|
|
| (28 intermediate revisions by the same user not shown) |
| Line 1: |
Line 1: |
| {{Header}}
| | #REDIRECT [[Paper - Observations on the neural crest of a ten-somite human embryo (1939)]] |
| Baxter JS. and Boyd JD. Observations on The Neural Crest of a Ten-Somite Human Embryo (1939) J Anat. 73:318–326. PMID 17104759
| |
| | |
| [[Historic Embryology Papers]] | |
| {{Historic Disclaimer}}
| |
| ==Observations on The Neural Crest of a Ten-Somite Human Embryo==
| |
| | |
| By J. S. Baxter And J. D. Boyd
| |
| | |
| | |
| In the course of a study of a ten-somite human embryo in a good state of preservation we observed an unusual arrangement of those neural crest cells which form the acoustico-facial primordium. This led us to investigate the arrangement and distribution of the whole of the neural crest, and, as there are few detailed accounts of the neural crest in human somite embryos, we present our results as a separate contribution.
| |
| | |
| | |
| The embryo was obtained by laparotomy from a case of tubal gestation. The clinical history suggests that, if ovulation occurred about the mid-point of the menstrual cycle, the conceptional age of the embryo is approximately 28 days.<ref>We are indebted to Dr H. T. Laycock of Addenbrooke’s Hospital, Cambridge, for the opportunity of studying this specimen. Details of the clinical history of the patient from whom the embryo was obtained will be given in a subsequent contribution.</ref> When received in the laboratory the intact chorionic vesicle had been fixed in formalin (of unknown strength) for several days. In its longest axis the vesicle measured 14 mm., in its shortest 12 mm. Having been dissected from the main part of the chorion, the embryo, with the connecting stalk and the adjacent chorionic wall, was stained in bulk with alum cochineal, dehydrated by the drop method, imbedded in paraffin and cut transversely at Sp. into a complete series of sections. The sections were then stained on the slide with orange G.
| |
| | |
| | |
| A number of reconstructions of this embryo have been made. Those of interest for the purpose of this description are a wax-plate model of the external form of the embryo, anda millboard-wax model (according to the method of Green, 1937), of the cranial portion of the nervous system and its associated neural crest primordia.
| |
| | |
| | |
| The sectioned embryo, and the reconstructions, show that the neural folds have united from a point somewhat cranial to the otic placodes to the level of the seventh somite. Here the closure of the neural tube is discontinuous, and the caudal extremity of the neural plate is a thickened, flattened area of columnar cells continuous laterally with the somatic ectoderm. The appearance of this caudal portion of the nervous system is very similar to that presented by other human embryos at a comparable stage of development. The cranial extremities of the neural folds, however, are not widely separated and thus contrast with the condition usually found at this stage. The anterior neuropore is, then, a narrow, deep cleft (Pl. I, figs. 1, 2); and, in our opinion, it is quite possible that this appearance may be ascribed to undue shrinkage of the embryo during fixation. There is a certain degree of asymmetry in the state of development of the two sides of the neural primordium, the right side of the central nervous system being more advanced than the left. This asymmetry has been described in a number of human somite embryos (cp. Bartelmez & Evans, 1926).
| |
| | |
| | |
| There are three regions in our embryo in which neural crest cells are found in relation with the developing nervous system (see Text-fig. 1). The most anterior of these regions is at the level where the cranial flexure is most pronounced, and here, on either side of the open neural folds, there is a discrete mass of neural crest cells. The right one is better developed and will be described first.
| |
| | |
| | |
| | |
| | |
| Text-fig. 1. Geometric projection of the right profile view of a reconstruction of the cephalic portion of the nervous system. The various primordia of the neural crest are shown. The hatched line indicates the margin of the left neural fold. The arrow shows the cranial limit of the first somite.
| |
| | |
| | |
| It is, obviously, the crista neumlis rostralis of Bartelmez & Evans, or the ''craniale Kopfganglienleiste'' of Veit (1919). Although, caudally, there is a small
| |
| isolated portion of this neural crest material, we do not think that a distinct
| |
| subdivision into a “pars optica” and a “pars trigeminalis” is present. The
| |
| neural crest cells do, however, extend forwards to the dorsal edge of the optic sulcus and, possibly, the aggregation of cells should be regarded as a compound of a crista neuralis rostmlis (associated with the trigeminal area and the
| |
| Gasserian ganglion) and a crista neuralis prosencephali (from the dorsal edge of
| |
| the optic primordium). If this interpretation is correct then the term primordium opto-cristale of Bartelmez & Evans might be used for the anterior part of
| |
| this portion of the neural crest. We incline to the opinion, however, which has
| |
| been expressed by Adelmann (1925), that the crista neuralis prosencephali
| |
| should be regarded with extreme caution. Adelmann was unable to find any
| |
| trace of such a portion of the neural crest in a large number of rat embryos of
| |
| the somite stage; he states (p. 52), “ absence of such a neural crest from at least
| |
| a major portion of the forebrain seems to be a general condition”. Schulte &
| |
| Tilney (1915) were also unable to find W neural crest cells arising from the
| |
| prosencephalon during the early development of the central nervous system of
| |
| the cat. Indeed, these investigators were so impressed by the absence of neural
| |
| crest cells in the region of the forebrain that they suggested the retention of
| |
| these cells in the wall of the neural tube to form an elementiadditional to the
| |
| alar and basal laminae. We are unable to find any evidence for such a retention
| |
| of alleged neural crest cells in the anterior portions of the neural plates, but we
| |
| have the impression that the cephalic portion of our crista neuralis rostralis is
| |
| not of prosencephalic origin but is an extension forwards of the main part of
| |
| the mass which is related primarily to the anterior part of the rhombencephalon
| |
| and the mesencephalon. It is, probably, that portion of the crest which will be
| |
| concerned with the development of the ophthalmic division of the trigeminal
| |
| nerve.
| |
| | |
| | |
| The cells constituting this right anterior neural crest mass do not show
| |
| continuity with the neural plate or the somatic ectoderm. In this character
| |
| (which may be due to the same shrinkage process which has caused the approximation of the two halves of the open neural plate in this region) they
| |
| differ from the corresponding cells in the ten-somite embryo described by
| |
| Corner (1929), for he both described (p. 90), and figured, cells passing to this
| |
| mass from “the inner surface of the neural epithelium and the neuro-somatic
| |
| junction” of the entire midbrain region and the rostral part of the rhombencephalon. We have been unable to find a trigeminal placode in our embryo so the
| |
| question of a contribution from this source to the neural crest does not arise.
| |
| | |
| | |
| There are distinct differences between the neural crest cells and the
| |
| surrounding mesenchyme, but it is impossible to be definite in the identification
| |
| of the cells in the transition zone between the two groups. The bulk cochineal
| |
| stain is, as in Corner’s specimen,‘ not well adapted to show cytoplasmic
| |
| differences. We feel quite certain, however, that the neural crest material
| |
| extends towards, and merges with, the mesenchyme of the first branchial arch,
| |
| particularly with that portion of the arch which will later form the maxillary
| |
| process. The existence of this mingling of neural crest cells with the surrounding mesenchyme does not, of course, constitute evidence for the derivation of mesenchyme from neural crest cells. On this point our material does not allow of any definite statement and, indeed, we doubt the value of any contributions to this problem which are based on description alone, particularly on the study of a single embryo or a very small series of embryos.
| |
| | |
| | |
| On the left side of the presumptive midbrain region there is a mass of
| |
| neural crest cells which in position and relations is similar to the right crista
| |
| neuralis rostralis (Pl. I, figs. 1, 2). It is, however, very much smaller than the
| |
| corresponding mass of the right side. We correlate this difference in size with
| |
| the relatively retarded development of the left side of the central nervous
| |
| system in the head end of this embryo. As on the right side, there is no
| |
| evidence of the migration of neural crest cells from the edge of the neural plate.
| |
| The smaller size of this left crista neuralis rostralis probably accounts for its
| |
| better delimitation and the absence of an appearance, on this side of the
| |
| embryo, of an extension of the crest material into the branchial mesenchyme.
| |
| | |
| | |
| Caudal to these two masses of neural crest cells there is a region of the
| |
| developing nervous system which has no such cells related to it. A short
| |
| distance behind the anterior limit of fusion of the neural folds there is found
| |
| the next aggregation of neural crest cells (Pl. I, figs. 1, 2). This portion consists
| |
| of a large mass of cells situated dorsal to the neural tube and intimately connected with it (see Pl. I, fig. 3 and PI. II, fig. 7). The cephalic part of this mass
| |
| forms a continuum across the mid-line of the embryo with no trace of subdivision into right and left halves; but, when this mass of neural crest cells is
| |
| traced caudally it separates into two, bilaterally symmetrical, horn-like processes which come to lie on either side of the dorsal portion of the neural tube
| |
| (Pl. II, fig. 5). This group is the primordium acaustico-facialis (Bartelmez &
| |
| Evans), or Veit’s caudale Kopfganglienleiste, and is that portion of the neural
| |
| crest associated with the hyoid arch and the acoustico-facial nervous complex.
| |
| It is situated, as the figures show, in close relation with the otic placodes, but
| |
| there is no appearance which would suggest a contribution of placodal cells to
| |
| the crest material. The neural crest cells can easily be differentiated from the
| |
| cells of the adjacent neural tube, but most of the sections through this region
| |
| show an appearance as if crest cells are being budded off from the line of
| |
| apposition, in the median plane, of the two halves of the neural plate. The
| |
| appearance, in fact, suggests that complete dorsal fusion of the neural folds
| |
| has not yet taken place (see Pl. II, fig. 7), although they are completely separated from the overlying, continuous, somatic ectoderm by the relatively huge
| |
| mass of neural crest cells. This acoustico-facial primordium is so large that it
| |
| produces a definite protuberance upon the dorsal aspect of the embryo.
| |
| | |
| | |
| The form taken by the acoustico-facial neural crest mass in this embryo is
| |
| very different from that seen in Corner’s ten-somite human embryo (cp.
| |
| Text-fig. 2B). In his specimen the anterior limit of fusion of the neural folds
| |
| has not extended so far forward as in our embryo. It reaches only to the level
| |
| of the acoustico-facial neural crest primordium which, here, is represented by
| |
| bilateral and entirely separate cell aggregations; these, according to Corner’s
| |
| description and microphotographs, seem to stream out of the angle of junction of the neural and somatic ectoderm. In some regions he found a sharp demarcation of the neural crest cells from the adjacent mesenchyme; in other regions
| |
| it was impossible to draw a line between the lateral margin of the crest and the
| |
| mesodermal elements. In our embryo we find no difficulty in distinguishing
| |
| between the cells of the acoustico-facial primordium and the surrounding,
| |
| frankly mesodermal, elements. Hence there is no appearance of continuity
| |
| between the crest material and the hyoid, or other, branchial mesodermal condensations. Other human embryos of the somite period in which the neural
| |
| crests have been studied seem to correspond with Corner’s description of the
| |
| arrangement of the acoustico-facial neural crest elements. Thus in Payne’s
| |
| (1925) embryo of seven somites (Text-fig. 2A), and Veit’s embryo of eight
| |
| somites, there are two, quite separate, acoustico-facial primordia; and Heuser
| |
| (1930), in his fourteen-somite specimen, describes bilateral acoustico-facial
| |
| primordia in an embryo with complete closure of the neural tube in the
| |
| definitive hindbrain region (Text-fig. 2C).
| |
| | |
| | |
| Text-fig. 2. Diagram to show the arrangement of the acoustico-facial neural crest primordia in
| |
| certain human embryos. A. Payne embryo of seven somites. B. Corner embryo (ten somites).
| |
| C. Heuser embryo (fourteen somites). D. Baxter-Boyd embryo (ten somites). Ectoderm,
| |
| neural folds and tube indicated in solid black; acoustico-facial neural crest material stippled;
| |
| endoderm and dorsal aortae outlined. (For explanation see text.)
| |
| | |
| | |
| | |
| There is, then, a marked difference between the acoustico-facial neural
| |
| crest primordium in our embryo and the same region in comparable human
| |
| embryos. Our specimen may, of course, be pathological; tubal gestations are notoriously prone to show abnormalities of development. We are inclined,
| |
| however, to regard it as showing no more than a variation of the usual neural
| |
| crest cell pattern, for, if further development had occurred, it is quite possible
| |
| that the mid-line mass would have separated into the typical, bilateral,
| |
| acoustico-facial primordia. Indeed in its caudal portion there is already present
| |
| such a separation (Pl. II, fig. 5) and the appearance here is very similar to that
| |
| shown by other human somite embryos. The neural crest is primarily a derivative of the lateral part of the neural plate and whether it arises by proliferation from the lateral margins of the neural folds or from the roof of the
| |
| closed neural tube is dependent upon the time at which the neural folds fuse
| |
| dorsally. With delayed closure the tendency will be for the crest cells to arise
| |
| from the edges of the neural folds and bilateral primordia will result. When
| |
| closure is early the cells will take their origin from the dorsal portion of the
| |
| fused folds and will, therefore, form a temporary mid-line mass of neural crest
| |
| material. Lenhossek (1891) described both these modes of origin in the human
| |
| embryo. Since the crest cells arise from the junctional zone between the
| |
| somatic and neural ectoderm it is not surprising that, for a short time, immediately after closure of the neural tube, some crest cells are found dorsal to
| |
| the line of closure. Raven (1932) has published figures of the development of
| |
| the neural crests in the Axolotl which show a mid-line arrangement of a considerable extent of the crest material dorsal to the closed neural tube and a
| |
| number of other workers (cp. Brachet, 1935) have drawn attention to this
| |
| temporary arrangement in other vertebrates.<ref>When this paper was presented at the Summer Meeting of the Anatomical Society, 1938, Prof. J. P. Hill showed a section through the acoustico-facial crest of a sparrow embryo in which the distribution of the crest cells was very similar to that shown by our human embryo. He kindly drew our attention to the work of Belogolowy (Zur Entwiclclung der K opfnerven der Végel, Moscou, 1910), who figures sections through the neural crest of chick embryos in which there is a mid-line arrangement of the crest cells. Belogolowy writes: “Charakteristisch fiir diesen Nerv (acousticofacialis) ist eine erhalten bleibende Zellgruppe der dersalen Seite des Neuralrohres.” Unlike our specimen, however, the acoustico-facial primordium in the chick appears to be connected as much with the ectoderm as with the neural tube. It would seem that the time relations between closure of the neural folds and dilferentiation of the crest cells dilfer in bird and mammal. Our specimen in this respect resembles the avian pattern, but development has proceeded too far to show the con nexion between the acoustico-facial primordium and the overlying ectoderm which is completely separated from it.</ref> In our embryo, however, cells
| |
| belonging to the neural crest are found in the dorsal mid-line only at the level
| |
| of the acoustico-facial primordium; none are found at more caudal levels
| |
| although closure of the neural tube has occurred as far back as the seventh
| |
| somite. We conclude, therefore, that in this specimen the cause of the unusual
| |
| arrangement of the acoustico-facial neural crest cells was either precocious
| |
| closure of the neural tube at this level only, or a delay in the time of appearance
| |
| of the neural crest cells. As other ten-somite human embryos show a less degree
| |
| of closure of the neural tube than our embryo, we think the former explanation
| |
| to be more correct; and if this be accepted, then the variation is easily understandable and is of no morphological significance, involving, merely, a time
| |
| relationship.
| |
| | |
| | |
| | |
| | |
| | |
| </references>
| |
| {{Footer}}
| |
