The mesencephalic neural plate of early-somite-stage mouse embryos differentiated underneath the renal capsule to form mostly neural tissues together with other tissues some of which were probably of neural crest cell origin. The capacity to form non-neural tissues such as skeletal tissues and melanocytes was lost at about the 5-somite stage. The lateral areas of the plate tended to form non-neural tissues more than the medial areas. The cephalic neural plate of presomite head-fold-stage embryos differentiated extensively to form both ectodermal and mesodermal tissues. However, upon completion of neurulation, the mesencephalic neuro-epithelium of forelimb-bud-stage embryos gave rise to neural tissues only. Therefore there is a progressive restriction in the histogenetic capacity of the mesencephalic neural plate during neurulation and this could be attributed to the cellular commitment for neural differentiation and the loss of the neural crest cells.

The differentiation of embryonic germ layers is characterized by a progressive restriction of the developmental capacity and the relocation of cells to their definitive position in the foetal body. The embryonic ectoderm or epiblast of mouse and rat egg cylinders is shown to be capable of extensive differentiation to generate tissues belonging to the three definitive germ layers both in an embryonic environment and in ectopic sites (Beddington, 1981,1983; Diwan & Stevens, 1976; Levak-Svajger & Svajger, 1974; Skreb & Svajger, 1975; Skreb, Svajger & Levak-Svajger, 1976). This extensive histogenetic potential of the embryonic ectoderm remains unchanged until the late-primitive-streak stage and there is also no detectable variation in the potency between the anterior (presumptive cephalic region) and the posterior regions of the embryonic ectoderm (Beddington, 1983; Skreb et al. 1976). A restriction in the histogenetic potential seems to have occurred in presomite head-fold-stage rat embryos and when the cephalic neural plate is grafted to ectopic sites, definitive endodermal (gut) tissues are absent in the teratomas (Svajger & Levak-Svajger, 1974). The neural plate of early-somite-stage rat embryos is still capable of producing mesodermal tissues in addition to the neural derivatives but the partially closed neural tube of 10- to 12-somite-stage embryos forms primarily neural tissues (Svajger, Levak-Svajger, Kostovic-Knezevic & Bradamante, 1981). Since the final composition of the graft is likely to be related to the initial developmental capacities of the tissue (Svajger et al. 1981), one possible interpretation of the change in histogenetic potential is that neural plate cells become progressively more committed to the differentiation of neural tissues during neurulation. However, the other possible factor contributing to this restriction of potential may be the loss of certain ‘mesodermal’ cell types from the neural plate at these stages. During the early stages of cephalic neurulation in the mouse, groups of cells leave the lateral edges of the neural plate and these cells, which show a positive staining reaction towards CPC-toluidine blue, are presumed to be the neural crest cells (Nichols, 1981). The neural crest cells first emigrate from the mesencephalic portion of the neural plate and are later seen leaving the rhombencephalic region. A similar pattern of neural crest cell migration has been described in the cranial region of rat embryos (Tan & Morriss-Kay, 1985). The common features are the emergence of the neural crest cells from the cranial neural plate well before the fusion of the neural folds and the early migration of the mesencephalic crest cells. In the present study, we have examined the histogenetic potential of the mesencephalic neural plate of early-somite-stage mouse embryos with a specific attention on the change in the capacity of forming mesodermal tissues such as cartilage, bone and pigment cells. These tissues are presumed to be of neural crest cell origin in the craniofacial region of the embryo (Bee & Thorogood, 1979; Jaenisch, 1985; Morriss & Thorogood, 1978; Noden, 1983; Rawles, 1947). For a comparison, the cephalic neural plate of pre-somite head-fold-stage embryos and the neuroepithelium in the mesencephalon of forelimb-bud-stage embryos were also studied.

Random bred ICR and inbred C57BL strains female mice were paired with syngeneic males and the presence of vaginal plugs was checked for occurrence of mating. Embryos were recovered from the pregnant mice at 8·0 and 9·5 days p.c. (the afternoon of the plug day = 0·5 dayp.c.). According to the somite number, the embryos were placed into five groups: presomite head-fold stage, 1- to 2-, 3- to 4-, 5-to 6- and 20- to 24-somite stages. At the presomite head-fold stage, the flattened portion of the ectoderm anterior to the flexure (Fig. 1) was isolated by dissecting with a pair of fine metallic needles. For the early-somite stages, the head region rostral to the preotic sulci was taken (Figs 2, 3). In the forelimb-bud-stage embryos, the brain region that is rostral to the otic capsule was used (Fig. 4). These embryonic parts were then treated with a mixture of 0·5 % trypsin (Sigma, Type II) and 2·5 % pancreatin (Sigma, Grade III) in calcium- and magnesium-free phosphate-buffered saline at room temperature for 10–15 min and the enzymic digestion was stopped by transferring the tissues to PB1 medium containing 20 % heat-inactivated foetal calf serum. The tissues were washed twice with fresh PB1 medium and were further dissected. The open neural plate of the embryos was bisected sagittally along the neural groove into two halves. At the presomite stage when the prospective brain areas were not yet discernible (Fig. 1), the entire half-plate was used, whereas in early-somite-stage embryos that showed a distinctive subdivision of brain regions, the mesencephalic neural plate was isolated. The underlying mesoderm was removed by dissecting with electrolytically polished alloy needles. The surface ectoderm was removed by cutting along the edge of the plate and the cut was usually made more on the neural plate side (Figs 2, 3). The half-neural plate was then bisected into medial and lateral portions (Figs 2, 3). The mesencephalon of the forelimb-bud-stage embryos was divided into dorsal and ventral portions (Fig. 4) which corresponded to the original lateral and medial parts of the open neural plate.

Fig. 1.

The sagittal view of a presomite-stage embryo. The entire portion of the neural plate rostral to the dotted line was isolated for enzymic treatment. Bar, 100 μm.

Fig. 1.

The sagittal view of a presomite-stage embryo. The entire portion of the neural plate rostral to the dotted line was isolated for enzymic treatment. Bar, 100 μm.

Fig. 2.

The dorsal view of a 2-somite-stage embryo. The mesencephalic neural plate was divided into medial portion (M) and lateral portion (L). Bar, 100μm.

Fig. 2.

The dorsal view of a 2-somite-stage embryo. The mesencephalic neural plate was divided into medial portion (M) and lateral portion (L). Bar, 100μm.

Fig. 3.

The dorsolateral view of a 4-somite-stage embryo, showing the subdivision of the mesencephalic neural plate into medial portion (Af) on the right side and lateral portion (L) on the left half of the plate. Bar, 100 μm.

Fig. 3.

The dorsolateral view of a 4-somite-stage embryo, showing the subdivision of the mesencephalic neural plate into medial portion (Af) on the right side and lateral portion (L) on the left half of the plate. Bar, 100 μm.

Fig. 4.

The ventricular aspect of the brain of a 20-somite-stage embryo, showing the two parts of the mesencephalon that were used for grafting. V, ventral portion; D, dorsal portion. Bar, 100 μm.

Fig. 4.

The ventricular aspect of the brain of a 20-somite-stage embryo, showing the two parts of the mesencephalon that were used for grafting. V, ventral portion; D, dorsal portion. Bar, 100 μm.

The tissue fragments were transferred by means of fine glass micropipettes underneath the renal capsule of syngeneic male mice under light Nembutal (Sigma) anaesthesia. For each recipient, fragments of neural plate were transferred to one kidney capsule and fragments of the mesoderm and surface ectoderm were transferred to the other capsule. The mice were killed two weeks after the transfer and the grafts were fixed in Sanfelice fluid and processed for histology. Paraffin wax sections of 7 gm thickness were stained with haematoxylin and eosin. Selected sections were stained with Bodian’s method for nerve fibres and nerve endings (Luna, 1968). Other grafts were fixed in half-strength Karnovsky fixative followed by 1 % osmium tetroxide and embedded in Spurr resin. Thick (1–2 μm) sections were stained with 1 % toluidine blue for light microscopy. Some of the original preparations of neural plate were fixed in half-strength Karnovsky fixative and processed for scanning electron microscopy using a JEOL JSM-35CF electron microscope, while others were fixed in Sanfelice fluid and processed for routine histology.

Fourteen dissected preparations of neural plates were examined microscopically. The basement membrane that normally associated with neuroepithelium was lost and large intercellular clefts were seen in the loosened epithelium (Fig. 5). No adhering mesodermal cells and surface ectoderm were seen in these preparations. For those preparations that were used for grafting experiments, a preliminary histological examination was not possible but great care was taken to scrutinize the preparations under the dissecting microscope for contaminating tissues prior to transfer. Between 50 to 75 % of the neural plate fragments grew into a recognizable mass under the renal capsule after two weeks, but grafts of mesoderm and surface ectoderm developed poorly and few (10–30 %) of them formed recognizable tissue masses. Apart from the presence of pigment cells in the grafts derived from C57BL embryos, there was no other significant difference in the tissue composition between the two strains used in this study and therefore the results were pooled. Like the observations made in other studies on the ectoderm of presomite head-fold-stage rat embryos, the mouse neural plate was capable to differentiate into a large variety of ectodermal and mesodermal tissues (Table 1). In the grafts of neural plate of other stages, the most prevalent tissues were those normally found in the developing nervous system (Table 1). Groups of basophilic cells were organized into a thick pseudostratified epithelium which lined the wall of many cystic and tubular structures. A peripheral layer of cellular processes was commonly seen on the basal aspect of the epithelium and this tissue arrangement is similar to that of the ventricular and marginal layers observed in the neuro-epithelium of the early neural tube. In other areas, large patches of mature neuronal cells were found. Typically, these cells had a large soma and they sprouted out neuronal processes (Fig. 6). The cell bodies were arranged in clusters surrounded by interwoven meshworks of neuronal processes and this tissue resembled the grey matter of the central nervous system. Other neural tissues such as choroid plexuses and ependyma that lined the luminal surface of cystic structures were also found. There was no significant difference in either the incidence or the relative amount of neural tissues formed by the cells in the lateral portion of the neural plate in comparison to those in the medial portion of the plate (Table 1).

Table 1.

The tissue composition of grafts derived from the mesencephalic neural plate and mesencephalon

The tissue composition of grafts derived from the mesencephalic neural plate and mesencephalon
The tissue composition of grafts derived from the mesencephalic neural plate and mesencephalon
Fig. 5.

A scanning electron micrograph showing the basal aspect of the neuro-epithelium of a 4-somite embryo after the enzymic treatment and dissection. The basement membrane has been removed and no adhering mesodermal cells are seen. Under light microscope (inset, H & E staining), the neuroepithelium of another embryo with 4 somites is free of any surface ectodermal and mesodermal cells, bs, basal surface. Bar, 50 μm.

Fig. 5.

A scanning electron micrograph showing the basal aspect of the neuro-epithelium of a 4-somite embryo after the enzymic treatment and dissection. The basement membrane has been removed and no adhering mesodermal cells are seen. Under light microscope (inset, H & E staining), the neuroepithelium of another embryo with 4 somites is free of any surface ectodermal and mesodermal cells, bs, basal surface. Bar, 50 μm.

Fig. 6.

Differentiated neural tissue that resembles grey matter of the central nervous system and contains silver impregnated processes (arrowhead). Bar, 100μm. Silver impregnation by Bodian method.

Fig. 6.

Differentiated neural tissue that resembles grey matter of the central nervous system and contains silver impregnated processes (arrowhead). Bar, 100μm. Silver impregnation by Bodian method.

While only neural tissues were seen in grafts of mesencephalon of 5- to 6-somite-stage and forelimb-bud-stage embryos, the neural plate of younger embryos also gave rise to non-neural tissues. Epidermal tissues such as keratinized epithelia, hairs and sebaceous glands (Fig. 7) were seen in 15–42 % of grafts of presomite head-fold-stage neural plate (Table 1). The tissues were organized in the proper topographical relationship seen in adult skin, but the dermal component was poorly developed. Initially, the skin-forming capacity was found in both portions of the neural plate but later it was limited to the lateral portion and was eventually lost by the forelimb-bud stage. Mesodermal derivatives such as bone, cartilage and adipose tissue (Fig. 8) were also formed by the neural plate cells of early-somite-stage embryos. But this mesodermal potency was progressively lost from both the medial and the lateral portion of the neural plate and was completely absent from the neural plate cells by the 5-somite stage (Table 1). Pigment cells (Fig. 9) were present in the neural plate graft of C57BL embryos having one to four pairs of somites (Table 1).

Fig. 7.

A cystic structure lined with keratinized stratified epithelium (k), hair follicles (f) and sebaceous gland (arrowhead). Bar, 100μm. H & E staining.

Fig. 7.

A cystic structure lined with keratinized stratified epithelium (k), hair follicles (f) and sebaceous gland (arrowhead). Bar, 100μm. H & E staining.

Fig. 8.

The ossification of the cartilage (c) to form bones (b) in the graft derived from the lateral portion of the neural plate of a presomite head-fold-stage embryo. a, adipose tissue; m, striated muscle. Bar, 100 μm. H & E staining.

Fig. 8.

The ossification of the cartilage (c) to form bones (b) in the graft derived from the lateral portion of the neural plate of a presomite head-fold-stage embryo. a, adipose tissue; m, striated muscle. Bar, 100 μm. H & E staining.

Fig. 9.

A cluster of pigment cells (arrowhead) found in the graft of the lateral portion of the neural plate of an early-somite-stage C57BL embryo. Bar, 100 μm. H & E staining.

Fig. 9.

A cluster of pigment cells (arrowhead) found in the graft of the lateral portion of the neural plate of an early-somite-stage C57BL embryo. Bar, 100 μm. H & E staining.

The grafts that derived from the early-somite-stage neural plate were re-examined with respect to the change in the potency to form presumed neural crest cell derivatives such as skeletal tissues and pigment cells (Table 2). It is clear from this analysis that such tissues were formed only in grafts of neural plate of 1- to 4-somite-stage embryos. Furthermore, the lateral portion tended to form presumed neural crest derivatives more frequently than the medial portion (Table 2). The presumed neural crest derivatives were also often formed in the absence of other mesodermal (such as adipose and muscles) or epidermal derivatives (Table 2). Among the 78 grafts involving the lateral areas of the neural plate of early-somite-stage embryos, epidermal tissues were found in 10 grafts (Table 1). None of the medial portions formed any epidermal tissues. The differentiation of epidermal derivatives in the former case was likely due to the contamination by surface ectoderm in the original grafts. Technically, this is unavoidable because, in early embryos, the morphological landmarks might not faithfully delineate the neural and epidermal areas of the ectoderm. When the underlying cranial mesenchyme and the adjacent surface ectoderm were grafted, mesodermal derivatives such as cartilage, adipose and connective tissues were commonly formed. Skin derivatives were only formed in grafts originating from embryos having five or more somites (Table 3). No neural tissues were ever formed.

Table 2.

The association of presumed neural crest cell derivatives with other epidermal and mesodermal structures in grafts of early-somite-stage neural plate

The association of presumed neural crest cell derivatives with other epidermal and mesodermal structures in grafts of early-somite-stage neural plate
The association of presumed neural crest cell derivatives with other epidermal and mesodermal structures in grafts of early-somite-stage neural plate
Table 3.

The tissue composition of grafts derived from the cranial mesoderm and surface ectoderm

The tissue composition of grafts derived from the cranial mesoderm and surface ectoderm
The tissue composition of grafts derived from the cranial mesoderm and surface ectoderm

Embryonic ectodermal cells taken from the anterior region of the mouse egg cylinder have been shown to colonize the surface ectoderm and neurectoderm in the craniofacial region of chimaeric embryos (Beddington, 1981). The analysis of cellular proliferation in tw18/tw18 mutant embryos similarly suggests that cells in anterior embryonic ectoderm are topographically predisposed to form cephalic neurectoderm (Snow & Bennett, 1978). However, when these cells are allowed to differentiate in an ectopic environment, they express a histogenetic potential far exceeding their normal ectodermal fate and form both mesodermal and endodermal derivatives (Beddington, 1983).

Our observation on the extensive range of tissue differentiation seen with the presomite head-fold-stage neural plate agrees with other studies in rat embryos (Levak-Svajger & Svajger, 1974). A restriction in the capacity to form endodermal tissues was already apparent in the neural plate at this stage. In the course of morphogenesis, the neural plate in early-somite-stage embryos lost the capacity to form mesodermal tissues, particularly those presumed to be neural crest cell derivatives. From about 5-somite stage onwards, the neural plate differentiated exclusively into neural tissues. Our results therefore complement those observations made on the neural plate of rat embryos at similar stages of development (Levak-Svajger & Svajger, 1974; Svajger & Levak-Svajger, 1974; Svajger et al. 1981), where a progressively diminishing capacity to form mesenchymal tissues has been noted. This progressive restriction in histogenetic potential could be attributed to the commitment of neural plate ectoderm towards the neurogenic pathway and this appears to occur concomitantly with morphogenesis of the plate. When the mesencephalic neural plate was transplanted to the renal capsule, the graft differentiated predominantly into neural tissues. This is in line with other studies which demonstrate that neural tissues such as neurones, ganglia and glia are commonly formed during the in vitro culture of the neural plate (Cohen, 1977; Ito & Takeuchi, 1984; Kahn & Sieber-Blum, 1983; Norr, 1973; Sieber-Blum & Cohen, 1980; Skreb & Crnek, 1977; Skreb, Scuknac-Spoljar & Crnek, 1976; Skreb & Svajger, 1975) or when the neural plate is grafted to renal capsules or the anterior ocular chamber (Levak-Svajger & Svajger, 1974; Lumsden, 1984; Skreb et al. 1976).

The changes in histogenetic potential may also be related to the ability of the neural plate to undergo the atypical morphogenetic process of ‘neoformation’ of mesenchyme in ectopic environment (Svajger et al. 1981). Early differentiation of ectodermal fragments of early-somite-stage rat embryos proceeds with a sloughing of cells from the edges of the graft in a manner that is reminiscent of neural crest cell migration (Svajger et al. 1981). It seems likely that the gradual loss of the ability to form skeletal tissues and pigment cells by grafts of the mouse mesencephalic neural plate was partly due to the diminishing population of precursor neural crest cells in plates of advancing developmental stages. Circumstantial evidence for this possibility was provided by the ability of the lateral portion of the early-somite-stage neural plate to generate mesodermal tissues rather than the medial portion. Furthermore, the temporal sequence of changes in the potency was also coincidental to the emigration of neural crest cells from the mesencephalic neural plate (Nichols, 1981; Tan & Morriss-Kay, 1985). In a recent study, cartilages and tooth primordia were formed when the lateral portion of the cranial neural plate of early-somite-stage rat embryos was grafted together with the mandibular arch epithelium to ectopic sites (Lumsden, 1984). This result has been taken to indicate that those neural crest cells forming the teeth and the jaw bones are found in the cranial neural plate. Explants of neural plate from chick embryos of early-somite stage form cartilage and melanocytes when cultured in vitro or on chorioallantoic membrane (Bee & Thorogood, 1979; Hall & Tremaine, 1979; Newsome, 1976). Extensive skeletal differentiation occurs when the lateral areas of the neural plate of 8-somite-stage chick embryos are recombined with epithelia from pigmented retina and maxillary process (Bee & Thorogood, 1979). However, the skeletogenic capacity is lost from explants taken from embryos at the stage when neural crest cells have left the plate (Hall & Tremaine, 1979). Our interpretation on the mesodermal-tissue-forming capacity of the neural plate therefore conforms with the morphological observations on the origins and emigration of neural crest cells at the early stages of neurulation. The apparently greater ability to form mesodermal derivatives endowed in the lateral portion of the plate may suggest that the precursors of neural crest cells are strategically located to facilitate their subsequent migration from the plate.

The authors are grateful to Professor D. J. Riches for his useful comment on the manuscript.

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