Paper - Symmetrical, segmental thickenings in the dorsal ectoderm of human embryos
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Ingalls NM. Symmetrical, segmental thickenings in the dorsal ectoderm of human embryos. (1929) Amer. J Anat. 44(3): 455-473.
|Carnegie Collection human embryos segmental thickenings in the dorsal ectoderm of human embryos.
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Symmetrical, Segmental Thickenings in the Dorsal Ectoderm of Human Embryos
N. William Ingalls
Department of Anatomy, Western Reserve University, Cleveland, Ohio
Five Text Figures And Two Plates (Eighteen Figures) 1929
Some three years ago, Grosser (’26), in opening the thirty fifth session of the Anatomische Gesellschaft, took occasion to dwell upon the primitiveness of the human organization, particularly in its developmental aspects. Among the great number of examples which could be cited from human ontogeny, we find many which are very constant, if not invariably present, while on the other hand certain features may be very ephemeral or so variable or inconstant in their appearance that they are only rarely encountered. There is, however, always the possibility, or rather the probability, that certain more or less usual conditions have been overlooked entirely or, if seen, have been left unnoted or unappreciated. The all but endless variability of the adult body is common knowledge, but we know next to nothing about the variability in the early stages of development. The reasons for this are very obvious, and, consequently, for many of the details of development, we can form no idea as to frequency or constancy. The material is available somewhere, but the information wanted is lacking. When a few thousand embryos have been worked over as carefully and as thoroughly as the many thousands of dissections of the adult, we shall know more about the early— and late—stages of development.
It is, therefore, not possible to make any definite statement as to the frequency or rarity of the conditions described in the present paper. The evidence available, as will appear later, would indicate that they may not be especially infrequent. Whatever their significance, however, one cannot escape the conclusion that they represent extremely primitive features of vertebrate organization, ancient integumentary organs, traces of which crop out now and again at certain stages in development.
When fully and completely developed, these symmetrical segmental thickenings, or disci dorsales, if we may adopt and extend the nomenclature of Bartelmez and Evans (726), appear as shown in figure A. This represents a left lateral view of embryo no. 155, C.R. 11.8 mm. The thickenings or dises are indicated by the row of dots parallel to the dorsal midline and extending from the level of the eighth cervical ganglion to the lower border of the first lumbar. The individual thickenings differ somewhat in size and structure, as will be noted later. Although varying to some extent in their relation to the spinal ganglia, they are, nevertheless, essentially segmental in arrangement, typically between or near the anterior or posterior borders of the ganglia, and at the same time close to or just dorsal to the center of the ganglia. Considering the dises as really intersegmental, in relation to the spinal ganglia, we find in this case, on the left side, fifteen dises and fourteen interspaces. There is one disc opposite the fifth ganglion, instead of between the fifth and sixth, and an extra one opposite the last thoracic ganglion. Except for these minor discrepancies, the arrangement is surprisingly regular, not only as indicating a segmental distribution, but even more so as regards the interval between each thickening and midline of the body behind, shown to a better advantage in figure C. In this latter respect they are even more regular than the ganglia themselves.
In figure B the typical relations of the thickenings in the same embryo are reproduced more diagrammatically and also on a larger scale. The lower drawing is a schematic representation of a cross-section at the level of the third thoracic segment. On either side appear the ectodermal thickenings, somewhat overdrawn for the sake of clearness (compare pl. 1, fig. 1). The nerve which runs laterally just beneath the thickening is the cutaneous branch of the posterior primary division; the muscular branches end in the underlying premuscle mass. In the upper drawing only the ganglia and the posterior primary divisions of the second, third, and fourth thoracic nerves are shown. The longer nerves, running forward and outward, apparently in close relation with the ectodermal dises, are the medial, or cutaneous branches of the posterior primary divisions. The forward, as well as lateral, course of these cutaneous nerves is quite characteristic, but it does not seem possible to attach any special significance to their relation to the epithelial thickenings.
EMBRYO NO. 155 CR. 118
Fig. A The symmetrical, segmental thickenings, or disci dorsales, so called, extend on this side of this embryo from the last cervical to the lower border of the first lumbar ganglion. The anterior divisions, intercostal nerves, from the second to sixth thoracic segments are shown and also the posterior divisions of the second, third, and fourth nerves. Ventral to the intercostal nerves: appéars the milk ridge.
EMBRYO NO, 55 CR 118
Fig.B Schematic representation of conditions in no. 155. Below, a section at the third thoracic segment, showing location and relations of dorsal dises. Compare plate 1, figure 1. Above, dorsal view, somewhat larger, of second, third, and fourth thoracic segments; the dises shown are the second, third, and fourth of the series on each side.
The entire series of discs in no. 155 may be seen in figure C, which shows twenty-seven in all, fifteen on the left side and twelve on the right. The upper limit is essentially the same on both sides, being between the last cervical and the first thoracic ganglion on the right, but overlapping the cervical ganglion on the left. The lower limit on the left is, as noted in figure A, the lower border of the first Jambar ganglion, while on the right it is exactly two segments higher. There are very evident variations in the intervals between successive dises, so that detailed comparisons between the two sides are hardly warranted. Embryo no. 155 shows by far the greatest number of discs and the most regular arrangement of any of the four embryos in which these structures have been found. For this reason it may be looked upon as the ‘type specimen’; on the left side at least it seems to have the full quota of discs. It is also significant that the thickenings presented by the other three embryos fall, without exception, within the limits set by no. 155.
EMBRYO NO. |S EMBRYO NO. 155 CR. 10.4 CR. ANS
Fig.C Dorsal dises of nos. 15 and 155.
A smaller embryo, no. 15, C.R. 10.4 mm., is also shown in figure C; it is the smallest, or youngest, in which these dorsal dises have been encountered. In this case there are seven, five on the right and two on the left. The posterior limit is about the same on the two sides, opposite or just beyond the last thoracic ganglion, while the uppermost dise on the right is between the sixth and seventh ganglia. In spite of some irregularities, the thickenings tend to be interganglionic in position.
EMBRYO NO. IBA CR. 124
Fig. D Dorsal dises in nos. 253 and 18A. The former embryo is apparently smaller, on account of being more sharply bent.
The other two embryos exhibiting dorsal thickenings are somewhat larger, no. 253 being 12.5 mm. C.R. and no. 18A, 12.4 mm. The former, on the left in figure D, is much like no. 15; there are two discs on the left and six on the right. The most posterior dises on both sides show relations practically identical with no. 15, while the upper limits are also much the same, except for the isolated disc high up on the right side between the first and second thoracic ganglia. Only two thickenings could be discovered in no. 18A, figure D, one on each side. The one on the right side is located opposite the first lumbar ganglion, the one on the left is near the lower border of the third thoracic ganglion.
The four embryos in which dorsal thickenings have been found are shown in figures C and D; their lengths, C.R., range from 10.4 to 12.5 mm. Careful search through a considerable number of other embryos, both larger and smaller, has failed to yield anything positive. It is altogether possible, however, that some thin, small, poorly developed discs may have been overlooked, since some of those shown in the figures were only found by noting the gaps in the series and again examining the slides. This failure to find anything in embryos under 10.4 or over 12.5 is all the more surprising, since of the five embryos within these limits, four, or 80 per cent, showed definite dorsal discs. Unless these four embryos represent a very exceptional and atypical sampling of embryological material, which is highly improbable, then the ectodermal conditions noted above cannot be looked upon as particularly uncommon. Beyond this nothing can be said as to their frequency. As regards their restriction to a limited period of development, the evidence is much less equivocal. It is extremely unlikely that the conditions in question would be found in four out of five cases, but not earlier nor later, unless these conditions are actually restricted to a short and rather definite stage in development; roughly, it would appear, between 10 and 13 mm.
The dimensions and histological characters of the discs vary considerably even in the same embryo. ‘They seem to be approximately circular in outline with a diameter ranging from 0.06 to 0.08 or 0.09 mm. Their thickness varies from 0.02 to 0.04 mm., while the ectoderm elsewhere in the neighborhood is only 0.005 to 0.008 mm. It is not possible to distinguish between younger and older stages, if such be present. Whatever these thickenings may represent, one could hardly expect any great uniformity either in structure or in location.
It is altogether probable that the twenty-seven discs shown in no. 155 are all that were ever present in this embryo, but it is also possible that there were never more than two in no. 18A. These and similar questions must await a more extensive material.
The histological details of some of the more characteristic thickenings from each of the four embryos concerned are shown in plates 1 and 2.
The general relations and location of the dises are shown in plate 1, figure 1, which represents a section through the third dise on the left side of no. 155 (compare figure B above). The disc appears as an elevated thickening in the ectoderm opposite the spinal ganglion. The small elongated structure in the mesenchyme, ventral and internal to the disc, is an oblique section of the cutaneous branch of the posterior primary division of the next spinal nerve. In figure 2, plate 1, is shown the most anterior disc on the right side of no. 155 at a considerably higher magnification. It is particularly well developed and lies opposite the interval between the last cervical and first thoracic ganglia. In section it is quite regular in outline, measuring about 0.07 mm. in diameter by a little more than 0.02 mm. in maximum thickness. The superficial ectoderm in the immediate vicinity is roughly 0.006 to 0.007 mm, thick. The external, free surface of the disc is slightly convex, projecting a little above the surrounding surface, while the deep surface is strongly convex.
The histological details of this disc are quite typical. The bulk of it is composed of a deep layer of cylindrical cells which seem to be directly continuous with the low cuboidal cells of the surrounding ectoderm. The cell boundaries of these basal cylindrical elements can be made out quite clearly, while their nuclei are located in the extreme distal part of the cells. This peripheral position of the nuclei, the apparently marked polarity of the deep layer of cells, is one of the most characteristic features of these discs, even where they are poorly developed. The more superficial, overlying cells are fewer in number and much smaller. They seem to be quite irregular, both in form and arrangement; cell boundaries cannot be made out, but some of the outermost cells are apparently squamous in type. It is the deep layer of large cylindrical cells, however, which is most evidently in direct continuity with the thin surrounding ectoderm. Occasionally there are appearances which suggest cavity formation in the thicker and larger discs. Almost exactly in the center of the disc in figure 2 is such an apparent opening, just external to the nuclei of the basal cells; a more conspicuous example will be noted later. The underlying mesenchyme is loose and delicate, made up of scattered branching cells.
Figure 3, plate 1, is the same disc and the same section as that shown in figure 1. It is somewhat smaller than the previous one, but distinctly thicker. It is also the only disc which is so prominent and conspicuous externally. It differs from the one just described in that the basal layer of cells is not quite so high, while the superficial cells are more numerous and apparently larger; the suggested cavity is also more superficially placed, being among the outer cells, instead of just outside the deep layer.
The largest disc in any of the embryos is that shown in figure 4, same plate. It is also from no. 155 and is the sixth disc on the right side, located opposite the sixth thoracic ganglion. The dorsal border, above in the figure, is fairly definite, but ventrally it fades out more gradually into the neighboring ectoderm. It measures nearly 0.09 mm. in diameter, as shown here, and about 0.025 mm. in thickness. Structurally, it is much like figure 2, but shows no indications of a possible cavity within. The dises represented in figures 5 and 6 are much less well developed than the preceding ones. The first is the tenth dise on the right side, the other occurs in the same section on the left side. The former is fairly large and shows the typical polarity of the basal cells. It projects outward rather than inward and its limits are not very sharply defined. The latter disc is quite thin and inconspicuous, its constituent cells are only a little higher than those of the adjacent ectoderm, but their polarity is still evident. This is an example of those dises which are found only by searching in the gap between the more conspicuous ones, they are very easily overlooked, and some of them may have escaped us.
None of the thickenings in embryos nos. 15 and 18A are as well developed as the more characteristic ones in no. 155. In figure 7, plate 1, is shown the most anterior disc on the right side of no. 15, lying between the sixth and seventh thoracic ganglia. It is not very thick, but of considerable extent in its other dimensions, tapering off gradually on either side. Except for size and number of cells, there is no essential difference between this disc and that represented in figure 5. The only disc on the left side of no. 18A, near the caudal border of the third thoracic ganglion, is shown in figure 8. In this case the dorsum is on the left, instead of above. There are two layers of cells here, the outer somewhat flattened, almost squamous, while the deeper layer is high cuboidal with the nucleus in the distal half of the cell. Around this disc the superficial ectoderm is two-layered, the outer layer being very thin and recognizable mainly from its nuclei, while the inner is made up of low, broad cells whose height is about equal to the diameter of the nuclei within. If none of the discs had been better developed than those represented in figures 6 and 8, there is little likelihood that they would have attracted any particular attention and they might well have remained unnoticed.
Excepting no. 155, there is only one other embryo which shows really typical dises, and that is no. 253. It has the greatest C.R. measurement of any of the four specimens, 12.5 mm., and also, except for no. 155, the greatest number of discs, eight in all (fig. D). Three of these are shown on plate 2, all from the right side. The first figure represents the most anterior disc, located between the first and second thoracic ganglia. It is rather thin, but perfectly definite, and shows the characteristic structure. The second disc on the same side, but separated from the first by a considerable interval, since it lies opposite the anterior border of the seventh ganglion, is shown in figure 2. This disc, although smaller than many others, is relatively quite thick and very sharply delimited. It presents no unusual features beyond the suggested cavity within it. Figure 3 represents the succeeding dise, it is also typical in structure and shows especially well the apparent cavity formation. Although the structures which have just been described under the name of dorsal dises are perfectly clear and obviously significant, their interpretation is by no means as evident. That some importance attaches to them is indicated by the characteristics outlined above. These are their essential symmetry and regularity of distribution, their apparent restriction to the thoracic and adjacent upper lumbar regions, their apparent restriction also to a very brief but definite period of development, and finally the definite and uniform structure presented by the discs where well developed. The conditions found in no. 155, on account of their extent and completeness, naturally form the starting-point for questions of interpretation.
Given a vertebrate embryo with integumentary organs arranged like the discs in no. 155, one naturally thinks of lateral line and more particularly of the dorsal row of lateral-line organs, which, in Amphibia, is often restricted to the region between the extremities. There are many other points, however, which are not so favorable to such an interpretation. As far as can be made out, these ectodermal thickenings arise in situ and quite independently of each other, there is no very definite evidence that the more anterior discs are older, although they may seem to be better developed, and nothing whatever to indicate any present or past relation of any of these thickenings with the vagus or a possible vagus placode. In all cases there is a wide gap between the region of the vagus and the most anterior discs. One would expect real lateral-line primordia to appear at an earlier date and also to give better evidence of their genetic relations, if such exists, to more anterior structures. Of some weight, also, in this connection is the statement, if it be correct, that not even traces of lateral-line organs appear in the ontogeny of amniotes. It is difficult, also, to understand why this particular part of the lateralis system should have been resurrected instead of some of its more primitive portions. As far as we can gather, aberrant lateralis branches of the X nerve have never been described, but the fact that anomalous branches or roots have been noted in other cranial nerves, on VI and XII, and especially the findings of Bremer (’21) that recurrent abducens branches are particularly frequent in human embryos, should not be overlooked. Whatever may be said, either for or against lateral line or its mode of development, it remains, in many ways, the most tangible and concrete condition with which these ectodermal thickenings might be compared.
It is more than doubtful if these dorsal dises have anything to do with later skin derivatives, such as glands, hair, etc., although, as far as their location goes, they are not unlike the dorsal glands of the Crocodilia (Reese, ’21). They are present, however, at too early a stage and in too characteristic a form to be anything but very primitive structures, probably sense organs.
Older even than the lateral line, but still showing a certain similarity with the conditions we have been describing, are the so-called primitive lines, noted by Miss Platt (’94) in Necturus and quite recently by Landacre (’26) in Amblystoma. The dorsal primitive body line of Landacre compares very accurately in location, if not in extent, with the conditions described above. Like these, the dorsal primitive body line is quite variable, or even inconstant; it appears, however, at a very much earlier stage of development. It is the oceurrence of these primitive lines, or ridges, in very young stages, which gives most weight to the criticism of Stone (’28), that they represent merely the modeling of the lower surface of the ectoderm, due to the underlying structure.
It is not possible, at present, to offer any satisfactory interpretation of the dorsal discs in human embryos. That they occur also in other amniote or mammalian forms would seem altogether probable. Their most important characteristic is their location and arrangement, possibly also their histological structure. The fact that they seem to be restricted to a relatively late period of development may not be as important as might appear. In any case, the conclusion seems justified that they represent some very primitive vertebrate condition.
Mention may be made at this time of some other thickenings which occur in the dorsal ectoderm of human embryos, but at a different stage and in another location. They differ from the dorsal dises, so called, in occurring at much earlier stages; they are also much farther forward, near the otic vesicle and rather nearer the middorsal line. They do not, however, exhibit the sharp differentiation and individuality of the typical dorsal discs. Two, and a doubtful third, are shown on the right side of embryo no. 503, C.R. 3 mm. (fig. E). None were found on the left side, nor have we seen traces of them in younger or older embryos. The most anterior structure is evidently the ‘discus incertus’ of Bartelmez and Evans (’26), noted again very recently by Corner (’29). Its structure is indicated in figure 4, plate 2, high cells with the nucleus located in the superficial part of the cell, but no sharp limits from the surrounding ectoderm. Just behind the most anterior disc, and rather close to it, is a very problematical structure which might be a second dorsal pre-otic dise. Close behind the otic vesicle is still another disc, differing in no essential details from the one in front. It is shown in figure 5, plate 2.
The significance of these anterior, cephalic discs is by no means clear, and they may be related only in a general way, if at all, with the dises which appear later in the thoracic region.
EMBRYO NO. 503
Fig. E Discs in the head regions of no. 503; they occur only on the right side. The otic vesicle is not yet cut off from the superficial ectoderm.
BarreLMez, G. W., anD H. M, Evans 1926 Development of the human embryo during the period of somite formation, including embryos with two to sixteen pairs of somites. Contributions to Embryology, vol. 17, pp. 1-67.
Bremer, J. L. 1921 Recurrent branches of the abducens nerve in human embryos. Am. Jour. Anat., vol. 28, pp. 371-397.
Corner, G. W. 1929 A well preserved human embryo of ten somites. Contributions to Embryology, vol. 20, pp. 8-102.
Grosser, O. 1926 Eréffnungsansprache. Verh. d. anat. Ges., S. 3-15.
LanpacrE, F, L. 1926 The primitive lines of Amblystoma jeffersonianum. Jour. Comp. Neur., vol. 40, pp. 471-495.
Puatr, Jutia B. 1894 Ontogenetische Differenzierunng des Ektoderms in Necturus. Arch. f. mik. Anat., Bd. 43, 8. 911-966,
Resse, A. M. 1921 ‘The structure and development of the integumental glands of the Crocodilia. Jour. Morph., vol. 35, pp. 581-611.
Sronz, L. 8. 1928 Primitive lines in Amblystoma and their relation to the migratory lateral-line primordia. Jour. Comp. Neur., vol. 45, pp. 169-190.
PLATE 1 EXPLANATION OF FIGURES
1 Embryo no. 155, section 547. x ca.55. Third dise on left side, counting from before backward. Low-power photograph, to show general position and relations.
2 No. 155, section 494. > ca.650. Uppermost, most anterior dise on right side, between last cervical and first thoracic ganglia, an especially good disc.
3 No. 155, section 547: X ca.650. Same as figure 1 just above it, but higher power. One of the few dises which project externally as well as internally.
4 No. 155, section 636. X ca.650. Sixth dise on right side, opposite sixth thoracic ganglion. Much like figure 2, but definitely larger.
5 No. 155, seetion 735. X ca.650. Tenth dise on right side, between ninth and tenth thoracic ganglia. Not as sharply limited as previous discs; projects outward rather than inward.
6 Same as figure 5, but left side; tenth dise, rather thin and poorly delimited.
7 Embryo no. 15, section 559. X ca.650. Most anterior dise on right side, between sixth and seventh thoracic ganglia, smaller than the dises shown in figures 2 to 5, but very definite.
8 Embryo no. 184A, section 622. X ca.650. Only dise on left side, near caudal border of third thoracic ganglion. The dorsum in this figure is toward the left.
PLATE 2 EXPLANATION OF FIGURES
1 Embryo 253, section 532. XX ca. 650. Most anterior dise on right, between first and second thoracie ganglia. Dorsum toward the left.
2 No. 253, section 684. X ca.650. Second dise on the right side, opposite anterior border of seventh thoracic ganglion, well marked, sharply limited thickening.
3 No. 258, section 712. X ca, 650. Next behind dise shown in figure 2, opposite eighth thoracic ganglion, apparent lumen or cavity in this dise.
4 Embryo no. 503, section 104. X ca.650. Discus incertus, most anterior of two pre-otic thickenings shown in figure E.
5 Same embryo, section 77. X ca. 325. Postotie dise.
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