Pre- and postmetamorphic organization of the vestibular nuclear complex in the turbot examined by retrograde tracer substances

Abstract

During metamorphosis of flatfish larvae, eye migration leads to a 90 degrees misalignment of the visual and vestibular frames of reference. In order to maintain vestibular eye stabilization, the vestibulo-ocular (V-O) pathways have to be radically reorganized. Here, we have examined the vestibular projections in turbot larvae and juveniles by means of conventional neurohistological techniques using horseradish peroxidase and fluorescent dextranamines as tracers. We have found that the vestibular projections to the rostral eye motor nuclei consist of five densely clustered groups of neurons projecting to the rostral eye motor nuclei, some through the ipsilateral, others through the contralateral medial longitudinal fascicle (MLF). In addition, there are three groups of vestibulo-spinal neurons. The most prominent of these gives rise to the ipsilateral vestibulo-spinal tract. The other two project contralaterally, one descending in the MLF, the other more laterally in the anterior funiculus of the spinal cord. These subnuclei of the vestibular complex are easily identifiable in larvae before metamorphosis, as well as in juvenile turbots. The number of projection neurons in each of the subnuclei is approximately doubled over the period of metamorphosis. Applying different tracers to rostrally and caudally projecting pathways, we found no double-labeled neurons, indicating that the V-O and vestibulo-spinal groups are distinct entities. However, by applying the two tracers ipsi- and contralaterally in the terminal fields in the rostral eye motor nuclei after metamorphosis, we found many double-labeled neurons in all the V-O subgroups. In contrast, we found only a small fraction of double-labeled vestibular neurons when the same strategy was applied to larval preparations. We conclude that 1) the basic organization of the vestibular nuclei of the turbot is similar to that of other teleosts, in larvae as well as juveniles; 2) there is a substantial increase in projection neurons over the period of metamorphosis in all the subgroups of the vestibular nuclear complex; and 3) many more of the V-O neurons project bilaterally to the rostral eye motor nuclei in juvenile than in larval turbots.

Second-order projection from the posterior lateral line in the early zebrafish brain

“…The variable bilaterality of the adult connections could then be a later addition to a stereotyped, completely lateralized scaffold of projections. Interestingly, it has been reported that there is a large increase in bilaterality of the vestibulo-ocular projection between larval and juvenile turbot [31]. This increase has been correlated to eye migration during metamorphosis of the flatfish [31], but our observations of the early zebrafish brain suggest that increased bilaterality may be a general feature of post-embryonic development.…”

Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish

“…However, the gross anatomy and bilateral symmetry of the labyrinths in flatfish (Jacob, 1928), the distribution of the vestibular nuclear complex in the hindbrain of larval and juvenile turbot Scopthalmus maximus (Jansen and Enger, 1996), and the peripheral and central oculomotor apparatus (Graf and Baker, 1985) are bilaterally symmetrical and similar to those of other teleosts. Interestingly, all flatfish except for the most primitive (Platt, 1983) display nearly omni-directional hair-cell polarization of the inner ear's saccular and lagenar otoliths (Jorgensen, 1976;Platt, 1973).…”

The Black Sea kalkan and the turbot, its closest relative

“…Соответствующая мигрирующему глазу вестибулярная система (отолит и лабиринт) не смещаются, однако, во время изменений, связанных с метаморфозом, происходит существенное увеличение числа нейронов, ведущих от глазного нерва к вестибулярно-нервному комплексу головного мозга, и происходит их реогранизация (Jansen, Enger, 1996). Несмотря на то, что отолиты остаются на обеих сторонах головы, реорганизация нейронов означает, что у рыб изменяется невральное определение физического значения «верх».…”