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.

Visualization of two distinct classes of neurons by gad2 and zic1 promoter/enhancer elements in the dorsal hindbrain of developing zebrafish reveals neuronal connectivity related to the auditory and lateral line systems

“…We used the promoter/enhancer regions of gad2 and zic1 to visualize the morphologies of these neurons. Identifying their axonal targets provided support for their involvement in the auditory and lateral line systems and allowed comparison of these neurons with those classified in adult fish of other species (Knudsen, 1977;Echteler, 1984;Finger and Tong, 1984;McCormick, 1989;New et al, 1996;Yamamoto and Ito, 2005). We established a transgenic line, Tg(zic1:Gal4VP16/UAS:GFP), which expressed GFP under the control of the zic1 promoter/enhancer in the dorsal hindbrain including the rhombic lip.…”

“…Electrophysiological and retrograde tracer incorporation studies of the TS in various species of adult fish including goldfish, carp, and catfish have revealed a mediolateral segregation of the inputs of the auditory and lateral line sensory modalities (Fig. 5C, right;Knudsen, 1977;Echteler, 1984;Finger and Tong, 1984). These medial and lateral parts of the TS receive projections predominantly from distinct nuclei of the octaval and octavolateral nuclei in the dorsal hindbrain.…”

“…Among the five octaval nuclei that receive primary inputs from the inner ear, the dorsal region of the descending octaval nucleus (DON) and anterior octaval nucleus (AON) provide projections to the medial (auditory-related) part of the contralateral TS in goldfish, carp, and catfish ( Fig. 5C, right ;Echteler, 1984;Finger and Tong, 1984;Yamamoto and Ito, 2005). Of the two octavolateral nuclei that receive primary lateral line inputs, the medial octavolateral nucleus (MON) provides projections to the lateral (lateral line-related) part of the contralateral TS in goldfish and catfish ( Fig.…”

“…Similarly to the MON, there is also a projection to the contralateral DON (blue, open oval and dotted line; Yamamoto and Ito, 2005). In other fish species such as carp and catfish, the anterior octaval nucleus (AON) also provides auditory information to the medial region of the TS (Echteler, 1984;Yamamoto and Ito, 2005). In goldfish, this nucleus seems to provide few, if any, projections to the TS (McCormick and Hernandez, 1996;Yamamoto and Ito, 2005).…”

Functional investigation of neural circuits in larval zebrafish

“…Water flow information received by the lateral line sensory organ is passed from primary ganglia to hindbrain nuclei such as the medullary nucleus medialis, with substantial secondorder projections connecting to the contralateral torus semicircularis (Fame et al, 2006, McCormick & Hernandez, 1996. Contralateral projections from auditory midbrain nuclei have also been seen in the torus semicircularis (Echteler, 1984), although separated anatomically from lateral line areas (McCormick & Hernandez, 1996). Since large areas of the torus project to the deep layers of the ipsilateral optic tectum (Carr et al, 1981;Perez-Perez et al, 2003), it therefore has the potential to integrate the visual and non-visual sensory inputs from one half of the animal that converge on this brain region.…”