Connections of the auditory midbrain in a teleost fish, Cyprinus carpio

Abstract

Central auditory pathways were traced in Japanese carp, Cyprinus carpio, using electrophysiological mapping and HRP tract-tracing methods. Multiunit recordings made from the carp torus semicircularis, the major midbrain area for processing octavolateralis information, revealed a mediolateral segregation of auditory and lateral line sensory modalities. Iontophoretic injections of HRP were made into the medial torus to trace afferent and efferent projections of the carp auditory midbrain. Following unilateral HRP injections into the medial torus, retrogradely labeled neurons were observed within six nuclei of the carp medulla. Two octaval nuclei, the anterior octavus nucleus and descending octavus nucleus, contained HRP-filled neurons. Labeled neurons were also observed within the ipsilateral superior olive, scattered among fibers of both lateral lemnisci, and bilaterally within the medullary reticular formation. In addition, bilateral retrograde cell labeling was found within a group of Purkinje-like cells located adjacent to the IVth ventricle, just rostral to the level of the VIIIth nerve. Few labeled neurons were found within the nucleus medialis, a principal target for lateral line afferents within the medulla. At midbrain levels, retrogradely labeled neurons were observed within the contralateral torus semicircularis and the ipsilateral optic tectum. Three forebrain nuclei project to the carp auditory midbrain. Within the diencephalon, descending projections originate from the anterior tuberal nucleus, bilaterally, and from the ipsilateral central posterior thalamic nucleus. The ipsilateral caudal telencephalon also projects to the carp auditory midbrain via large multipolar neurons within area dorsalis pars centralis. Anterograde labeling of fibers and terminals revealed efferent projections of the carp auditory midbrain to the following targets: the ipsilateral superior olive, the ipsilateral medullary reticular formation, the deep layers of the optic tectum, the contralateral torus semicircularis, the anterior tuberal nucleus, and the central posterior thalamic nucleus. These results, together with recent studies of lateral line pathways in teleosts (Finger, '80, '82a), demonstrate that central auditory and lateral line pathways are anatomically distinct in the carp, at least from medullary to diencephalic levels. Furthermore, there are striking similarities in the organization of the central auditory pathways of the carp and those of amphibians and land vertebrates.