Paper - The development of the neural folds and cranial ganglia of the rat

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Adelman HB. The development of the neural folds and cranial ganglia of the rat. (1925) J. Comp. Neurol. 39(1): 19-171.

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This historic 1925 paper by Adelman described development of the early rat central nervous system and cranial ganglia.

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The Development of the Neural Folds and Cranial Ganglia of the Rat

Howard B. Adelmann

Department of Histology and Embryology, Cornell University, Ithaca, New Pork

Six Text Flgures and Twenty-Four Plates (Ninety-Five Figures) 1925.

It is a pleasure to acknowledge here the generous help of many friends. I am especially indebted to Prof. B. F. Kingsbury for constant advice and encouragement. It was he who suggested that I take up the work. Miss Janet A. Williamson kindly allowed me to use the models of the head of the rat which she constructed as well as a number of important series prepared by her. I also wish to thank Dr. Fred W. Stewart for the use of many excellent series of older embryos, and finally I should like to express my appreciation of the skill and unfailing courtesy of Miss F. Louise Duhring, who collected the material at The Wistar Institute. I am indebted to the Mrs. Dean Sage Research Fund, which bore the expenses of the investigation.


The early development of the neural tube and cranial ganglia has been investigated with some degree of completeness in only a few mammalian forms. There are, it is true, numerous accounts based upon the study of very limited material and the literature abounds with observations on the development of the neural tube and cranial ganglia made incidentally in works dealiiig with the general anatomy of the embryo. Bartelmez ('22, '23) has recently called attention to the paucity of our knowledge of this subject and has himself contributed greatly to our understanding of the early development of the neural folds and sensory anlagen of the human embryo.

The reasons for the scarcity of work dealing with the development of these structures in the Mammalia are obvious, since the difficulties attending the collection of complete series of mammalian embryos are well known. In studying human embryos investigators have been especially handicapped both by the scarcity of the material at their command and the faulty preservation which such embryos frequently exhibit due to the circumstances under which they are obtained.

There are still many features of the development of the neural crest and cranial ganglia in mammals upon which additional observations are much needed, and many inter- esting questions are still at issue. Workers on the lower forms, especially the Ichthyopsida, seem to be quite generally agreed that the epibranchial and lateral-line placodes contribute liberally to the formation of the cranial ganglia, but the occurrence of such placodal contributions in Mammalia is still an open question. Several authors have described the formation of mesenchyme (mesectoderm) from neural-crest elements in the mammal, and this has been denied by others. The anterior limit of the neural crest, a point of the greatest theoretical importance, has not yet been clearly determined in the mammal. Further observations are needed on the exact mode of origin of the crest and its relation to the neural plate and ectoderm.

In addition, there are problems in connection with the individual cranial ganglia which have not been adequately solved. What, for instance, is the exact mode of origin of the ophthalmic ramus of the trigeminus in the mammal? Does it arise, as Belogolowy ('10) suggests for the bird, as a condensation of diffuse neural crest proliferated from the mid-brain; by placodal proliferation, as some have maintained; or by forward growth from the main ganglionic mass of the trigeminus? Is there a separate profundus anlage of the trigeminus, as Schulte and Tihey (’15) indicate in the cat? Does the acoustic ganglion split off from a common acoustico-facial mass? Is it increased by proliferation from the walls of the otic vesicle? Is it true that the ganglia petrosum and nodosum have an origin distinct from that of the rest of the IX-X anlage, as Streeter (’04) thought possible?

The answers to some of the questions proposed above depend upon a knowledge of the subdivisions of the early neural plate and tube.

The foregoing brief outline makes clear, I think, the desirability of further studies. The writer has taken advantage of the facilities bf The Wistar Institute for the collection of a close series of rat embryos upon which a study of the above problems was made. He has tried to keep constantly in mind the actual growth transformations of the whole head, in which the developing ganglia are involved. The early history of the neural plate and tube has been followed, inasmuch as an understanding of the growth and subdivisions of the early neural tube is necessary in studying the relations of the ganglia.

Material and Methods

This paper is based upon the study of more than 200 series of embryos of the white rat, Mus norvegicus albinus. The rats were obtained from The Wistar Institute and most of the uteri were removed and fixed there. The embryos were fixed at three-hour intervals from the nine-day-twelve-hour stage until thirteen days ; after that at less frequent intervals. Of many of the younger, more critical stages, two or even three litters were sectioned. Considerable variation was found in some uteri. Most of the material was fixed in Bouin’s fluid; a few were fixed in Carnoy’s and some of the older stages were fixed in Zenker’s, Helly’s or vom Rath’s picro-aceto-osmic-platinic chloride mixture by Doctor Stewart. All the material was cleared in xylene or toluene and embedded in paraffin. Most of the younger embryos were cut at 7.5 um, others at 10. Most of the embryos were stained in toto with Mayer's HC1 carmine, a few in Delafield's haematoxylin. A few were stained on the slide in iron haematosylin or in haematoxylin and orange G. Models were made of several stages by the Born method.

It was found best to section the younger stages in utero, after carefully cutting away the musculature. Since early embryos of the rat are oriented in a perfectly definite fashion with respect to the axes of the uterus, it is possible to secure favorable planes of sections in a large majority of cases, even of embryos sectioned in utero, up to a certain stage. The orientation of the embryos in the uterus has been found to be essentially as described by Widakowich ('09, '11). At eleven days and after, it is quite feasible to remove embryos from the uterus so that they may be oriented for cutting.

Throughout this paper the age will, so far as possible, be given in somites, since that method is most reliable. The Cornell collection now contains one or more embryos of every somite number from 1to 32, besides a large number of older embryos beginning with 34 somites. Of many stages trans- verse, sagittal, and frontal series are available, making it possible to check up carefully the interpretation of series.

The Development of the Cranial Neural Folds

The present work, begun primarily as a study of the devel- opmental history of the cranial neural crest, might naturally begin with a consideration of such questions as the origin of the neural crest, the site of its proliferation and the locus of its first appearance. However, the work had not progressed far before it became evident that a study of the growth and differentiation of the neural plate and tube of the rat was a necessary preliminary, so that important questions concerning the relation of the neural crest to the prospective sub- divisions of the neural plate and tube might be answered with some degree of certainty. Bartelmez's ('23) recent paper on the subdivisions of the neural folds of the human embryo has been very helpful in this connection.[1] As might be expected, the results are in general quite comparable. The developmental idibsyncrasies of the two forms must, however, be kept in mind in comparing them. It was found that the rat lends itself nicely to such a study, since certain landmarks are early established on, or in relation to, the early neural plate which allow one to follow accurately the differentiations of its regions.

I n the hindbrain region of the neural folds Bartelmez ( ’23) recognizes three primary rhombomeres in young human em- bryos. These he designates rhombomeres A, B, and C. Rhombomere A divides first into two secondary rhombomeres- A, and 3- and still later, rhombomere A, divides into rhombomeres 1 and 2. Ultimately, therefore, rhombomere A gives rise to the first three rhombomeres. Rhombomere B (otic rhombomere) is a secondary as well as a primary rhombomere, undergoing no division.[2] It is the fourth of the series and is recognizable very early as a marked expansion of the neural plate related to the otic placode. Rhombomere C furnishes the last three rhombomeres -5, 6, and 7. For the sake of convenience, the nomenclature employed by Bartelmez will be used in this paper.

Like the human embryo, the rat ultimately develops seven typical rhombomeres. Figure 19 illustrates those of a 26- somite embryo. The first or cerebellar rhombomere is very shallow, sloping gradually to the isthmus ; the second marks the broadest region of the rhombencephalon and is related to the V nerve. The third rhombomere is narrow, separated from the second by a shallow groove, and free (externally at least) from nervous connections. The facial nerve is attached to the fourth or otic rhombomere, which is uniyue among the rhombomeres in that its swelling extends to the midventral line, producing there a prominent bulge. The others all ‘fade out’ before they reach the midventral line. It is somewhat wedge-shaped, being narrower dorsally than ventrally. The otic vesicle is related to the fifth rhombomere. In contrast to the preceding rhombomere, the fifth is wider dorsally than ventrally. The sixth calls for no special comment. The sev- enth is remarkable for its size, but it produces no prominmt swelling. Bradley ( ’04, p. 628) has already commented upon the large size of the seventh rhombomere of the pig embryo. The cristal proliferation for the IX-X ganglia is related to the two caudal rhombomeres. The above description is purposely brief and designed to show the essentially typical development of the rhombomeres in the rat. They seem to correspond fundamentally in their form and relations to those described by Broman ( ’95), Bartelmex ( ’23) in man and Bradley (’04) in the pig. Broman’s figure 2 (text and plate) is most serviceable for comparison, but his confusion of the cerebellum with the second rhombomere must be kept in mind. It is interesting to compare these results with the work on other rodents, which in spite of minor variations is essentially in agreement. Chiarugi (’97, pp. 33, 34) de- scribes six rhombomeres in the guinea-pig. The six described correspond perfectly with rhombomeres 1to 6 of the rat, his sixth rhombomere being related to the IX nerve. He states that the neural tube has a uniform contour posterior to the sixth rhombomere, but a model would possibly have revealed a seventh rhombomere between Chiarugi’s sixth and the first somite. Meek (’10) finds eight rhombomeres in the rabbit. He finds three rhombomeres related to the IX-X nerves. His rhombomeres 1to 5 are identical with the corresponding ones of the rat. Volker (’22) reports that eight are macroscopically observable in the ground-squirrel (Spermophilus citillus). His description disagrees with mine in assigning the trigeminus to the third instead of the second rhombomere. Valker states, however, that his rhombomeres 1 and 2 are recognizable in sections “nur bei einiger Aufmerksamkeit.” I have made no special study of the rhombomeres beyond the 26-somite stage.

At 26 somites the midbrain is fairly extensive, showing two faintly marked mesencephalic segments. Diencephalon and telencephalon are well marked and require no special description.

I now turn to a description of younger stages, in an at- tempt to show the gradual differentiation of the regions above outlined. A brief description of two young embryos, one of 1somite and another of 2 to 3 somites, will serve to introduce the description of a 5-somite embryo which marks the real starting-point of our study. In a 1-somite embryo (fig. 7) the neural folds have just begun to elevate. The folds diverge somewhat caudally. At both extremities they gradually subside to the level of the blastodisc. At the apices of the folds there is, as yet, no delimitation of neural from somatic material, although in the most elevated regions the arrangement of the cells suggests a future line of cleavage.

In a 2-to-3-somite embryo (fig. 8) marked expansion of the neural plate has occurred. Forward growth and expansion has resulted in the formation of a short head fold into which the foregut extends. The elevation of the anterior end of the embryo is unquestionably in the nature of an overgrowth of more ventrally lying parts, initiating a growth process which for a long time continues to characterize the development of the anterior end of the head. In certain sections through this embryo a definite cleft has appeared marking the boundary of neural plate and ectoderm, but as a rule this is not prominent until somewhat later. The two embryos just described should be compared with those figured by Parodi and Widakowich ( ’20).

The 5-somite embryo (figs. 10, 11) is most important for the purposes of this study. In this specimen the head region has grown enormously as contrasted with the preceding stage. The medullary plate is greatly expanded anteriorly, but the neural groove is relatively shallower than in the 2-to-3-somite embryo. The most interesting feature is the sharp ventral bend of the cephalic end of the medullary plate, so that the most anterior region of the plate is directed at right angles to the more caudal portion. Urith respect to this bending of the neural plate, the rat stands in marked contrast to the human embryo, where in early stages the neural plate shows no pronounced flexure (cf. figs. 3 and 4 of Bartelmez, '32). As might be expected, the spermophile (Volker, '22) seems similar to the rat in this respect, and the condition is approximated in the sheep (cf. Neumayer, '99, '06), and pig (Keibel, '96), being much more marked and occurring more preco- ciously in the rat, however. It is without doubt an expres- sion of great forward growth and expansion in restricted quarters. The anterior edge of the medullary plate is some- what recurved to form a rather prominent lip or ridge, which becomes less evident as development progresses.

The perpendicular anterior face of the neural plate has on each side a very shallow depression (fig. lo), probably the earliest indications of the optic foveae: This is the only one of many 5-somite embryos in which the optic foveae have started their development, and in spite of the fact that transverse sections are not in general favorable for the study of shallow depressions so situated, a careful study of this particular series has convinced me that the optic pits here shown are not artifacts. From the same aspect one can also see a marked deepening of the neural groove anteriorly, but not affecting the extreme cephalic end of the neural plate. It is bounded on each side by eminences which form the summit of the bend of the neural plate. This is the primitive infun- dibulum.

In the dorsal view of this embryo reproduced in figure 11, a well-marked groove is shown extending across the neural plate. I have designated this the preotic sulcus, since it lies just ahead of the otic expansion of' the neural plate. This preotic sulcus will be shown subsequently to mark the site of the third rhombomere. The grooves of the two sides end in a slight depression medially.

The medullary plate is widest anterior to the preotic sulcus. Posterior to it there is a conspicuous expansion marking the site of the otic rhombomere (Rh.4). Figure 11 shows the marked elevation of the neural plate anterior to the pre- otic sulcus and the sharp declivity posterior to it in the region of the otic rhombomere. A shallow postotic groove bounds the otic rhombomere caudally. The interval between the postotic groove and the anterior margin of the first somite is small (fig. 1). It is still smaller at 3 somites (fig. 22). There is some doubt in my mind as to whether one has the right to designate as rhombomere C this territory, showing no expansion, and as yet none of the characters of a rhombomere.

Sections through the region of the otic rhombomere (fig. 23) show a marked thickening of the somatic ectoderm which is probably the a d a g e of the otic placode. It is impossible to delimit it absolutely from the thickened ectoderm in the territory of the future first gill arch. Its approximate extent is shown in figure 1.

Between 5 and 6 somites a marked elevation of the cephalic regions has occurred (fig. 12). One notes, however, that while the anterior, perpendicular face of the neural plate has expanded somewhat and the optic pits have deepened, there has been no appreciable growth of that portion of the neural plate lying between the rostra1 flexure and the preotic sulcus. The ‘wave’ of expansion has now progressed caudally, affecting principally at this time the region lying between the preotic sulcus and the anterior boundary of the first somite, so that in the 6-somite embryo its extent is almost three times as great as in the 5-somite embryo.

The optic foveae are now broad, shallow depressions. The infundibular groove is somewhat more vertical in position than at 5 somitea, but it has not deepened especially. The pre-otic sulci meet medially in a shallow, but well-defined pre-otic pit, and, as previously, the neural plate returns rapidly to the general level of the blastoderm caudal to this point. The declivity affects almost the entire region between the preotic sulcus and the first somite. The expansion of the otic rhombomere is pronounced, but a postotic sulcus cannot be detected bounding it caudally. The plane of section (Sagittal) is, moreover, such as would not obscure such a sulcus if present. As far as the plane of section allows one to judge, the otic placode corresponds approximately with the otic rhombomere, extending somewhat ahead of its anterior boundary.

Fig. 1 A plotting, to scale (xloo), of tlie dorsal aspect of the neural plate of a 5-somite rat embryo (Ser. 110), showing the prospective subdivisions of the neural plate. The rostra1 neural crest is shown in stipple, extending along the margin of the prospective midbrain and rhombomere A,. The extent of the otic placode is indicated by a bracket. An arrow marks the level of the first somite.

The 8-somite (figs. 13 to 15) embryo shows marked ad- vance in the expansion and elevation of the head region. The optic pits have deepened considerably and the lateral borders of the neural plate in this region have begun to swing medially, initiating the closure of the neural tube. Forward and downward growth of the material of the anterior portion of the neural plate has resulted in a significant change. The two eminences previously spoken of as bounding the primitive infundibulum have now moved downward and lie slightly above the middle of the anterior face of the neural plate. As a result, the contour of the rostral flexure, viewed dorsally, has been changed markedly (cf. figs. 1 and 11 with 2 and 15).

Fig. 2 A plotting, to scale ( X l00), of the dorsal aspect of the neural plate of an 8-somite rat embryo (Ser. 85a), showing further differentiation of the prospective regions of the neural folds. The ganglionic anlagen are indicated in stipple. The extent of the otic placode is marked by a bracket and the level of the first somite is shown by the arrow. I n studying figures 1 and 2 it should be appreciated that the anterior perpendicular portion of the neural plate is not shown. See figures 10, 11, and 13 for comparison.

G.V., ganglionic crest of trigeminal ganglion; G.VII-VIII, acoustico-facial ganglion; G.IX-X, ganglionic crest of the glossopharyngeal and vagus ganglia ; Xe., mesencephalon; 0t.pZ., otic placode ; ah., rhombomere ; R.n.c., rostral neural crest, 8.1,level of first somite; Sp.n.c., spinal neural crest.

The preotic sulcus is prominent. Corresponding to it there is a ridge on the ventral surface of the neural plate (fig. 14), which runs slightly cephalad as one proceeds from the lateral margin of the neural plate toward the mid-line. Anterior to the sulcus lies the proliferation for the V ganglion, which has a much less extensive attachment to the neural plate than in the 5- or 6-somite embryo - a fact to which more attention will be devoted later. On the right side there is a shallow sulcus at the boundary between neural and somatic ectoderm, marking externally the site of the V anlage. Similar neuro-ectodermal sulci mark the position of the VTI-VIII and IX-X anlagen on the right side, but on the left only the IX-X anlage produces one.

The otic rhombomere is marked and there is a broad post- otic depression on the right. On the left side, however, while the expansion is more pronounced, no postotic sulcus can be detected and the otic rhombomere is not so clearly sepa- rable from the more caudal regions. Related to this rhombomere are the cristal proliferation for the VII-VIII ganglion and otic placode. The latter extends caudally beyond the territory of the otic rhombomere to the level of the IX-X anlage; it shows a slight invagination (fig. 27), which is, however, an artifact. There is an absolute break in the neural crest in the region of the preotic sulcus and another for eight sections caudal to the acoustico-facial anlage, probably mark- ing the site of rhombomere 5. The IX-X ganglionic anlage is directly continuous caudally with the spinal neural crest.

In the 9-somite embryo (fig.3) it is possible to establish the cephalic limit of the hindbrain. The embryo from which figure 3 was constructed is cut frontally - a favorable plane for a study of the subdivisions of the neural folds. Figure 20 is a photograph of a section through the hindbrain, showing the relations of rhombomeres 1 to 5. Just caudal to the midbrain there is a broad, shallow depression involving the entire extent of rhombomere A, and comprising secondary sulci related to external rhombomeric swellings. On the right there are two rhombomeres related to it, the smaller caudal one, free from neural crest, is rhombomere 3, while the broader cephalic swelling is rhombomere A,, which later divides into rhombomeres 1and 2. The double nature of this rhombomere is shown on the left, where two swellings are evident anterior to rhombomere 3, and there are indications of two shallow internal sulci corresponding to them. Bartelmez ( ’23) records evidence of subdivision of rhombomere A, in human embryos from the 14-somite stage on. The fifth anlage is attached to rhombomere A, on the right and to hombomeres 1 and 2 on the left. I n this embryo, then, the boundary between hindbrain and midbrain may be definitely determined at the anterior limit of rhombomere A,.

Fig. 3 Drnwing from a model ( X 100) of a rat embryo of 9 somites (Ser. 223), to show the subdivisions of the neural folds. The extent of the V, VII-VIII ganglia, and the otic placode is indicated by broken lines. The plane of section (frontal) was not favorable for determining the exact anterior or ventral limits of the IX - X ganglionic anlage, hence it is not shown here. It begins a very short distance caudal to the otic placode and extends caudally to become con- tinuous with the spinal neural crest at the level of the first somite. A good idea of its ventral extent cnn he obtained from figure 71, which is a cross-section through the IX-X anlage of an embryo of the same age. The neural folds are entirely open anterior to the level of the fourth somite, gaping most widely in region of mesencephalon and rliombomere A,. The position of the ventral lip of the neuropore is marked by an asterisk. A section of this embryo is given in figure 20.

Di.,diencephalon ; Di-me., di-mesencephalic boundary; G., ganglion ; M., mesencephalic ‘segment’; Me.-Rh., boundary between mesencephalon and rhombencephalon; Op.zi., optic vesicle; Ot.pZ., otic placode; Pr.inf., primitive infundibulum; Rh., rhombomere; 8.1, first somite; Te., telencephalon.

While the external swelling for rhombomere 4 is promi- nent, there is practically no indication of an internal sulcus corresponding to it. The fifth subdivision is a gentle swelling free from neural crest (excepting, possibly, a small portion caudally), and not yet well defined caudally. From the region lying between its caudal border and the first somite the sixth and seventh rhombomeres will arise. The otic placode is still an extensive thickening covering the terri- tory of the fourth andmost of the fifth rhombomeres. Since the plane of section was not favorable for an accurate plotting, the IX-X proliferation is not shown in figure 3. It extends from the caudal border of the otic placode caudally to become continuous with the spinal neural crest.

The midbrain is interesting. The di-mesencephalic bound- ary lies along the line of the rostral flexure, and from this level the midbrain extends caudally for some distance. There are two mesencephalic 'segments' plainly visible, each marked internally by a broad, shallow sulcus. Chiarugi ( '22) finds a similar number of segments in the midbrain of the guinea-pig.

In this embryo closure of the neural folds has not occurred anterior to the level of the fourth somite, but in a 10-somite embryo the folds have approximated and are about to fuse as far cephalad as the anterior border of rhombomere 5. At 10 somites the nearal folds of the hindbrain anterior to this point and the entire midbrain are still widely open, gaping most markedly in the region of the midbrain. In the fore-brain region the folds approach, but have not fused.

There are few significant changes in the 10-somite embryo (fig. 16). The di-mesencephalic boundary which has ap- peared along the line of the rostral flexure of the 8-somite embryo (cf. figs. 3, 14, and 16) is unmistakable. Two mesencephalic segments are very prominent. Rhombomere A, marks the widest part of the hindbrain. Its doable nature is attested by the presence of two shallow sulci related to it internally (fig. 21). The otic rhombomere shows the mid-ventral swelling which is so characteristic of it. On the left side it possesses an atypical dorso-caudal swelling to which the VII-VIII anlage is attached, and this atypical swelling has an internal sulcus related to it. On the right side the rhombomere is typical. Rhombomere 5 is rather indistinct on the left side. The otic placode is invaginated slightly in the 10-somite embryo, the anterior lip of the pit overlying the VII-VIII ganglion. Its extent is indicated in the figure.

In the 14-somite embryo (fig. 17) the forebrain is distinctly differentiated into telencephalon and diencephalon, and the dimesencephalic boundary is so obvious as to require no comment. The midbrain shows no evidence of segments, possibly because the plane of section was not favorable for their demonstration in the model. I have examined sagittal and frontal sections of other 14-somite embryos where they also seem to be absent. Strangely enough, there are faint in- dications of two mesencephalic ‘segments’ in both the 18- and 26-somite embryos. In a 14-somite embryo sectioned sagittally the floor of the midbrain shows a marked bend which may possibly mark the inter-mesomeric boundary, but certainly there are no marked lateral swellings of the mid- brain in any of the 12-to-14-somite embryos I have examined.

It will be convenient to begin the description of the hind-brain with the preotic rhombomere 3 which is well marked, but which does not extend to the midventral line. Rhombomere 2, the trigeminal rhombomere, is narrow and also dis- appears before the mid-ventral line is reached. Rhombomere 1is difficult to delimit. At 14 somites it is only a slight swelling with a very shallow internal sulcus. While not prominent, it can be demonstrated in favorable frontal and sagittal sections. It will be remembered that it is split off from the anterior portion of rhombomere A,, which early shows its double character. In frontal section it is separated from the midbrain anteriorly and rhombomere 2 posteriorly by shallow grooves. Although it is inconspicuous at 14 somites, it rapidly expands until at 18 somites it is easily recognizable, and I have no doubt that if a fixer with greater shrinking properties than picro-aceto-formol were employed it would be more conspicuous at 14 somites. The trigeminal anlage extends along the side of rhombomeres 1 and 2, but has lost its attachment to rhombomere 1 and is closely applied to the neural tube only in the region of the second hindbrain ‘segment.’ The otic rhombomere to which the VII- VIIT anlage is attached shows a typical midventral swelling and is more extensive ventrally than dorsally. Postotic rhombomere 5 is wedge-shaped, more expanded dorsally than ventrally, and is free of nervous attachments. Rhombomeres G and 7 are apparently present, although a transverse plane is not favorable for the demonstration of such slight swell- ings. However, there are broad, shallow internal sulci cor- responding to the rhombomeres indicated in the figure. Rhombomere 6 (if I am correct in so calling it) is more extensive than 7. In later embryos the last rhombomere expands greatly and becomes most extensive of all. The pro- liferation of the neural crest for the IX-X nerves begins immediately caudal to rhombomere 5 and is continuous with the spinal neural crest. The otic pit has a prominent an- terior lip of thickened ectoderm which overlies the VTI-VIII ganglion. Figure 53, a frontal section of another 14-somite embryo, illustrates many of the above statements.

I n the 18-somite rat (fig. 18) the rhombomeres have reached their full development and are similar jn all essentials to those described in the %somite embryo. Rhombomere 1 is now distinct, having expanded considerably in the interval between 14 and 18 somites. The internal sulcus corresponding to this ‘segment’ is broad, but shallow even when best developed. It will be noted that the otic vesicle has not yet been completely constricted off from the overlying ectoderm.

The foregoing descriptions will perhaps serve to bring out the following facts :

  1. As Bartelmez (’23) has pointed out in the human embryo, so also in the rat, the expansion of the neural plate marking the site of the otic rhombomere is from early stages a prominent landmark with characteristic relations to the VII-VIII anlage and the otic placode. The proliferation of neural crest related to this rhombomere is first found in embryos of 8 somites, but the position of the otic rhombomere is indicated by an expansion of the neural plate at least as early as the 3-to-4-somite stage (fig. 22).
  2. A second landmark, appearing simultaneously with the otic rhombomeric expansion (fig. 22) is the preotic sulcus. The latter is situated between the otic rhombomere and the caudal edge of the V anlage and marks the position of rhom- bomere 3. From the beginning, the margin of the neural plate corresponding to the preotic sulcus is free from neural crest, so that the ‘crest-free’ condition of rhombomere 3 would thus seem to be a primary condition in the rat.
  3. At 9 somites, rhombomere A, (rhombomeres 1 and a), involving that portion of the neural folds related to the V anlage, has appeared anterior to rhombomere 3. This makes it possible to fix accurately the boundary between midbrain and hindbrain. The V anlage is related to the entire extent of rhombomere A, in embryos of 9 and 10 somites, but with the subdivision of this segment into rhombomeres 1 and 2 at fourteen somites, we find that the trigeminal anlage has lost its attachment to the first segment and is adherent only to the second rhombomere - its definitive relationship.
  4. The postotic region of the neural plate anterior to the first somite is extremely small at 5 somites and has expanded somewhat at 8 somites, but with subsequent growth furnishes the material for rhombomeres 5, 6, 7. Since the postotic sulcus is not a very definite structure in the rat, it is hard to determine accurately the anterior limit of this territory in young embryos.
  5. The di-mesencephalic boundary is clearly defined at 9 somites. Comparison of the 8-, 9-, and 10-somite embryos shows that the di-mesencephalic boundary of the 9- and 10- somite embryos lies approximately along the line of the rostra1 flexure of the 8-somite embryo.

The question oP the delimitation of the forebrain and mid- brain in the 5-and 8-somite embryos may now be considered. Figures 1and 2 are outline sketches of the dorsal aspects of models of 5- and 8-somite embryos, suggesting the probable subdivisions of the early neural plate in the rat. The positions of the ganglionic anlagen have been indicated by stippling and the extent of the otic placode is shown.

Let us first fix the anterior limit of the hindbrain in the 8-somite embryo. In this specimen rhombomere 3 is represented by the pre-otic sulcns. Its direction is oblique, running slightly cephalad as it passes from tlie lateral margin of the neural plate toward the midline. The region of the prospec- tive rhombomere A,, the anterior margin of which marks the rostral limit of the hindbrain, must lie anterior to it. Now since we have seen that the anlage of the trigeminus ganglion is coextensive with rhombomere A, in 9- and 10- somite embryos, and since the V adage is about equal in extent in 8- and 9-somite embryos, it is probably not far from correct to consider that the anterior limit of the V proliferation of the 8-somite rat marks the approximate anterior limit of the prospective rhomhomere 9,and hence the ceph- alic boundary of the hindbrain. There is a ridge on the ventral surface of the neural plate which marks the course of the preotic sulcus, and just ahead of it there is a groove (cf. fig. 14) about as wide as the V anlage, which runs parallel to the ridge just described, and like it runs forward as it approaches the mid-line. The line which I have drawn to mark the anterior limit of the prospective rhombomere A, of the 8-somite embryo runs along the anterior margin of this groove and parallels the course of the preotic sulcus.

One can be less sure of the anterior limit of the hindbrain in tlie 5-somite embryo. Tlie preotic sulcus and otic rhombomere are definite and convenient landmarks. The rostral neural crest (V anlage) is much more extensive than at 8 somites, reaching from a point immediately anterior to the pre-otic sulcus to the rostral flexure of the neural plate.

  1. Since the completion of this work, I have had the opportunity of examining the manuscript of Bartelmez and Evans’ (’25) significant monograph on “The development of the human embryo during the period of somite formation, including embryos with 2 to 16 pairs of somites,” in which they deal exhaustively with the development of the neural folds and cranial ganglia. The exchange of manuscripts was effected through the kindness of Prof. C. J. Herrick. Footnotes will call attention to comparisons made in the course of the paper.
  2. Bartelmez (’25) now believes that rhombomeres 3 and 4 appear at first as a single ‘segment’ (rhombomere B ).

Cite this page: Hill, M.A. (2021, September 19) Embryology Paper - The development of the neural folds and cranial ganglia of the rat. Retrieved from

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