocarbocyanine perchlorate (DiI) was inserted into VCN on the unablated side in animals ranging in age from 3 to 14 days. To assess the permanence of any altered pattern of innervation, horseradish pero xidase was injected into VCN on the unablated side in adult, neonatall y ablated animals. Finally, electrophysiological responses to acoustic stimuli delivered to the ear on the unablated side were recorded in t he superior olivary complex of adult animals to assess whether altered innervation patterns were functional. Normative data were derived fro m our accompanying study of the development of VCN projections to the superior olivary complex in normal gerbils (Kil et al., this issue). W hereas VCN normally projects to the lateral aspect of the ipsilateral medial superior olive and to the medial aspect of the contralateral me dial superior olive in control animals, in experimental animals VCN on the unablated side projects to both sides of these nuclei. Whereas in the gerbil, VCN normally projects only to the hilar area and to the v entrolateral limb of the contralateral lateral superior olive, in expe rimental animals VCN on the unablated side projects throughout this nu cleus. This induced projection is specific in that the efferents to ea ch limb of the contralateral nucleus are linked to the normal projecti on to the homotopic region of the ipsilateral nucleus. Whereas VCN inn ervates the contralateral medial nucleus of the trapezoid body in cont rol animals, in experimental animals VCN on the unablated side provide s calyces of Held in the ipsilateral nucleus as well. The induced proj ections to these three major subnuclei of the superior olivary complex first appear within 24 hours of the cochlear ablation and continue to develop over at least the subsequent 11 days. Thus, prior to the day when the cochlea becomes functional, VCN has established specific ecto pic projections to loci normally innervated by VCN on the ablated side . All induced ectopic projections observed in neonatal animals were al so present in neonatally ablated adult animals, indicating their perma nence. As in the case of the normal projections from VCN to these subn uclei, all labeled synapses contained round vesicles and formed asymme tric synaptic junctional complexes with dendrites and somata in these target nuclei. Electrophysiological responses of single units in the i psilateral medial nucleus of the trapezoid body demonstrated that the induced calyces of Held in this structure are quite functional in adul t animals. (C) 1995 Wiley-Liss, Inc.