Embryonic Development of the Inner Ear of the Catshark Scyliorhinus canicula.

Abstract

Introduction: The inner ear is a complex three-dimensional structure responsible for the detection of sound, balance, and acceleration. Detailed knowledge about the development of the inner ear of gnathostomes (jawed vertebrates) comes from studies in bony fishes and tetrapods, but comparable information about this process in chondrichthyans, the oldest gnathostome radiation, is lacking. This study describes for the first time the embryonic development of the inner ear and its innervation in the catshark Scyliorhinus canicula.

Methods: By using molecular markers of proliferating cells, migrating neuroblasts, and early differentiating neurons and genes expressed in placode-derived sensory neurons (NeuroD) and inner ear sensory patches (Sox2), we have established the spatiotemporal developmental pattern of the catshark inner ear also observed with micro-CT, and we have characterized developing sensory patches and described the establishment of the inner ear innervation.

Results: The development of the catshark inner ear takes place by invagination of the otic placode, as revealed by the expression of NeuroD at very early stages. From the very simple initial epithelial structure, the otic epithelium gradually grows and subdivides to form a complex three-dimensional labyrinth already recognizable at early stage 32. At this stage, the anterior semicircular canal and the horizontal semicircular canal of the catshark meet and fuse over the utricular concurrently with the beginning of the maturation of the inner ear sensory organs. We also show that the endolymphatic duct is formed as consequence of the invagination process; that the primary neurons of the statoacoustic ganglion originate by delamination from the otic epithelium, as in other vertebrates; that inner ear innervation starts when fibers immunoreactive to DCX link the otic cup to the brain at stage 20; and that the innervation pattern is completed at stage 32.

Conclusion: Present results provide cytological data on developmental changes that may be helpful for comparison with the development of this sensory system in other vertebrates and thus to gain knowledge on the evolution of the development of the inner ear.