Paper - The development of the anterior post-otic somites in the rabbit
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Hunter RM. The development of the anterior post-otic somites in the rabbit. (1935) J. Morphology, 57(2): 501-529.
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- 1 The Development of the Anterior Post-Otic Somites in the Rabbit
The Development of the Anterior Post-Otic Somites in the Rabbit
Ruth MacMillan Hunter
Department Of Histology And Embryology, Cornell University, Ithaca, New Y Ark
Four Plates (Twenty-Nine Figures)
A study is presented of the most anterior post-otic somites in a series of embryos from the five-somite stage to 16 days. A gradual fading out of the somite forming tendency in this region seems to be indicated both by the formation of a rudimentary somite and by conditions found in the first true somites.
There are, in the rabbit, three occipital somites, all of which form myotomes. The fate of the myotomes is traced until their identity is lost in the formation of deﬁnitive muscle masses.
From the sclerotomes two occipital arche, comparable to those of vertebrae, are formed and can be identiﬁed as late as the time of beginning chondriﬂcation. There is a marked compression of the tissues in this region, the sclerotomal material being not only relatively but actually horter in older embryos. This compression results in, 1) the approximation of the hypoglossal roots, and, 2) the fusion of the two occipital arches.
The cartilaginous basal plate in rabbits begins development at its caudal end and differentiates anteriorly from this with little evidence of a primitive segmentation except as this posterior ﬂrst center might be called a segment.
Ever since the early nineteenth century, when Goethe and Oken disputed the honor of first stating the vertebral theory of the skull, scientists have been actively interested in the idea of the segmental nature of this portion of the animal body. Huxley, who attacked the vertebral theory of the skull in 1858, believed, as a result of his study of the ontogeny of the skull of elasmobranchs that the early segmentation of the mesoderm extended only as far anteriorly as the posterior limit of the skull and stated that “no trace of such segmentation has been observed in the head itself.”
Gegenbaur (1872), Froriep (1882), and Fiirbringer (1897), all interested in the phylogeny of the skull, considered it to be made up of two regions, an anterior prechordal or prevertebral unsegmented region and a posterior region in _which segmentation was evident. Both Froriep and Fiirbringer considered the vagus nerve to be the anterior boundary of the segmented region of the skull. The phylogenetic signiﬁcance of these observations will not be considered in this paper, as it has been my intention to not enter that discussion at all, but rather to trace in one form, a mammal, what has happened in ontogeny, to determine how many somites are involved in the development of the occipital region and to trace as deﬁnitely as possible their fate in relation to the formation of the basi-occipital cartilage.
The number of myotomes present, the number of hypoglossal nerve roots, and the development of sclerotomes into occipital cartilage have all contributed evidence for the determination of the number of occipital segments. In mammals three occipital myotomes have been reported for sheep and cow (Froriep, 1882 and 1886), human (Mall, 189]), rabbit (Chiarugi, 1890), and rat (Butcher, ’29). Froriep, in ruminants, Mall, in man, and Weiss, in rat (’01), reported three hypoglossal roots, while Chiarugi reported four such nerve roots in the rabbit and because of this considered the occipital region to be composed of four segments. Froriep, in a consideration of the formation of the occipital cartilage in cow embryos, found the only evidence of sclerotomal segmentation in lateral extensions present between successive myotomes. Most workers have recognized one occipital vertebra, but have seen no segmentation ahead of this, except that indicated by the position of the hypoglossal nerve roots. Jager (’24), in the chick, however, has demonstrated two very clear occipital segments which form deﬁnite arches and bodies before losing their identity. It was principally to demonstrate in a mammal, as Jager has done in a bird, any evidence of segmentation in the development of the cartilage from sclerotome in this region that this work was undertaken.
- I wish at this time to thank Prof. J. P. Hill, of Univerity College, London, for his generosity and friendly help. It was in his laboratory that this research was begun. The major part of the work was done at Cornell University, Ithaca, New York, under the upervision of Profs. B. F. Kingsbury and H. B. Adelmann. I want to express my appreciation of their help and criticism, and also to thank Prof. J. L. Bremer, who very kindly loaned me embryos from the Harvard Embryological Collection, many of which were those used in the compilation of the Normentafeln by Keibel and Taylor.
Rudimentary Somite Formation
Two main points of disagreement result in a considerable confusion in the literature dealing with the nature and fate of the most anterior somite. Williams (’10) calls the mesodermal material immediately anterior to the most cephalic intersomitic cleft somite 1 and believes that, in the chick, it gives rise to the most anterior myotome. Rex (’05), on the other hand, believes that in the gull the material ahead of the most anterior cleft varies in both its relations and degree of development and in many cases breaks up into mesenchyme without ever differentiating into dermatome, myotome and sclerotome. He, therefore, referred to this material as a rudimentary somite, using the term somite 1 to apply to the next block of tissue, the most anterior paraxial mesoderm to form a deﬁnite myotome. Butcher (’29) ﬁnds in the rat conditions comparable to those Rex described in the gull, that is, he reports that the material anterior to the ﬁrst cleft beaks up without forming a myotome. His terminology, however, is different from that used by Rex in that he calls this material somite 1, although he refers to it as rudimentary, describes it as involuting at about the 7-somite stage, and compares it to the structure Rex found dedifferentiating at about the same stage. I have, in this paper, followed the numbering system of Rex which seems to me less confusing especially in comparing embryos of diﬁerent ages. Furthermore, the posterior end of the unsegmented mesodem anterior to the ﬁrst intersomitic cleft does not, in the rabbit, exhibit a structure sufficiently well developed and constant enough to deserve classiﬁcation as a true somite.
In a study of this region we must rely almost exclusively upon sagittal series for our decisive evidence. Because of this fact, I will consider ﬁrst those embryos cut in sagittal section and refer later to those cut transversely. A series of photographs are presented to show conditions in the development in the rabbit of somite 1 and the mesoderm ahead of it. The youngest embryo of this series (ﬁg. 4) is one in which 5 somites are preent. Somite 1, although slightly smaller than the four caudal to it, is completely organized as a somite. While there is no wide cleft in front of it such as can be seen between somites 2 and 3 and those more caudal, nevertheless, the cells on its cephalic side are deﬁnitely arranged with relation to its center and are not merely continuous with the mesoderm ahead. Between somites 1 and 2 there is a connecting band of cells which does not, however, affect the organization of either somite. Ahead of somite 1 there is no evidence of segmentation nor is there the slightest sign of an epithelial arrangement of the cells.
The next embryo photographed, a particularly interesting one, was, unfortunately, sectioned in two pieces, the posterior part transversely and the anterior sagittally, so that it was diﬁicult to determine exactly the number of somites present. There seemed to be seven, subject to error, however, as some material between the two pieces may have been lost. As can be seen in the section photographed (ﬁg. 5), the ﬁrst true somite has a myocoele and complete anterior wall, although it is very intimately associated with the mesoderm ahead of it. The unsegmented mesoderm is simlar to that in some of Rex’s pictures. Immediately in front of somite 1 it is thickened in the dorso-ventral direction and for about the length of two somites is markedly condensed. Neither this nor any other of the sagittal series which I examined showed any epithelial arrangement of the cells ahead of somite 1 as Rex frequently found in the gull. It was, however, evident in several of the transversely cut series, which I will describe later, and as this is apparently a variable and transitory condition I consider it merely coincident that it was not present in any one of those cut sagittally.
One possible explanation for the difference in appearance of the 5-somite embryo of ﬁgure 4 and the 7-somite one of ﬁgure 5 is that the somite 1 of the younger embryo is in the later embryo undergoing dedifferentiation and that the most anterior complete somite of the older stage (the most cephalic one possessing a myocoele) is, in reality, the somite‘ 2 of the younger embryo. This possibility seems unlikely in view of the fact that I have not been able to ﬁnd any stages which might be considered intermediate between the condition of the unsegmented mesoderm in ﬁgure 5 and so far advanced a somite as the ﬁrst one of ﬁgure 4. The epithelial arrangement, when present, was always suggestive of a much smaller somite, as can be seen by comparison of ﬁgures 9 and 11, transverse sections of the rudimentary somite with ﬁgures 7 and 12 of the ﬁrst true somites of the same embryos. It seems to me more likely that ﬁgures 4 and 5 represent merely different expressions of the potentialities of the mesoderm ahead of the region of true segmentation. In fact, this mesoderm in ﬁgure 5 is even suggestive of the formation of two segments ahead of somite 1, the anterior boundary of the ﬁrst being indicated by the slight depression labeled r. Both anterior and posterior to this depression the mesoderm is markedly condensed and it is possible that this condensation may be an abortive attempt at somite formation which has appeared after the organization of somite 1.
The next embryo ﬁgured (ﬁg. 6) in which the ninth somite is being formed, presents another variation of the organization of this anterior mesoderm. When compared with the other embryos already mentioned, there is no reason, judging from its size and degree of development, to consider the most anterior somite here anything other than the structure which I have called somite 1 in the others. It is different, however, in having a very incomplete cephalic wall, and in not being separated from the mesoderm ahead of it. I have indicated by s what I consider to be the most anterior limit of somite 1 and by r the anterior limit of the condensation of the mesoderm ahead of somite 1. This condensation between s and r is, I believe, the same rudimentary somite which was present in the embryo of ﬁgure 5. Only, in this case, it has taken a slightly different form and is more broadly continuous with somite 1 as well as with the looser mesoderm ahead.
Rex, in his analysis of this region, thought of the mesoderm ahead of somite 1 as expressing the forward spread of the segmentation impulse beyond the material actually out up into somitic blocks. Since this work of Rex, Harrison and other investigators using experimental methods have shown that organ formation in the embryo is often associated with a high center of potency gradually fading off in all directions. Harrison (’18) concluded from his experiments on the fore limb of Amblystoma that the limb rudiment may be regarded not as a deﬁnitely circumscribed area, like a stone in a mosaic, but as a center of differentiation in which the intensity of the procss gradually diminishes as the distance from the center increases until it passes away into an indifferent region. Many other systems seem to have the same indeﬁnite boundaries which may even overlap one another.
It is possible that this same principle applies to the formation of somites as well as to that of the limb buds, and, judging from what has been shown to be true of other developmental tendencies, it seems probable that Rex’ theory was correct and improbable that the tendency to somite formation should stop abruptly at either the anterior boundary of the ﬁrst somite or the posterior boundary of the last. This theory is further supported by the work of Butcher, who found, in the rat, not only a rudimentary somite anterior to the ﬁrst myotomeforming somite, but also what he termed the mesodermal rudiment caudal to the last intersomitic cleft. This mesodermal rudiment he found exhibited a differentiation which resembled that of the cephalic rudimentary somite with no complete somite formed. It, therefore, seems reasonable to interpret these different appearances at the critical region of transition from segmented to unsegmented mesoderm as weak attempts at segmentation resulting sometimes in what Rex has designated as a rudimentary somite. Conditions in the rabbit are very similar to those which Rex described in the gull, where he found this material immediately in front of somite 1 either cut off from the mesoderm ahead and attached to somite 1 or remaining in more or less intimate relation to the mesoderm ahead.
In the embryos which I examined the somite-forming tendency anterior to the ﬁrst true somite is best shown in those of ﬁgures 5 and 6. In the ﬁrst, the characteristic condensation extends further cephalically and the separation between somite 1 and the rudimentary somite is greater. In the second, on the other hand, the condensation ahead of somite 1 is more limited and its relation to that somite more intimate. This difference may be due partly to the dilference in age of the two embryos, but is more probably due chieﬂy to the fact that the expression of this fading out of potency Varies in different individuals and even in the two sides of the same individual as Rex pointed out to be true in the gull and as is also the case in the rabbit.
Embryos out transversely also give evidence of attempted somite formation ahead of somite 1. Rabbits of from 5 to 8 somites showed the greatest development of this rudimentary somite. My inability to ﬁnd it in younger embryos may be merely due to the scarcity of material and the fact that I did not happen to have the right specimen, or it may be indicative of its tardiness to develop. In any case, in very young embryos, where the somites are all small, it is very difficult to distinguish with certainty between somite 1 and a rudimentary somite.
Figures 7 through 13 show the conditions present in the anterior portion of the paraxial mesoderm of two transversely cut embryos of 6 somites. In both there is a clear epithelial arrangement of the cells ahead of somite 1 (ﬁgs. 9 and 11). This organization forms a much smaller structure than the ﬁrst true somites of the same embryos (ﬁgs. 7 and 12). Not only is it much smaller in width, but it is also present in only two or three sections as compared with the seven to ten sections of the true somites. In some other slightly older embryos studied the suggestion of a rudimentary somite is much less evident. One cannot be certain whether the attempt at somite formation is almost over or has never been very strong in these particular embryos.. Although 5- to 8-somite embryos have this rudimentary somite more frequently than those of other ages, it is not present in all cases (ﬁg. 4)~a phenomenon not unusual in the case of any rudimentary structure.
Early Differentiation of Anterior Somites
This fading out of the somite forming tendency at the anterior end of the post-otic mesoderm is expressed in the development of the most anterior true somites as well as in the condition of the more cephalic mesoderm. As already mentioned, Williams thought that, in the chick, the ﬁrst somite gives rise to only half as much muscle and mesenchyme as those following. Other workers have also observed that the most anterior somite is noticeably smaller than those caudal to it, especially by the time its myotome is formed. This same size relation is shown in the rabbit. In young stages this difference in size, like the degree of development of the rudimentary somite just discussed, varies in different individuals. After the sclerotome begins to form it is diﬁicult to compare the sizes of somites until all those in question are equally broken up and concerned in the formation of myotome and sclerotome. In the embryos examined in which sclerotome formation had not yet begun there was a variation in the comparative sizes of somites 1 and 2 which was not correlated with the somite age of the embryos. Figures 4, 12 and 13 show only slight variation if any in the size of these two somites, while in other embryos not ﬁgured somite 2 is sometimes much larger than 1. and contains a larger myocoele. In some embryos of these same ages both somites 1 and 2 were smaller than those following, thus indicating, as might be expected some variation in the fading out tendency.
Another peculiarity of these anterior somites is the frequent presence between 1 and 2 of a continuous band of cells which have apparently not been separated by the cleft (ﬁg. 4). In some embryos this band is present only between somites 1 and 2, in others also between 2 and 3 and in one transversely cut 4- to 5-somite embryo even the last two somites seemed to have a slight connection on the left side. This band when present was always at the median border of the somite (ﬁg. 14). This lack of complete separation of the anterior somites might be interpreted as another expression of the fading out of potency in this region, or of the cephalo-caudal differentiation of somites, which Williams found in the chick and Butcher in the rat, resulting in a more complete separation of more caudal somites.
Later Differentiation of Occipital Somites
Differentiation of somites into dermatome, myotome, and sclerotome begins in rabbit embryos of 10 to 11 somites with the ventral migration of sclerotomal mesenchyme from somite 1 (ﬁg. 15) ‘and proceeds caudally. By the time 23 somites are cut off the notochord in the regions of the anterior somites is surrounded by mesenchyme, although there is as yet no condensation of it. As the mesenchyme move ventrally from the somites its segmental origin is somewhat obscured, although still visible in the more lateral region where the posterior half of each sclerotomal segment is more condensed than the anterior. The sclerotome of the ﬁrst somite is intimately associated with the mesenchyme ahead of it and with that of somite 2. I was never able to distinguish in it any separation into looser anterior and denser posterior regions. In a 23somite embryo this division in the sclerotome of the second somite is ﬁrst apparent more by the presence of a very narrow cleft of von Ebner (ﬁg. 16) than by any noticeable difference in the density of the two regions. These sclerotomal divisions later become much more distinct and are of great aid in tracing the fate of the individual somites.
The lack of any distinct posterior head boundary in these early stages makes the determination of the constituents of the somitic portion of the skull very diﬂicult. Not until the spinal neural crest has differentiated into ganglia is there any visible distinction between occipital and cervical regions. Even after these ganglia are present the individual as well as species variation of the ﬁrst cervical and hypoglossal ganglia (Froriep and Beck, 1895) presents an added difficulty.
Only when the boundary between atlas and occipital arches is clearly indicated can one be certain of the posterior extent of the head. At this stage, however, both myotomes and sclerotomes have been so reorganized that it is impossible, without careful examination of the intervening stages, to ascertain the relation of the sclerotomes present to the somites found in earlier embryos. An important aid in tracing the fate of these anterior somites is given by the nerves of the region, the anterior cervicals and the hypoglossal as well as the vagus.
Froriep (1882), in a study of the development of the hypoglossal nerve of sheep, found that it was formed from three ventral roots, the most caudal of which had associated with it a dorsal root and ganglion. This ganglion was considerably smaller than those of the spinal nerves and superﬁcial to those of the vagal complex. His (1888) later found this same ganglion in man and in lower animals and named it after its discoverer Froriep’s ganglion. The presence of even more anterior clumps of crest cells as well as great variation in the development of this ganglion and that of the ﬁrst cervical nerve has led to considerable discussion as to both the phylogenetic and the ontogenetic signiﬁcance of these conditions. His study of this region led Chiarugi (1890) to deﬁne the occipital region of the skull as “a fragment of the trunk which is fused with that which is in front of it and which has modiﬁed its characters in a manner such that in the late stages of development and in the adult one cannot recognize the primitive condition.”
Froriep and Beck (1895) examined sixty-one species of ﬁfteen classes of mammals including man and found all degrees of development of the dorsal root and ganglion of both the ﬁrst cervical nerve and the hypoglossal. Their conclusion was that the hypoglossal, although in many cases composed of only ventral roots, is essentially a spinal nerve complex. In the rabbit, of which they examined eight individuals, they found the dorsal hypoglossal roots always lacking and those of the ﬁrst cervical nerve always well developed. Chiarugi describes in rabbit embryos two rudimentary dorsal roots of the hypoglossal nerve in addition to the four ventral ones.
In the rabbit embryos which I examined the ventral rootlets of the twelfth cranial nerve are first grouped into three roots, one at the level of each of the three anterior somites. In only one case did I see a fourth and more anterior root associated with material ahead of the ﬁrst somite. None of these ventral roots had accompanying dorsal roots. However, there were in most cases dorsal clumps of neural crest cells at the level of the third occipital root (Froriep’s ganglion) and scattered crest cells extending some distance cephalically.
At 9.5 days, the tenth cranial ganglion is present close in front of the first somite (figs. 1 and 16). Although in transversely cut embryos of this same age there is a. suggestion of the clumping of the spinal neural crest cells, in embryos which I examined it is not until 10% days that the chain of neural crest cells present between the neural tube and the dorsal part of the medial Wall of the somites can be clearly seen in sagittal section, divided into segmental clumps, the future spinal ganglia, each of which is associated with a somite.
At 10.5 days, the most anterior spinal ganglion is associated with the fourth sclerotome. Although no embryo of this age is ﬁgured, conditions are very slightly altered by 11 days (fig. 2), at which time large spinal ganglia are present associated with the somites behind the third. Figure 17 shows the first ganglion and cephalic to it, at the level of the third somite, a clump of crest cells which are identiﬁed as Froriep’s ganglion. These cells are lateral to the ﬁbers of the accesory nerve and I could not ﬁnd any dorsal root ﬁbers coming from them. Although there are no ganglionic clumps in the regions of somites 1 and 2, there are present scatttered crest cells along the accessory nerve in this region (ﬁg. 2). The most anterior sclerotomal condensation in ﬁgure 17 is the caudal half of somite 2 and ventral nerve rootlets can be seen for some distance ahead of this.
In a 12.5 day embryo the nerves are farther developed but no change great enough to obscure any part of this region has yet occurred (ﬁgs. 3 and 18). The ventral rootlets of the hypoglossal nerve have grown farther ventrad and are grouped into three main roots, one of which is at the level of the anterior half of each sclerotome. Anterior to the ﬁrst somite and to these main roots can be seen another single rootlet. This is probably the ﬁrst root ﬁgured by Chiarugi (1890). I found it in only this one embryo, but this may be a transitory condition in more embryos than those in which it is actually seen. The compression which soon takes place in this region
A usually brings about a fusion of the hypoglossal roots of somites 1 and 2 (ﬁg. 19) and at the same time may add any persistent ﬁbers of this anterior root. That this compression varies in its extent and completeness is shown by the individual variation in number of hypoglossal foramina present in the adult skull of different forms. The presence or absence of this ﬁrst root is probably dependent upon the degree of compression present. In an embryo of 14 days there is a suggestion of the presence of this anterior root (ﬁg. 20), but in a more lateral section of the same embryo (ﬁg. 21) where the nerve roots are traversing the now greatly condensed sclerotomal material only three roots are present, the anterior one being fused with the one next behind it.
In all of these embryos, from those of 10.5 days in which the spinal ganglia were ﬁrst identiﬁed through those of 14 days in which chondrification of the occipital region has begun, essentially the same relations prevail. The tenth cranial nerve bends around the anterior end of the ﬁrst somite. There are three sclerotomes and associated hypoglossal roots ahead of the ﬁrst well-developed dorsal root ganglion. In all there is present at the level of the most posterior of these three sclerotomes an accumlation of neural crest cells which can be identiﬁed as Froriep’s ganglion. In all, the sclerotomal material still shows its segmental history, but in it changes are taking place, the transformation of relatively undifferentiated mesenchy'me into the deﬁnitive structures of skull and vertebral column.
A comparison of sagittal sections at the level of the spinal ganglia of embryos of 12:1; and 14 days (ﬁgs. 18 and 21) shows clearly what is happening. In the younger embryo the dark halves of sclerotomes 2 and 3 are clear, the former being shorter in both cephalo—caudal and dorso-ventral directions. The ﬁrst cervical ganglion, which can be identiﬁed by comparison with older embryos, is well developed and its nerve is traversing the less dense anterior half of the fourth sclerotome. The third and second hypoglossal roots are also traversing the loose. halves of their respective sclerotomes and the ﬁrst occipital root (here present as three converging rootlets and a fourth anterior rootlet) are moving toward the mesenchymal condensation which is destined to form occipital cartilage. The effect of the increased cervical ﬂexure on the direction of growth of these nerve ﬁbers is already shown. The ﬁrst cervical root traverses the sclerotome in a direction almost parallel to the anterior and posterior boundaries of the! somite. The ﬁbers of the third occipital root, however, are moving caudally at their ventral end and are here traversing the denser half of the sclerotome (fig. 3). Streeter (’O4), in describing the development of the hypoglossal nerve in man, says that the hypoglossal and upper cervical nerve fibers start out perpendicularly from the neural tube, but due to the cervical ﬁexure are forced together like the spokes of a wheel. Figures 2 and 3 show this same condition in the rabbit. The same factors which are causing the nerve roots to change their course are also affecting other tissues in the same region. As the nerve roots change their direction they are pushed closer together and at the same time the sclerotomal material of the ﬁrst three somites is compressed. It is interesting to note that this compression results in not only a relative, but also an actual decrease in the cephalo—caudal length of the occipital material (compare figs. 18 and 21). In figure 21 there can be little doubt that the material in front of the ﬁrst ganglion is forming occipital cartilage and that the precartilaginous mass behind the ﬁrst ganglion is the arch of the atlas. Having determined that the ﬁrst well-developed ganglion is on the ﬁrst cervical nerve and that this marks the head-neck boundary, we are now in a position to determine which of the somitic elements are occipital in their destiny. A comparison of reconstructions and photographs of embryos from the first appearance of the somites through the development of occipital cartilage indicates that in the rabbit the three most anterior somites contribute material to the formation of the occipital cartilage and that two arches smaller than, but comparable to those of vertebrae, can be seen in the occipital region as late as the time of beginning chondriﬁcation. Although the sclerotome of the first somite can be traced from the early stages and is unquestionably contributing to the occipital cartilage, it does not form any separate arch.
More diﬂicult to determine than the make-up of the occipital arch is that of the basi-occipital plate. Evidences of segmentation here have been described in birds and mammals. Jager (’24) found, in the chick, two segments at first independent which later fuse with each other and with the unsegmented material ahead to form the basi-occipital cartilage. Terry (’17), in the cat,,describes the basal plate as being derived from a pair of parachordal cartilages andptwo or probably three hypochordal commissures. He considers the developmental processes of the occipital region to be comparable to those of an atypical vertebra, such as the atlas, and places the basal plate in the category of arch structures rather than centra. The atlas he considers to be intermediate in type between that of the typical vertebra and that of the occipital vertebra.
Noordenbos (’O5) described the basal occipital plate in the rabbit as growing forward, without indication of segmentation, from a single center, the point of union of the arches of the two sides. Nor do DeBeer and Woodger (’30) mention any indication of somitic segmentation in the development of the parachordal plates of the rabbit. The fact that, in the rabbit, beginning chondriﬁcation of the occipital arch and a marked compression of the region have occurred before the basal plate is formed considerably obscures the primitive relationships. At the level of the arches, the early condensation of the posterior halves of the sclerotomes makes deﬁnite landmarks by which one can trace the changes of the original sclero-tome into definitive arches. In the median portion, on the other hand, there is very little differentiation previous to the formation of the cartilage.
- 1 In an embryo of 12% days, in the midline in the occipital region there is a slight condensation of mesenchyme around the notochord (ﬁg. 22). There is one localized condensation which suggests the beginning forma.tion of a vertebral body. This traced laterally is continuous with the occipital arch condensation somewhat anterior to its posterior boundary. I was not able to ﬁnd two occipital segments in the midline, as Jager reported in the chick.
By 14 days the anterior segmental condensations are more marked in the midline. The hypochordal brace of the atlas can now be made out and the posterior end of the basioccipital cartilage has now begun to be formed. By 15 days (ﬁg. 23) the basal cartilage has grown farther anterior and there is a suggestion of a posterior segment somewhat separate from the main cartilage. A’ comparison of ﬁgures 23 and 24 indicates that this posterior segment which can be identiﬁed in a 14-day embryo and is conspicuous in one of 15 days has by 16 days become more compressed and deﬁnitely diiferentiated into non-cartilaginous material behind the cartilaginous basal plate. Its outline is still visible in the oldest embryo and its relations similar in all three in that it extends dorsal to the notochord as compared to the more cephalic basioccipital condensation which is in all cases chieﬂy hypochordal at this posterior end. The decrease in cephalo-caudal length in the older embryo is probably an expression of the growth mechanics of the region. The cervical ﬂexure of the older embryos is further developed, forming a more acute angle between occipital and vertebral elements and at the expense of the softer tissues at the angle.
Jager referred to the basioccipital segments in the chick as bodies of vertebrae, while Terry felt that the same material in the cat was comparable to hypochordal braces and essentially arch rather than body structures. The variation in the course of the notocord through the occipital cartilage makes it very diﬂicult to draw any conclusions from a comparison of different species. Nor is the reason for this variation in notochordal relation clear enough to be of any as— sistance. The fact that the mesenchyme in the midline does not show in the occipital region of the rabbit either any somitic boundaries or any division into regions of different density makes it difficult to determine from which portion of the sclerotome the ﬁrst basioccipital condensation and cartilage really develops. Even tracing the condensation laterally gives dubious evidence due to the compression which is taking place and which is very likely affecting the median and lateral regions differently. The fact that the caudal end of the basioccipital cartilage which is the first to put in its appearance is somewhat anterior to the caudal end of the posterior occipital arch seems to indicate that the posterior half of the third sclerotome from which this arch has developed has probably contributed mesenchyme to the tissue behind rather than to that of the basioccipital cartilage. The presence of a deﬁnitely outlined condensation behind the basal plate and at the level of the lateral arch material in embryos of 14, 15 and 16 days suggests that the later connective tissue and ligaments between the atlas and occipital bone are formed from the median part of the posterior dense half of somite 3 as Well as from the anterior loose half of somite 4.
In a comparison of basal occipital plate with vertebrae, the conditions in rabbit embryos seem to me to indicate rather a comparison with body than with arch material. Although it is true that the posterior end is mainly hypochordal its relation to notochord is rather that of the ventral half of a vertebral body than of a hypochordal brace (ﬁg. 24). But, in any case, it seems to me better, in the rabbit at» least, to extend the comparison between occipital and vertebral cartilage and bone only so far as to say that the occipital region is formed out of a fusion of material of three sclerotomes which are‘ apparently the equivalent in young stages of the material of three vertebrae. This material retains for some time in its lateral part evidences of segmentation and arch formation comparable to that in vertebrae, but in the midline modiﬁcation and loss of segmentation occur much earlier.
The literature presents considerable evidence that there are in mammals three occipital myotomes. This number has been reported for cow (Froriep, 1886), sheep (Froriep, 1882), rabbit (Chiarugi, 1890), rat (Butcher, ’29) and human (Mall, 1891) embryos. My observations on rabbit are in agreement with Butcher’s on the rat that the ﬁrst myotome is formed from the ﬁrst completely out off somite and since the ﬁrst three somites are concerned in the formation of the occipital region there are thus three myotomes which must be classiﬁed as occipital which is a conﬁrmation of Chiarugi’s ﬁndings in this same form.
Although many workers have been interested in the number of occipital myotomes much less has been said concerning their fate. Froriep thought of the hypoglossal musculature of mammals as developing from ventral extensions of the anterior somites and felt that this was the only satisfactory explanation for its innervation by occipital nerves. Although the origin of the hypoglossal musculature from somites has been demonstrated in lower forms there is still some question as to its derivation in mammals (Lewis, ’10), and Kingsbury, ’15). There is in the rabbit some indication of such a downgrowth of material from the somites, but it is not my purpose in this paper to trace the development of the hypoglossal musculature or any contribution to it by occipital myotomes, but rather to consider the fate of that portion of the occipital myotomes which does not become incorporated into such foreign territory, but remains in the region of the axial skeleton. Lewis (’10), in his discussion of the development of the musculature in man, says that the deep muscles of the back arise from the fusion of the myotomes proceeding in an antero-posterior direction and he adds that “the occipital myotomes, at least the caudal ones, are probably fused into this myotome column.”
Butcher found the earliest myotome formation in the rat present in a 15-somite embryo. By a 23-somite stage this same myotome which had always been small was present only as a condensation of radiating cells. He was able to trace it in older embryos and, in one of 34 somites, described it as still present althoug “very small and principally disintegrated.” The fate of the other two occipital myotomes he did not take up.
In rabbit embryos of 22 and 23 somites (figs. 16 and 25) the anterior myotomes are distinct and that of somite 1 differs from those caudal to it only in being much shorter. All the myotomes then continue to increase in size and in an 11-day embryo the ﬁrst one compares very favorably with those caudal to it (ﬁg. 2). This is, however, about the height of its development. It now begins to break up and in at 12%-day embryo (ﬁg. 3) it is much reduced in size. In fact, all three occipital and even the ﬁrst cervical myotomes are smaller than those immediately caudal to them, although none so markedly so as the ﬁrst. Figure 26 shows the appearance of the ﬁrst and second myotomes of this embryo in section. Only a few myoblasts can be seen in the ﬁrst and the second is also breaking up, although to a lesser extent than the ﬁrst. At this stage each occipital myotome is still deﬁnitely associated with a hypoglossal nerve root.
In a 14-day embryo the occipital region has become more compressed and the hypoglossal nerve has grown further ventrad and caudad with its roots pressed closer together. I could no longer ﬁnd any trace of the ﬁrst myotome and what is left of the second is now fusing with the third (ﬁg. 27). In its medial part the third can still be identiﬁed, but it is now becoming intimately associated with the ﬁrst cervical. In this plane the other myotomes are separated from each other by the vertebrae, but since the occipital cartilage does not extend so far ventrally, there is nothing to separate the third occipital and ﬁrst cervical myotomes. The compression and ventracaudal pull which is inﬂuencing the growth of the hypoglossal nerve is also tending to bring together these myotomes at the head-neck boundary. Going laterally in this embryo beyond the region of developing cartilage one ﬁnds the myotomes fusing into the myotomic column from which the muscles will be formed. A longitudinal split is already present, although the primitive segmentation is still visible.
In a 15-day embryo the occipital myotome can still be identiﬁed in the parasagittal plane of the spinal ganglia with a branch of the ﬁrst cervical nerve entering it (ﬁg. 28). I was not able in any of the embryos I examined to ﬁnd any hypoglossal branch to this mass. In a more lateral plane of this embryo the original myotomal segments have almost disappeared. I could not be sure whether the occipital myotome contribution extended into this lateral region or not.
In a 16-day embryo the original segmentation is lost even in the median region (ﬁg. 29) and by 17 days the mass of tissue resulting from the fusion of ﬁrst cervical and occipital myotomes is now developing a secondary division into the anterior and lateralis parts of the rectus capitis muscle.
In the series of rabbit embryos examined somitic development resulted in the formation of three occiptal myotomes, the ﬁrst of which disappears without any visible participation in the formation of skeletal muscle tissue. The second largely disappears in similar fashion, but a few myoblasts seem to persist and fuse with those of the third myotome which in turn can be identiﬁed in its medial part as late as 15 days. Soon after this, however, it loses its identity as it becomes fused with the ﬁrst cervical and innervated by a branch of the ﬁrst cervical nerve. No evidence of innervation of this occipital myotome material by a branch of an occipital nerve was seen. This at ﬁrst seems contrary to what might be expected from its segmental origin. However, Bardeen (’O0) pointed out that muscular branches of nerves do not grow into the tissue which they are to innervate until relatively late and that although “in a general way . . . . nerve territories are ﬁxed early in embryonic life . . . . the individual twigs supplied to the various special regions are determined largely by conditions of growth and hence vary greatly.” In this way he explained the variation in peripheral nerve territories and thought of nerves as having an inherent power to grow into regions needing nerves. This is probably the explanation for the innervation of the muscle cells of the occipital myotomes by the ﬁrst cervical nerve. By the time the nerves are sending branches into muscle masses the occipital myotome is so closely associated With the ﬁrst cervical that, in these cases at least, it receives its innervation from the same source. Of the cervical muscles only the mass destined to give rise to the rectus capitis muscles is sutﬁciently isolated for one to be able to say certainly from which myotomes it is formed. Here there can be little doubt that the ﬁrst cervical and occipital segments are the contributing ones. However, the myoblasts of these segments become so intermingled before the ﬁnal differentiation of the muscles that I Was not able to trace further the fate of the individual myotomes.
1. Ahead of the ﬁrst true somite in the rabbit there is formed a rudimentary somite which varies in its degree of development, but which in all cases breaks up into mesenchyme Without differentiating into dermatome, myotome and sclerotome.
2. There are in the rabbit three occipital hypoglossal roots. The first well—developed spinal ganglion is that of the ﬁrst cervical nerve. Ahead of this is a ganglion of Froriep at the level of the third occipital hypoglossal root and further anterior crest cells can be seen scattered along the root of the accessory nerve. No dorsal occipital hypoglossal roots were seen.
3. There are three occipital somites.
4. The sclerotomes of somites 2 and 3 differentiate into anterior loose and posterior dense halves. No such division was seen in the sclerotome of somite 1.
5. Two occipital arches comparable to those of vertebrae a.re formed and can be identiﬁed as late as the time of beginning chondriﬁcation. Soon after this their segmental character is lost.
6. There is a marked compression of the tissues in this region, the sclerotomal material being not only relatively, but actually shorter in older embryos. This compression results in 1) the approximation of the hypoglossal roots and 2) the fusion of the two occipital arches. Individual variation in the number of hypoglossal foramina present in the adult skull of mammals is undoubtedly due to variation in the degree of compression of the hypoglossal roots previous to the time of ossiﬁcation of this portion of the skull.
7. The cartilaginous basal occipital plate in rabbits begins development at its caudal end and differentiates anteriorly from this with little evidence of a primitive segmentation, except as this posterior ﬁrst center might be called a segment.
8. There are in the rabbit three occipital myotomes. The ﬁrst of these disappears early. A few myoblasts of the second persist and fuse with those of the third which in turn fuse with those of the first cervical and contribute to the formation of the rectus capitis muscles. Other occipital myoblasts may be added to the myotome column from which develop the deep muscles of the neck and back.
Financial assistance toward publication from the Mrs. Sage Research Fund is hereby gratefully acknowledged.
BUTCHER, E. 0. 1929 The development of the somites in the white rat (Mus norvegicus albinus) and the fate of the myotomes, neural tube and gut in the tail. Am. J. Anat., vol. 44, pp. 381-439.
ma Bum, G. R., AND J. H. Woonasa 1930 The early development of the skull of the rabbit. Phil. Trans. Roy. Soc., B, vol. 218, pp. 373-414.
CHIARUGI, G. 1890 Le developpement de nerfs vague, accessoire, hypoglosse, et premiere cervicaux chez les sauropside et chez les mammiferes. Archiv. Ital. de Biol., vol. 13, pp. 309-341, 423-443.
FRORIEP, A. 1882 Ueber ein Ganglion des Hypoglossus und Wirbelanlagen in der Occipitalregion. Beitrag zur Entwickelungsgeschichte des Sangethierkopfes. Archiv. 1. Anat. u. Physiol., 1882, s. 279-302. 9
1886 Zur Entwickelungsgesehichte der‘ Wirbelsiiule, insbesondere des Atlas und Epistropheus und der Occipitalregion. Archiv. f. Anat. u. Physiol., 1886, S. 69-150.
FRORIEP, A., AND W. BECK 1895 Ueber des Vorkommen dorsaler Hypoglossuswurzeln mit Ganglion in der Reihe der Siiugethiere. Anat. Anz., Bd. 10, S. 688-696.
FﬁB.BRINGER, M. 1897 Ueber die Spine-occipitalen Nerven der Selachier und Holocephalen und ihre vergleichende Morphologie. Festsch. v. C. Gregenbaur, Bd. 3, S. 349-788.
GAUPP, E. 1897 Die Metamerie des Schisidels. Ex-geb. der Anat. u. Entwick., Bd. 7, S. 793-885.
GOODRICH, E. S.’ 1930 Studies on the structure and development of vertebrates. Macmillan & Co., Ltd., London. V
GEGENBAUR, C. 1872 Untersuchungen zur vergleichenden Anatomie der Wirbelthiere. Drittes Heft, Leipzig.
Hmuusow, R. G. 1918 Experiments on the development of the fore limb of Amblystoma, a self-diﬂ:‘ei-entiating equipotential system. J. Exp. Zo61., vol. 25, pp. 413-461.
HIS, W. 1888 Centralen u. peripherischen Nervenbahrcn beim menschlichen Embryo. Abhandl. math.-phys. C1. Kgl. Sachs. Ges. Wiss., Bd. 14.
HUXLEY, T. M. 1858 On the theory of the vertebrate skull. Proc. Roy. Soc., vol. 9, pp. 381-457.
JAGER, J. 1924 Ueber die Segmentierung der Hintex-haupt—region und die Besiehung der Cartilage acrochordalis zur Mesodermcommisur. (Ein Studium bei Vﬁgeln.) Groningen Dissertations, vol. 25.
Noommueos, W. 1905 Ueber die Entwicklung des Chondrocraniums der Sangetiere. Petrus Camper, Bd. 3, S. 367-430.
REX, H. 1905 Ueber das Mesoderm des Vorderkopfes der Lachmtiwe. Morph. Jahrb., Bd. 33, S. 107-347.
TERRY, R. J. 1917 The primordial cranium of the cat. J. Morph., vol. 29, pp. 281-433.
WEISS, A. 1901 Die Entwicklung der Wirbelsaule der weissen Ratte, besonders der vordersten Halswirbel. Zeits. f. wiss. Zo6l., Bd. 69, S. 492-532.
- These two reviews (Lewis, Streeter) are included in this list, although they are not cited in the text, because they both have excellent bibliographies on the development of the skull.
PLATE 1 EXPLANATION or FIGURES
1 to 3 Reconstructions from sagittal sections of embryos 91¢, 11 and 12% days, respectively, embryos 567, 558 and 150 of the Harvard Embryological Collection. X 32}, X 15, X 15. Red outlines the myotomes except in ﬁgure 1. In this embryo the somites are not yet broken up into dermatome, myotome, and sclerotome and here the red outlines the undifferentiated somite. Fine dense stippling indicates the posterior dense regions of the sclerotomes. Fine diffuse stippling indicates the looser portions of the sclerotomes. Coarse stippling indicates the ganglia and scattered neural crest cells.
1, 2, and 3, ﬁrst, second and third XII, XII’ and XII", ventral occipital
pharyngeal pouches hypoglossal roots of the ﬁrst, second IX and X, superior ganglia of nerves and third segments, respectively IX and X 01, ﬁrst cervical ganglion IX’ and X’, inferior ganglia of nerves F, Froriep’s ganglion IX and X 0, otic vesicle
XI, eleventh cranial nerve ANTERIOR POST-0T1O SOMITES IN RABBIT PLATE 1 RUTH MACMILLAN HUNTER
JOURNAL; OB‘ MORPHOLOGY, VOL. 57, N0. 2 PLATE 2 EXPLANATION or FIGURES
4 Sagittal section of R348, :1 5—somit0 onlbryo to Sl10\\' the somitc tlcveloplnont typical of this stage. )< 113.3 s1, smuitc 1.
5 Sngittal s(‘("t.ion of R 8 (la, 10 hrs., PNO E, n 7-somitc embryo, to show the ru(lin1entu1'y somito foriilzition mltorior to somite 1. X 113. s1, soniitc 1; 1', 1-udinientnry sornito
6 Sagittal section of R573, an embryo in which the ninth somite is being fornied. X 113. s, copllalic end of solnitc 1; 1', cephalic end of rudimentary soiuite.
7 T1':u1s\‘c1's(a sottioli of R260, 21 (i—somife enibryo, through somite 1. X 169.
S Saine, through the 1ncsode1'1n immediately anterior to soinito 1. X 169.
9 Same, through ru(li1i1c11tary somito forinatioli. X 169.
10 Saino, still further ant.e1-ior. X 169.
11 to 13 'I‘1'ansvorse sectioils of 650, a 5-smnito embryo, through rudirnontary somite fornmtion, tlirougli somite 1 and through somife 2, 1'espe(<tiv('ly. X 285.
14 ’1‘r:u1sverse section of R314, through :1 median band of cells which extends botweou somifes 1 and 2. X 169.
15 Sagittal section of R279, an 11—somit‘o mnbryo, to show the beginning of sclcrotome form:L‘rion of soinite 1. X 139. s1, somife 1
16 Sagittal section of 567, a 22-soinite einbryo, through the anterior soinitos. X 51. V, Von Elmer ’s ch-ft
“I wish hero to express my gr-altitude to Mr. F. Pittock, of Uiiiversity College, London, for the photoinicrograplis of ﬁgures 4, 5, 6, 7, 8, 9, 10, 14, 15, and 25. The remaining ﬁgures are of en1br_Vos from the Harvarrl E111|>1'y<>logi(1al Collection. ANTERIOR POSTIMHC SOMITESIN RABBIT RUTH MACMUJAN HUNTER
S ‘ > _V ’.1Lr.\w'-"V
2 PLA TE 3
EXPLANATION OF‘ FIGURES
17 A sagittal section of 558, an 11-(lay embryo. X 55.
18 A sagittal section of 1:30, :1 1‘.’§—day embryo. X
19 A sagittal section of 162, a 16-day embryo, showing the hypoglossal roots traversing the basioccipital cartilage. In this case the original three roots are fused into two. X 55.
20 A sagittal section of 1:36, a 14»d21_v embryo, showing ventral occipital hypo» glossal rootlets becoming grouped as they move ventrally toward the basioccipim] precartilage. X 55.
21 The same embryo. A more lateral section, showing the occipital hypoglossnl rootlets grouped into three roots as they traverse the precartilnge of the region. X 55.
22 Mid-sagittal section of 150, a 12._‘;—d:1_v enilmryo, showing the beginning of sclerotomal condensation around the n()t()(‘ll0I'(l. X .35.
23 A sagittal section of 159, a 15-day enibryo. X 55.
24 A sagittal section of 162, a 16-day cnibryo. X ‘.35.
an, arch of the atlas oal, occipital arch formed from the lo, basioccipital cartilage second selcrotoine 0, first cervical ganglion 02:2, occipital arch formed from the con, condensation posterior to basiocn third sclerotome
cipital cartilage s, most anterior midline segmental eon» F, Fr0riep’s ganglion (lensation, that of the third somite h, hypoglossal roots s2, s3, contlensntions of posterior halves hl’, most anterior hypoglossnl rootlet of’ sclerotomes of somites 2 and 3, ha, hypochordal arch of the atlas respectively
n, anterior ventral rootlets. of the hypoglossal nerve
528 ANTERJOR. 1‘0ST—0T1G SOMITES IN RABBY1‘ PLATE '5 RUTII MACMILLAN HUNTER
529 PLA TE 4
EXPLANATION OF FIGURES
.) A sagittal section of R255, :1 23—son1ite embryo through the developing dc1'mo—myoto1nc. The first somitc is at the loft. X 170.
26 A sagittal scction of 156, a 14-day cn1br_yo, showing the close approximation of the occipital and ﬁrst cervical inyotonles. X 40.
27 A sagittal section of 150, a 12:};-(lay embryo, showing‘ the condition of the
ﬁrst and second myotonics. X 285.
This is tho same clnhryo from which the reconstruction of figure 2 was nludc.
28 A n1irl—sz1gittul section of 159, a ].'>—(lay cnibryo, showing the fusion of occipital anrl ﬁrst (-,c1'vi(:al rnyotonlcs. X 55.
29 A sagittal section of 162, a 16-day embryo, through approxiniatcly the
same region as ﬁgurc 28. X 55.
Occipital and (-ervical nlyotmnes can no longer be distinguished.
aa, arch of’ the atlas 1111,1112, ﬁrst and second myotomes
C, first cervical ganglion oa, occipital arch
cni, (:01-vicul niyotorno
l1, co11\'01‘gi11g occipital roots of the hypoglossal nerve
om, occipital myotmno m, rcctus capitis muscle mass AN'I‘I-JRIOR POST-OTIC SOMITES TN RABBIT PLATE 4 RUTH MACMILLAN HUNTER
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