Development of the nervus terminalis: Origin and migration

Abstract

The origin of the nervus terminalis is one of the least well understood developmental events involved in generating the cranial ganglia of the forebrain in vertebrate animals. This cranial nerve forms at the formidable interface of the anteriormost limits of migrating cranial neural crest cells, the terminal end of the neural tube and the differentiating olfactory and adenohypophyseal placodes. The complex cellular interactions that give rise to the various structures associated with the sensory placode (olfactory) and endocrine placode (adenohypophysis) surround and engulf this enigmatic cranial nerve. The tortured history of nervus terminalis development (see von Bartheld, this issue, pages 13-24) reflects the lack of consensus on the origin (or origins), as well as the experimental difficulties in uncovering the origin, of the nervus terminalis. Recent technical advances have allowed us to make headway in understanding the origin(s) of this nerve. The emergence of the externally fertilized zebrafish embryo as a model system for developmental biology and genetics has shed new light on this century-old problem. Coupled with new developmental models are techniques that allow us to trace lineage, visualize gene expression, and genetically ablate cells, adding to our experimental tools with which to follow up on studies provided by our scientific predecessors. Through these techniques, a picture is emerging in which the origin of at least a subset of the nervus terminalis cells lies in the cranial neural crest. In this review, the data surrounding this finding will be discussed in light of recent findings on neural crest and placode origins.

Developing a sense of scents: Plasticity in olfactory placode formation

“…Consistent with this hypothesis, we have found that in zebrafish GnRH3 cells of the terminal nerve and GnRH2 cells of the midbrain (Fig. 2B,C) have their origin in the cranial neural crest [53,57,60] whereas the GnRH cells of the hypothalamus arise from the region of the adenohypophyseal placode [54,56,57,60] (Fig. 2D).…”

“…The use of more refined techniques for labeling and following cells in the early embryo, suggests the olfactory placodes arise from the neural ridge or neural plate as opposed to the non-neural ectoderm. We completed a single cell fate map of the olfactory placode domains at 4-5 somitestage zebrafish embryo (~11-12 hours post-fertilization at 28.5C) and demonstrated that the olfactory placode develops from a field of cells within the edge of the anterior neural plate which is initially continuous with the pre-migratory cranial neural crest and the adenohypophyseal placode [59], for reviews see [51][52][53]. Our model has also been supported by work in the chick studying the formation of a similarly patterned sensory placode, the otic placode.…”

Terminal nerve in the mouse‐eared bat (Myotis myotis): Ontogenetic aspects

“…In Myotis myotis, this presumably takes place at about D27 and a CRL of 4 mm. In recent studies, Whitlock et al (2003Whitlock et al ( , 2004 (2004) investigated over 300 serially sectioned human embryos and clearly demonstrated nasal crest material in several Š těrba stage 4 specimens directly underneath the basement membrane of the olfactory placode. This material originates from the nasal plate at the neurosomatic junction, as does the neural crest, and contains LHRH precursor cells (Verney et al, 2002).…”

“…Mü ller and O'Rahilly (2004) observed that crest cells began to adhere to each other and to form cords, which a little later began to migrate toward the region of the olfactory tubercle. In this context, one can assume that the majority of TN neurons, particularly the endocrine cell populations of the TN in humans, originate from crest material of the neurosomatic junction, which is a major source of endocrine cells in general (von Bartheld and Baker, 2004;Whitlock, 2004). In contrast to this, a most recent investigation of the Indian major carp (Cirrhinus mrigala) by Biju et al (2005) very clearly demonstrated GNRH peptide only in surprisingly well-differentiated bipolar epithelial cells of the olfactory placode and not in the neural crest on D1 [probably corresponding to stage 3 of Š těrba (1990)].…”

“…As mentioned above, these cells originate from the rostralmost edge of the neural crest (Whitlock, 2004). In early embryonal stages they associate with the material of the olfactory placode before it is morphologically distinct, and they migrate along TN fibers into the hypothalamus during early fetal development.…”