The fate map of the cephalic neural primordium at the presomitic to the 3-somite stage in the avian embryo

The results of those experiments that concerned the prosencephalic area have been the subject of two articles by Couly & Le Douarin (1985,1987), and are summarized in the fate map represented on Fig. 3.

The significant findings of this series of experiments are the following. Prior to and during neural tube formation, the most-rostral region of the neural plate is the anlage of the hypothalamus, which means that it corresponds to the diencephalon. Moreover, the hypothalamus territory is in continuity with that of the adenohypophysis lying in the anterior neural ridge (Figs 4, 5). Behind the hypothalamus lies the area from which the neurohypophysis arises. The hypothalamus and neurohypophysis complex is flanked by the neuroepithelium that yields the optic vesicles (Fig. 3).

Although rostral in the fully developed brain, the bilateral telencephalon territories are laterally located with respect to the ventral diencephalon (i.e. the hypothalamus and neurohypophysis) in the folding neural plate. The part of the diencephalon that will become the thalamus is located caudally to these structures (Fig. 3).

Our investigations on the neural plate itself have been limited so far to the area corresponding to the prosencephalon, the posterior limit of which is situated at the 0- to 3-somite stage at approximately 300–450 μm from the anterior neural ridge. Behind this level the neuroepithelium corresponds to the primordium of the mesencephalon.

The fate of the neural ridge located between the pituitary anlage and the beginning of the neural crest (characterized by its ability to dissociate into single cells that migrate and give rise to ectomesenchyme) was a surprise. This part of the neural ridge contains the precursor cells of large areas of superficial ectoderm corresponding to (i) the epithelium of the olfactory cavities including the sensory olfactory placodes and (ii) the vestibular epithelium of the nasal cavity, the epidermis of the nasofrontal area and the beak (including the egg tooth) (Fig. 6). Caudally are located the anlagen of the thalamus (in the plate) and epiphysis (laterally) (Figs 7, 8), while the corresponding neural fold yields the epidermis covering the forebrain (zone C of Fig. 2).

Following the observation that the placodal territory of the adenohypophysis is in contact with that of the hypothalamus, we have also found a continuity between the neural ridge containing the olfactory placodal territory and the basal region of the telencephalon which gives rise to the rhinencephalon. When the territory of a chick neural primordium, as indicated in Fig. 2, experiment IV, is replaced by its equivalent from quail not only are all the cells of the olfactory epithelium and the olfactory bulb of donor type, but so are the Schwann cells of the olfactory nerve (Fig. 9).

It is tempting to speculate that this early spatial juxtaposition of precursor cells which will later become parts of integrated functional units, such as the hypothalamohypophyseal complex or the peripheral and central olfactory structure, is not devoid of developmental significance. One can imagine that allthe cells constituting these complexes arise from a few progenitors, which, in the early neuroepithelium, become restricted in their developmental capacities to a family of related cell types. Further cell specifications subsequently emerge, probably when the tridimensional arrangement of the system is established, i.e. when its central (hypothalamus and olfactory centres) and peripheral (adenohypophysis and sensory epithelium) subunits separate. Later on, these subunits become linked again by vascular and nervous connections.

If such a speculation is valid, one can predict that there is a stage in development when the ‘plate’ and ‘ridge’ territories are not yet specific to yield, respectively, the central and peripheral subunits of the complex. If so, they should be spatially interchangeable without bringing about patterning alterations of the whole structure. This hypothesis will be tested in a subsequent study.

In experiments VI of Fig. 2, a double graft involving the adenohypophysis territory and that corresponding to region B of the fold with the adjacent neural plate (as in experiment IIIB) was performed on the same embryo (Fig. 10A).

The purpose of this particular study was to visualize the relative positions of these territories at different stages of development. As shown in Fig. 10B, the presence of two implants did not disturb the morphogenetic movements of the neural primordium. More-over, the infolding of the rostral region of the neural plate was clearly apparent when the localization of the grafted tissues was determined at sequential developmental stages (Fig. 10C–J).

Moreover, the laterorostral regions of the fold that will give rise to the olfactory tractus rapidly reach a ventral position, while the lateral regions of the neural plate become rostrally positioned as they move forward with the telencephalic anlage.

Fig. 11 projects onto the embryonic avian head (face and brain) the presumptive territories delimited at the folding neural plate stage. A parallel picture could be tentatively derived for human brain and facial structures. This approach has a certain interest, since it suggests explanations of the genesis of certain congenital human abnormalities such as those belonging to De Myer’s mediofacial syndrome (De Myer, 1967), in which malformations of the diencephalo-telencephalic regions (also called holoprosecenphalies) are associated with nasofronto-premaxillary hypoplasia. This is why it is interesting to demonstrate, as in this work, the close topographical relationships existing at early ontogenie stages between the prosencephalic neural primordium, the adenohypophysis, the olfactory organs and the facial ectoderm. Other examples include adenohypophyseal deficiencies, revealed by an insufficient production of growth hormone, associated with nasofrontal malformations (Couly, Rappaport, Brauner & Rault, 1982) and De Morsier’s syndrome (De Morsier, 1968), in which anosmia is associated with a functional genital deficiency of hypothalamo-hypophyseal origin. (For further discussion of human craniofacial abnormalities, see Posuillo, this volume).

This work was supported by the CNRS and grants from the Birth Defects March of Dimes Foundation, the Fondation pour la Recherche Médicale Française and the Ligue Française contre le Cancer.