Paper - Migration of the ear vesicle in the tadpole during normal development (1921)

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Streeter GL. Migration of the ear vesicle in the tadpole during normal development. (1921) Anat. Rec. 21(2): 115-126.

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This historic 1907 paper by George Streeter described the development of the frog tadpole otocyst.

See also: Streeter GL. Some experiments on the developing ear vesicle of the tadpole with relation to equilibration. (1906) J Exper. Zoology. 3(4): 544-558.

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Migration of the Ear Vesicle in the Tadpole during Normal Development

Embryology History George Streeter
George Linius Streeter (1873-1948)

George L. Streeter

Department of Embryology, Carnegie Institution of Washington, Baltimore, Marylayid

Eleven Figures

In 1837 von Baer made the observation that the diaphragm is situated in the neck region in very young embryos, receiving its innervation from the cervical nerves, and that in the course of its development it acquires a more caudal position corresponding to the enlargement of the heart and lungs. This descent of the diaphragm was subsequently described in greater detail by Mall ('97). Uskow ('83) and Mall ('97) pointed out the marked shifting of position which the heart, lungs, liver, intestinal tract, and Wolffian bodies undergo during development in relation to each other and to the vertebral column. The migration of these organs in the embryo has given us the explanation of the peculiar course of their nerves of supply; for example, the inferior laryngeal, the vagus, the phrenic, and the splanchnic nerves. Kolliker ('61) showed that the shifting in position of the spinal cord produces an elongation of the spinal-nerve roots and the formation of the Cauda equina. The influence of this factor in the formamation of the filum terminale has been recently studied by Kunitomo ('18). It has been shown by Lewis ('01, '10) that such muscles as the trapezius and the eye muscles undergo considerable shifting in position between the time of their first appearance and the time when they have acquired their permanent attachments. Among others, Futamura ('06) has described the migration of the facial muscles and the consequent deflected distribution of the branches of the facial nerve. Within the central nervous system there are several instances where the component nuclear masses exhibit a distinct migration in the course of their development (Streeter, '08; Kappers, '10). As a result of their disproportionate growth, the primary divisions of the brain shift into new positions relative to each other, and this is accompanied by an interesting adjustment on the part of the vascular drainage of these structures. Kohn ('07) and others have shown that the sympathetic gangUa undergo an extensive peripheral migration. When the places of origin of the thjTQus and thyroid glands were first discovered, it was recognized that these organs exhibit a conspicuous type of migration. Even in the case of the skeleton, it has been maintained (Rosenberg, '76) that the point of vertebral articulation of the pelvic girdle moves along the column into the lumbar territory during development, although this has not been adequately substantiated. There is, however, a very good example of topographical adjustment of bony structures in the case of the teeth.

To any one occupied with the study of organogenesis, the developmental alteration in topography that is everyAvhere in progress is very striking. In some cases it is obviously a matter of mechanical stress exerted by adjacent organs upon each other, the controlling factors being their relative increase in size and the relative resistance of their tissues; or it may be a matter of traction in connected organs. In other instances we find structures invading new territories by virtue of the direction of their growth, which is dependent on the fact that the proliferation and increase in size of their constituent cells are more active in one direction than in another. In some cases this is associated with a thinning out and disappearance (possibly dedifferentiation) of the opposite pole of the organ, resulting in its complete transposition. Such factors are easily understood and various combinations of them explain most of the instances of developmental topographical alteration in organs which we encounter. There are other cases, however, which are more obscure and in which the movement of the organs or structures during their development cannot be entirely explained by simple mechanical factors; in these the phenomenon resembles a true migration such as is seen in individual cells. For lack of a better explanation, we must consider the possibility of the existence of some force, of the nature of a chemotaxis, interacting between these structures and their environment. It is in this group that we must place the ear vesicle which, during the course of normal development, exhibits a considerable change in position. It is to this that I would call attention here.

From several studies previously reported by the writer (Streeter, '07, '09, '14) and from a recent paper by Ogawa ('21), it is apparent that the determining factors in the posture of the membranous labyrinth involve something more than a passive development of the ear vesicle in the position in which it originally finds itself. It is clearly evident, moreover, that the final position of the labyrinth is not simply the result of an adjustment brought about during its development by the interaction of mechanical processes of the adjacent structures, but that it is due, in part at least, to an autostatic tendency inherent in the vesicle itself, by virtue of which it maintains and accurately adjusts its position during development with reference to the brain and the surrounding structures. When an early ear vesicle is experimentally rotated into an abnormal position, or transplanted in an abnormal position to the opposite side of the same specimen or to another specimen, it subsequently tends to correct its posture, and the final labyrinth, in spite of the previous displacement, is found to possess normal topographical relations.

It is of interest to record that not only under artificial conditions, but also in the ordinary course of development, the ear vesicle of the tadpole undergoes a definite migration, moving from the point of its detachment from the skin to a more median and dorsal location, so that it eventually lies close against the side of the hindbrain with its endoljonphatic appendage overlapping the margin of the thin medullary velum that forms the roof of the fourth ventricle.

If one prepares sections through the auditory region in a series of tadpoles covering the period between the premotile stage and the end of the first month, the changing relations of the ear vesicle to the surrounding structures can be readily made out (figs. 1 to 9). These figures are made with the same magnification and thus, by comparing them, it is possible to determine the actual increase in size, as well as the differentiation of the walls and the alteration in the position of the individual vesicles. In figures 7 and 8 the length of the specimens is given; in the remaining figures the age given is the length of time the specimen was allowed to develop after reaching the operating stage, i.e., when it has acquired a distinct tail bud and gill eminences, but has not yet exhibited any motor response to stimuli.

In the first stage shown (fig. 1) the relatively thin lateral wall of the ear vesicle lies tight against the ectoderm. The vesicle is separated from the thick endoderm and the brain tube by a narrow interval filled with mesenchyme which is beginning to show open spaces in the vicinity of the notochord, elsewhere being relatively compact and heavily laden with yolk. As yet there are no blood-vessels in this region and the acoustic nerve and ganglion are not clearly differentiated from the surrounding tissue. It will be noticed that the lateral plate of the brain tube lies in a vertical plane and the point at which the ventral nerve roots are to converge lies opposite the dorsal tip of the ear vesicle.

In the next stage (fig. 2) the ear vesicle remains in close contact with the ectoderm. The surrounding mesenchyme is assuming a reticular character and in it the primary bloodvessels can be recognized. The acoustic ganglion is distinctly marked off, being attached to the anteromedian surface of the vesicle and connected by a strand with the brain wall. The roof of the latter is thinning out and the lateral walls are undergoing eversion. In the third stage (fig. 3) the conditions are essentially the same, although the vesicle wall has undergone further differentiation, the mesenchyme is distinctly reticular, and there is further eversion of the brain wall. In the sections oral to the one selected for illustration, the acoustic-nerve ganglion is present. It can be seen that the ear vesicle at this time is widely separated from the brain and almost wholly ventral to it. The intervening mesenchyme is loose and would offer slight mechanical obstruction to the migration of the vesicle, and certainly the primary brain blood-vessel cannot be regarded as a serious obstruction, since we find that even a much more mature vascular system can readily accommodate itself to any movement of the surrounding organs. A brilliant example of this is seen in the case of the venous drainage of the fetal cerebrum. Migration, however, cannot occur so long as the vesicle adheres to the ectoderm. Its detachment therefrom becomes complete in the next two stages.

Figs. 1 to 9 Sections showing the changes in the topographical relations of the ear vesicle of the tadpole during the period between the premotile stage and the end of the first month. In figures 1 to 6 and figure 9 the age given is the length of time the larva was allowed to develop after reaching the operating stage; i.e., tail bud and gill eminences present, but no motor response to stimuli exhibited. X 50. B.V., primitive blood-vessel ple.xus; Endol., endolymphatic appendage; VIII, acoustic nerve ganglion; IX, glossopharyngeal nerve ganglion.

The stage illustrated in figure 4 is at the critical point where the vesicle is becoming detached coincident with an invasion of mesenchyme between it and the ectoderm. At the same time the brain shows further development of the roof of the fourth ventricle and continued eversion of its walls which tends to thrust it toward the ear vesicle. The vesicle itself is assuming a more dorsal position, as compared with the previous stage. The portion that is to form the endolymphatic appendage can be clearly recognized from five hours on; by the second day it is not only thicker than the rest of the wall of the vesicle, but also shows a beginning evagination and a distinct differentiation of its component cells. A conception of the shifting that is in progress can be obtained by the realization that the endolymphatic appendage of figure 4 will eventually overlap the rhombic lip of the brain wall.

By the third day (fig. 5) the upper half of the ear vesicle is above the level of the junction of the brain and notochord and is surrounded on all sides by reticular mesenchyme which should favor its migration. Its only attachment is that of the acoustic nerve ganglion which forms a massive strand firmly attached at one end to the brain wall and at the other to the anteromedial wall of the ear vesicle. From the differentiation of the mantle zone -of the brain wall it can be seen that the point of attachment of the nerve corresponds closely to its permanent point of entrance and, tracing it peripherally to the vesicle wall, its fibers can be followed to the macular area. The size and character of the acoustic nerve might lead one to attribute to it a definite influence in any subsequent movement of the vesicle; but we know that the phrenic nerve exhibits no restraining influence in the descent of the diaphragm and there is no evidence that the facial nerve exercises any guiding force in the migration of the musculature of the face. It is to be noted that there is still a relatively wide interval between the vesicle and the brain wall. As yet the mesenchyme shows no differentiation into skeletal framework, but on each side of the notochord can be seen the oral extension of the spinal musculature.

Up to the fourth day (fig. 6) there has been a gradual thinning of the main part of the wall of the ear vesicle, accompanied by an increase in the am.ount of the contained otic fluid, and at this time the first steps occur in the formation of the semicircular ducts. A little more than half of the vesicle is now above the level of the junction of the notochord and the brain. The vesicle and brain wall are more closely approximated, which may be explained in part by the further eversion and growth of the latter. On the other hand, there is a beginning differentiation of the subcutaneous tissues and pigment membrane producing an increase in the distance between the ear vesicle and the surface of the larva.

In larvae 9 mm. long (fig. 7) one finds the formation of the semicircular ducts well under way and at the same time the mesenchyme lateral to the ear vesicle is differentiated into a characteristic subcutaneous tissue, while that median to the vesicle shows a condensation into precartilage tissue. Spreading from the chordal area toward the ear vesicle and surrounding the brain can be seen arachnoidal spaces of a primitive type. Notwithstanding this more permanent type of environment, the dorsal migration of the vesicle is not yet complete, for in older stages almost the entire vesicle lies dorsal to the level of the chorda.

In larvae 12 mm. long the endolymphatic appendage and the dorsal crest of the vesicle have nearly reached the level of the rhombic lip, and at the same time the lowest point of the vesicle lies opposite the level of the center of the notochord. The dorsal extension at this time is due in part to the direction of the growth, associated with the formation of the anterior and posterior semicircular ducts and the increase in the length of the endolymphatic appendage.

At one month the ear vesicle is completely differentiated into a membranous labyrinth with three semicircular ducts and a characteristic macular area to which is attached the gangHon and its peripheral nerve terminations. A characteristic endolymphatic appendage is present, consisting of a relatively large sac connected by a slender duct with the vestibular portion of the labyrinth. As can be seen in figure 9, the sac now Ues in close contact with the thin roof of the fourth ventricle. The labyrinth lies wholly dorsal to the midlevel of the notochord and is secured in this position by the mesenchymal otic capsule, consisting of precartilage tissue, portions of which are already differentiated into typical cartilage cells surrounded by a homogeneous matrix. With this stage the essential relations of the labyrinth may be regarded as established; the subsequent minor changes in its topography are those determined by the mechanical factors of its own further growth and the further growth and differentiation of the surrounding structures.

Fig. 10 Diagram showing the migration of the ear vesicle relative to the brain wall from the position it occupies at the end of the second*,day (ot.) to the position it attains as a differentiated labyrinth at the end of the first month (of), the brain wall being represented as stationary.

From the foregoing comparison of the individual stages it is clear that the ear vesicle shifts its position relative to the brain wall to the extent diagrammatically shown in figure 10. ^Miereas at the end of the second day the vesicle lies ventral to and apart from the brain, at the end of the first month it is situated close against the lateral brain wall with its endolymphatic appendage overlapping the rhombic Hp. In the figure there has been no account taken of the lateral movement of the brain wall, and therefore to that extent the path of migration of the ear vesicle is exaggerated. Its dorsal migration relative to the notochord, the ectoderm, and the everted brain wall may be represented as in figure 11, which shows more accurately than figure 10 the extent of its change of position relative to the whole environment. Although the normal migration of the ear vesicle is not so marked as that of the thymus and many other organs, nevertheless that phenomenon unquestionably occurs. To some extent the mechanical forces of growth of the concerned parts can be recognized as influencing the migration; no single one of these factors, however, or no combination of them would appear to adequately explain it.

Fig. 11 Superimposed sections of the ear region of a tadpole of the nineteenth hour (dotted) and of another at the end of the first month, enlarged so that the brain is the same size in both cases, the two being fitted so as to exactly coincide.

The detachment of the vesicle from the skin is readily explained by the differentiation of the subcutaneous tissues and the formation of the pigment membrane. This begins to take place about the second day. By the fourth day the elements of the pigment membrane make their appearance, and in tadpoles 12 mm. long there is a relatively complete membrane separating the vesicle from the loose tissue underlying the ectoderm. This differentiation releases the vesicle from its firm attachment to the ectoderm, but it does not in any way favor its dorsal migration.

The change in the relative position of the ear vesicle and the brain wall is in part accounted for by the direction of growth of the latter, which undergoes an eversion whereby it is thrust ventralward and lateralward toward the vesicle. The maximum effect of this eversion is reached at the end of the fourth day, but at this time, in addition to the close approximation of the brain wall and the ear vesicle, a dorsal shifting of the latter has occurred relative to the level of the notochord, a fact which can hardly be explained by the change in position of the lateral brain plate.

As to this dorsal migration of the vesicle as a whole, which takes place gradually throughout the first month, one should consider the possibility of its being due to the direction of growth of the vesicle; i, e., that the dorsal portions of the vesicle may perhaps grow more rapidly than the ventral portions. In the case of the endolymphatic appendage, the direction of growth may very well constitute a factor in the attainment of its final position. The dorsal growth of the sac and the elongation of its duct would favor its dorsal shifting. Aside from the slender endoljTiiphatic duct, however, there appears to be nothing to prevent the sac from occasionally going astray orally or caudally, where the tissues would offer httle obstruction to its extension in these directions. That it never does so forces one to postulate the existence of some form of determinative attraction between the endoljiiiphatic sac and the medullar}^ roof to which it later invariably becomes intimately attached.

There is no evidence that the acoustic nerve gangUon plays any considerable part in the way of a guiding or traction force. The nerve can be recognized at the fifth hour, connecting the vesicle with the brain wall, but when it is experimentally detached, as in the transplantation of a vesicle from one tadpole to another, the severing docs not interfere with a correct adjustment of the posture of the vesicle. This corresponds to our experience with other organs, in which the nerves do not act as a check or show any evidence of influencing the migration of the organs in any way. The surrounding mesench>^ne and primitive blood vessels can also be dismissed as factors.

The cartilaginous skull does not make its appearance until the final relations of the labyrinth to its environment are essentially estabhshed, that is, toward the end of the first month, and therefore cannot play a primary part in the migration of the vesicle. However, after the firm otic capsule becomes differentiated the latter must absolutely control those further alterations in the posture of the contained labyrinth which are associated with the final changes in the form of the base of the skull.

Literature Cited

V. Baer, K. E. 1S37 Ueber Entwickelungsgeschicht der Thiere. Konigsberg.

FuTAMURA, R. 1906 Ueber die Entwicklung der Facialismuskulatur des Men schen. Anat. Hefte, Bd. 30.

Kappers, C. U. Ariens 1910 The migrations of the abducens-nucleus and the concomitating changes of its root-fibers. Psychiatrische en Neuro logische Bladen.

1910 The migrations of the motor cells of the bulbar trigeminus, abducens and facialis in the series of vertebrates, and the differences in the course of their root -fibers. Verh. d. k. Akad. v. Wetenschr. t. Amsterdam, Tweede sectie, Deel 16.

KoHN, A. 1907 Ueber die Schiedenzellen peripherer Ganglionzellen. Anat. Anz., Bd. 30.

KoLLiKER, A. 1861 Entwicklungsgeschichte des Menschen und der hoheren Thiere. Leipzig.

KuNiTOMO, K. 1918 The development and reduction of the tail and of the caudal end of the spinal cord. Contributions to Embryology, vol. 8. Carnegie Inst. Wash., Pub. 271.


Lewis, W. H. 1901 The development of the arm in man. Am. Jour. Anat., vol. 1. 1910 The development of the muscular system. Manual of Human Embryology (Keibel and Mall), vol. 1.

Mall FP. Development of the human coelom. (1897) J Morphol. 12: 395-453.

Mall, F. P. 1897 Development of the human coelom. Jour. Morph., vol. 12.

Ogawa, C. 1921 ExQeriments on the orientation of the ear vesicle in amphibian larvae. Jour. Exp. Zool., vol. 32.

Rosenberg, E. 1876 Ueber die Entwickelung der Wirbelsaule und das Centrale carpi des Menschen. Morph. Jahrb., Bd. 1.

Streeter, G. L. 1907 Some factors in the development of the amphibian ear vesicle, and further experiments on equilibration. Jour. Exp. Zool., vol. 4.

1908 The nuclei of origin of the cranial nerves in the 10 mm. human embryo. Anat. Rec, vol. 2, p. 115.

Streeter, G. L. 1909 Experimental observations on the development of the amphibian ear vesicle. Anat. Rec, vol. 3.

1914 Experimental evidence concerning the determination of posture of the membranous labyrinth in amphibian embryos. Jour. Exp. Zool., vol. 16.

UsKOW, N. 1SS3 Ueber die Entwicklung des Zwerchfells, des Pericardiums und des Coloms. Arch. f. mikr. Anat., Bd. 22.

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