Paper - The subdivisions of the neural folds in man
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The Subdivisions of the Neural Folds in Man
G. W. Bartelmez
Department of Anatomy, The University of Chicago, and the Laboratory of Embryology, Carnegie Institution of Washington
Veit and Esch have recently given us the most complete and detailed study of a vertebrate embryo during the period of somite formation that has ever appeared. All the labor and study expended upon it has been Well worth while, as human embryos of this period are very rare. The specimen is certainly normal and the preservation above reproach. The embryo has eight somites and belongs to the beginning of the third Week, a period which Prof. H. M. Evans and I have been studying for some years. Most of Veit and Esch’s findings fit well into the sequence of events as We have interpreted it from our series of embryos. There is, however, a radical disagreement in our interpretations of the nervous system, and in View of the great importance of the Veit embryo to human embryology, it would seem wise to call attention to the matter.
In his first paper based upon this embryo (’18), as well as in the complete description (’22) Veit has adopted a slight modification of the traditional interpretation of the nervous system in young human embryos. This seems to have originated with Kollmann (’89) in his description of the celebrated embryo ‘Bulle,’ which he had studied simply as a whole mount in balsam. The identification of the regions of the brain was, in the nature of the case, almost wholly subjective. The subsequent Writers who have ventured interpretations of the nervous system of embryos younger than ‘Bulle’ have followed Kollmann more or less closely. They have all made the forebrain relatively enormous and the hindbrain insignificant in size. None of these workers had a series of stages, such as is generally recognized as essential for the interpretation of the differentiations which can be seen in young embryos. It is not surprising that gross errors have crept into our text-books in spite of the correct interpretations of Giglio-Tos (’02; 15—somite embryo) and Low (’O8; 14-somite embryo).
We have now made a minute study of fourteen human embryos ranging from two to sixteen somites. In addition, the Davis (’20, ’23) embryo, of twenty somites, and the perfect 4-mm embryo no. 836 of the Carnegie Collection have been available for study. Of the latter there is a complete series of models in the Carnegie Laboratory, prepared (under the direction of Professor Evans) by Mr. O. O. Heard, who has made most of the other models I have used in this work. I am indebted to Doctor Davis for the use of his series of models. The identification of certain landmarks has made it possible to trace the history of the primary subdivisions of the brain to the 4-mm. stage, where there can be little doubt as to the three primary brain vesicles or the rhombomeres. Two of these landmarks are present from the youngest embryos on; others appear a little later, and together they afford a substantial body of evidence upon which our analysis is based. This evidence may be summarized as follows:
- A marked enlargement of the neural folds (or tube as the case may be) in the region of the otic plate can be recognized in every embryo. It may be termed the otic segment and can be shown to become the fourth rhombomere of the usual terminology. It could not escape notice even in a superficial study, and most writers have called it the second brain Vesicle, viz., Kollmann (’89), Dandy (’10), Bujard (’21, fig. 2), and the authors of various texts. This may also be the interpretation of Keibel and Elze (_’08, p. 18) for ‘Klb.’ Wallin (’13) and Veit and Esch (’2‘2) termed it the rostral end of the hindbrain. Giglio-Tos C02) and .Low (’08) have correctly analyzed the nervous system in their specimens, which were older than any described by the authors just referred to. The peculiarities by which the otic segment can be recognized are these:
- The form of the neural folds characteristic at this level (cf. p. 236).
- From the four—somite stage on, the acoustico-facial primordium is arising from its dorsal edge, and this division of the neural crest is distinctive in form and behavior (cf. p. 242).
- The adjacent ectoderm is thickened as the otic plate which can be readily recognized in the two- somite embryo (Ingalls, ’20), although it does not begin to invaginate until the eleven-somite period.
- The relation of the otic segment to such structures as the pharyngeal pouches, the heart, the aortic rami, etc., shift but slowly during the few hours of development we are studying, and these relations serve to confirm our identification.
- The second landmark is the midbrain which constitutes the knee of the cranial flexure. The latter can be recognized as the first abrupt bending of the neural axis which we encounter as We pass back from the rostral end. It is obvious at least as early as the two-somite stage, but the midbrain thus located does not always have well-defined boundaries, unfortunately. Other differentiations appear, however, which help to delimit it. The optic primordium is such a one, since its caudal end serves to locate the di-mesencephalic boundary.
- The behavior of the neural crest of the trigeminal segment is distinctive so that it can be used to identify this part of the hindbrain in the older members of the series.
- The first somite is unmistakable because of its form and the behavior of its cells, and during the period involved there is but little shifting with reference to the nervous system.
The following figures are from midsagittal projection reconstructions which, with the exception of the first, were made at amagnification of 200 diameters. In the original charts every section was plotted and all were controlled by the study of themodels. The figures are from accurate copies by Mr. J . F. Didusch of my original charts.
Figure 1 presents an analysis of a two—somite embryo (no. 1878 of the Carnegie Collection) which has been well described by Ingalls (’20). The neural folds can be divided into five segments which are separated either by constrictions or by sulci on the lateral surface of the folds. The midbrain (mesen.), defined by the cranial ﬂexure, separates the forebrain (prosen.) from the hindbrain. The latter exhibits three subdivisions: the first (rh.A) is small but clearly defined, especially on the right side; the second, the otic (rh.B), is prominent, and the third (rh.C) involves the rest of the neural folds rostral to the first pair of somites. The otic segment in this specimen differs from those of all succeeding stages in that there is a general enlargement of the neural groove corresponding to it. The otic plate (disc.ot.) is practically coextensive with the otic segment and is well marked, as was pointed out by Ingalls (’20).
Figure 2 gives the relations in a four-somite embryo (H279, U. of C. Coll.) in which abundant mitoses are to be seen, although the specimen underwent great shrinkage during dehydration. It belongs to a group which includes that just described as well as Wilson’s ‘H3’ (’14) and ‘Klb’ (Keibel and Elze, ’O8, Normentafel No. 3). Forebrain, midbrain, and three hindbrain subdivisions were clearly visible in the gross specimen when studied in 80 per cent alcohol. It will be seen in the figure that the forebrain has begun to grow forward beyond the pharynx and that it is relatively longer than in the previous case. The midbrain is wedge—shaped. There are clear signs of differentiation in the hindbrain in that there are four segments and a ganglionic anlage. The first segment (rh.A) is still small and inconspicuous, whereas the second (rh.B) has acquired new characters which distinguish it for the rest of our period. The enlargement is sharply marked off by constrictions fore and aft, and corresponding to it there is a dip in the ﬂoor. Ventrally the neural groove is enlarged in the manner typical for neuromeres, but dorsally the folds approach one another only to diverge again at the dorsal edge where they are thickened. The thickening is the acoustico-facial primordium (pr.ac.fac.). These relations may be seen in figure 1 of my 1922 paper. The level of that section is indicated in the present figure 2, where it will be seen that the plane of section passes obliquely through the otic segment (rh.B) and the two succeeding segments. The latter two (rh.C1 and rh.C2) correspond in position to the third hindbrain segment of the previous specimen (rh.C). It may be that that segment has divided, but it is possible that H279 is an individual in which the segmentation of the nervous system is particularly pronounced.
Fig. 1 A projection reconstruction on the midsagittal plane of a two-somite embryo (no. 1878, Carnegie Coll.). x100. The cut surfaces of the nervous system are hatched, those of the gut, stippled. The body ectoderm and the primitive streak are indicated by broken lines. The arrows show the plane of section. Section 44 is reproduced by Ingalls (’20) as figure A, page 81. disc.ot., otic disc or plate; lm.pr., primitive streak; mem.cl., cloacal membrane; mem.ph., pharyngeal membrane; mesen.,midbrain; n.pr., primitive node of Hansen; p.int.a., anterior intestinal portal; ph., pharynx; prosen., forebrain; rh.A,B, and C’, first, second and third hindbrain segments; 3.1, first somite with myocoale.
The eight-somite embryos, no. 391 of Mall (Dandy, ’10) and H87 (U. of C. Coll), are transitional to the next phase in the development of the nervous system. H87 has been brieﬂy described and figured (Bartelmez, ’22; figs. 2b, 3, 4, 5, 7 , and 9a). VVe can recognize forebrain, characterized by the optic primordium, midbrain, and three hindbrain segments. The first hindbrain segment is larger than in any younger embryo and its crest primordium is proliferating mesectoderm as far caudal as the acoustico-facial anlage. The second segment is the otic from which the acoustico—facial primordium is beginning to separate. The third clearly corresponds to the first postotic of H279 (fig. 2, rh.C1), but the segment homologous to C2 is only vaguely indicated. The typical form of the otic segment with its hourglass-shaped lumen is shown in figure 2b of my paper of 1922. In d and e of the same figure it will be seen that the corresponding lateral fossa lodges the expanded crest primordium, but the presence of the fossa in H87, as well as in the younger embryos (e.g., ‘Klb’ and the Mall embryo no. 391), shows that it is not merely the result of the splitting off of the primordium, as would appear to be the case in the later stages.
Fig. 2 A reconstruction like that of figure 1, of a four—somite embryo (H279, U. of C. Coll.); magnified 200 diameters and reduced one half in reproduction. The plane of section is indicated by the position of section 54 which was shown as figure 1 in my 1922 paper. camn-e., neurenteric canal; ch., chorda; disc.o£., otic disc; mom. cl., cloacal membrane (the entoderm has shrunken away from the cctoderm) ; mem. ph., pharyngeal membrane; mesen., midbrain; ph., pharynx; pr.ac.fac., acoustic0-facial primordium; prosen., forebrain; rh.A, rh.B, first and second hindbrain segments; rh..C'1 and 7'h.C'2 have resulted from the division of rh.C’ in the previous embryo; rh.B is identical with the definitive fourth rhombomere, rh.C'; with the fifth.
Our next stage in the development of the nervous system is represented by Veit’s embryo (eight somites), ‘DuGa’ of Eternod (nine somites), and H392 (U. of C. Coll., eleven somites). The analysis of the second of these is given in figure 3. VVhile I have not studied the sections of this beautiful specimen, I have had the series of accurate and detailed tracings of every section, magnified 200 diameters, made by Professor Evans in the laboratory of Professor Eternod, as well as the latter’s descriptions and the Ziegler model. These data, together with the study of the similiar H392, have left few uncertainties as to interpretation. The models and projection reconstructions were stacked from the profile given in figure 5 of Eternod’s (’99) paper. In this embryo (fig. 3) the continued growth of the forebrain around the end of the pharynx is associated with the great growth of the midbrain. The rostral end of this region has remained uncertain, as indicated in the figure by the dotted line. The other subdivisions can be recognized in the Ziegler model as well as in our own. The first hindbrain segment of the previous stage has not only increased in length, but has divided into two (rh./11 and rh.5’ in fig. 3), for there are now two segments between midbrain and the otic segment. The hindbrain subdivision A of figures 1 and 2 has split off a neuromere (rh.3) caudally, because later stages show that this new segment becomes the first preotic neuromere, i.e., the third rhombomere of the usually recognized series. Crest proliferation has ceased in this segment, but is still present rostrally as far as the forebrain. The cristal and optic primordia are probably continuous here as in other embryos of the same period, but this region is very difficult to interpret because it is cut tangentially. The otic rhombomere of ‘DuGa’ is typical in form, as may be seen in the Ziegler model, where it can be identified by the fact that the neural folds have closed as far as its caudal end. The first postotic neuromere (?'h.5) is, as usual, easily recognized and there is an indication of another
Fig. 3 A projection reconstruction of the head end of Eternod’s nine somite embryo ‘DuGa,’ based upon a complete series of tracings made by H. M. Evans. Magniﬁed 200 diameters and reduced one half in reproduction. The neural tube is closed as far forward as the caudal end of the otic segment (rh.4). The broken lines at the level of the ﬁrst somite represent the eight lost sections. The extent of the optic-neural crest primordia is indicated by stippling. ch.op.?, probably the chiasrna ridge; c7'.neur., occipital neural crest; cr.n.rost., rostral division of the neural crest; dz'sc.ot., otic disc (outlined by dashes); mesen., midbrain; pr.a,c.fac., acoustico- facial primordium; p1'.op. , rostral end of the optic primordium which probably continues caudally to the region of crest proliferation; prosen., forebrain; rh.A1, the remains of the primary ﬁrst hindbrain segment after the separation of the third deﬁnitive rhombomere (rh.8); rh.4 and 5, the otic and first postotic neuromeres; sac.br.I, the broken line indicates the extent of the ﬁrst visceral pouch; sin.or., oral sinus; sul.cr., the clearly cut margin of the stipple indicates the extent of the ventricular cristal sulcus; s.1, probable first somite; thy., anlage of thyroid. The arrows indicate the levels of the sections of this embryo ﬁgured by me in 1922 (ﬁgs. 2c and 9b).’
3 Attention may be called here to a misprint in the legend to this ﬁgure. The section reproduced as ﬁgure 2c is number 21, not 41, of the series.
- Keibel and Elze (’08, p. 18) have called attention to a cranial flexure in the five- to six-somite embryo ‘Klb’ (Normentafel no. 3). It is not clear from the text whether they refer to the flexure as we have identified it or whether they mean the more caudal one. The latter is a more abrupt bend which appears in the Keibel model, but not in the figures of Kroemer which were reproduced by Pfannenstiel (’03). It is located at the rostral extremity of the otic segment which is well marked in this embryo.
Cite this page: Hill, M.A. (2020, December 4) Embryology Paper - The subdivisions of the neural folds in man. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_subdivisions_of_the_neural_folds_in_man
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