Abstract
The olfactory system represents an excellent model for studying different aspects of the development of the nervous system ranging from neurogenesis to mechanisms of axon growth and guidance. Important findings in this field come from comparative studies. We have analyzed key events in the development of the olfactory system of the shark Scyliorhinus canicula by combining immunohistochemical and tract-tracing methods. We describe for the first time in a cartilaginous fish an early population of pioneer HuC/D-immunoreactive (ir) neurons that seemed to delaminate from the olfactory pit epithelium and migrate toward the telencephalon before the olfactory nerve was identifiable. A distinct, transient cell population, namely the migratory mass, courses later on in apposition to the developing olfactory nerve. It contains olfactory ensheathing glial (GFAP-ir) cells and HuC/D-ir neurons, some of which course toward an extrabulbar region. We also demonstrate that Pax6-ir cells coursing along the developing olfactory pathways in S. canicula are young migrating (HuC/D and DCX-ir) neurons of the migratory mass that do not form part of the terminal nerve pathway. Evidences that these Pax6 neurons originate in the olfactory epithelium are also reported. As Pax6 neurons in the olfactory epithelium show characteristics of olfactory receptor neurons, and migrating Pax6-ir neurons formed transient corridors along the course of olfactory axons at the entrance of the olfactory bulb, we propose that these neurons could play a role as guideposts for axons of olfactory receptor neurons growing toward the olfactory bulb.
Highlights
The olfactory system is an excellent model for studying several developmental aspects of the nervous system, including cell migration, tract formation and guidance as well as adult neurogenesis
We have identified the main key events that take place during the development of the olfactory system in the lesser spotted dogfish (S. canicula) and we have framed them into the context of the three developmental periods that were established on the basis of tract-tracing experiments and the expression of various immunohistochemical markers
This study describes for the first time in cartilaginous fish the development of the olfactory nerve and characterizes the nature of some cells observed in the developing olfactory epithelium and associated with the olfactory nerve, the intriguing Pax6-expressing population that was recently observed along the olfactory pathway during the development of S. canicula (FerreiroGalve et al 2012a)
Summary
The olfactory system is an excellent model for studying several developmental aspects of the nervous system, including cell migration, tract formation and guidance as well as adult neurogenesis. The placodal origin of these populations has been traditionally accepted, it is still a matter of discussion and the neural crest is considered as an alternative source for some of them (Whitlock 2004; Barraud et al 2010; Forni et al 2011; Katoh et al 2011) Regardless of their origin, several cell populations have been described traveling along this pathway closely related to developing olfactory axons which seemed to serve as tracks for their migration (Mendoza et al 1982; Farbman and Squinto 1985; Valverde et al 1992, 1993; Pellier and Astic 1994; Pellier et al 1994; De Carlos et al 1996; Whitlock and Westerfield 1998; Fornaro et al 2001, 2003; Balmer and LaMantia 2005; Maier and Gunhaga 2009; Miller et al 2010; Blanchart et al 2011). This is the case of a population apparently implicated in neocortical development (De Carlos et al 1996), and the population of LHRH (luteinizing hormone-releasing hormone)/GnRH (gonadotropin-releasing hormone) expressing cells that are part of the terminal nerve system (Wray et al 1989; Whitlock 2004)
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