Paper - The history of the eye muscles (1917)

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Neal HV. The history of the eye muscles. (1917) J Morphol. 30(1): 433.

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This historic 1917 paper by Neal is an early description of eye muscle development.



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The History of the Eye Muscles

H. V. Neal

Tufts College

Twenty Figures

Introduction

The muscles which move the eye-ball are a specialized group whose functional importance is quite disproportionate to their size. They are muscles of ancient origin, presumably antedating by millions of years muscles such as tho?e which move the eye-lids. As a result of the investigations of two generations of morphologists we are now in a position to sketch in general outline their probable phylogenesis. The present paper raises the problems — What has been the past history of the eye muscles? That changes have they undergone in their transformation of the fish into the mammal? How many myotomes enter into their formation? Are they, like the tongue and appendicular muscles, exotic in origin and derivatives of the post-otic lateral trunk muscles? To what do they owe their present isolation? Can their history be traced back into stages before eyes made their appearance?


Comparative anatomy has thrown very little light upon the history of the eye muscles. Like the eyes with which they are so intimately associated, they appear in the lowest vertebrates in essentially the same form as in man. Indeed their number and their nerve relations are the same in man as in the dogfish. Of the entire group of eye muscles only the superior obhque shows a functional change in the course of phylogeny. The direction of its pull is altered as the result of the development of the trochlear tendon. Comparative anatomy also reveals some aberrations in the innervation of the eye muscles and such curious modifications as in Astroscopus where some of the eye muscles are transformed in to electroplaxes with some striking changes in their innervation. Moreover, in reptiles and some mammals a retractor bulbi (oculi) makes its appearance as a derivative of the external rectus muscle (Johnson, '13; Fraser, '15), but in the great majority of vertebrates the number and the nerve relations of the eye-muscles remain identical and unchanged. Nature seems to have pursued with regard to them the policy of letting well-enough alone.' Their 'evolutionary potential' appears to be approximately zero.


Were we therefore dependent upon comparative anatomical evidence alone for our conclusions concerning the history of the eye-muscles, we should be obliged to consider them as an isolated and peculiar group, the pre-craniote history of which is unknown. While we should not feel forced to assert that they arose, Minerva-like, full-formed, nevertheless it, would remain a matter of uncertainty or of speculation whether they were exotic or endogenous, whether visceral or somatic, in their origin. Comparative embryology, however, appears to justify the assertion that the eye-muscles are a remnant of the lateral trunk muscles which, in the ancestors of vertebrates, extended in an unbroken series throughout the entire length of the body. Of the parietal muscles anterior to the ear they alone have persisted, through their functional relations to the eye-ball. Their isolation is associated with the growth and enlargement of the otic capsules and of the cranial skeleton.


The details of this story have been slowly gathered. First, Balfour ('78) discovered the extension of the body cavity into the head region of Elasmobranch embryos, thereby demonstrating the fundamental similarity of head and trunk regions in Vertebrates. He also showed that the mesoderm of the head undergoes a segmentation independent of that of the vis-ceral arches, resulting in the formation of the so-called head-cavities. Later, Marshall ('81) proved that the eye-muscles arise from the walls of these head-cavities. He asserted that four of the eyemuscles (those innervated by the oculomotor nerve) develop from the first head-cavity, the superior oblique muscle from the second and the external rectus muscle from the third. Subsequent investigation has repeatedly confirmed these results for all classes of vertebrates — Cyclostomes (Koltzoff '01), Elasmobranchs (VanWijhe '82, Miss Piatt, '91, Lamb '02), Reptiles (Corning '00, Filatoff '07, Johnson '13), Mammals (Miss Fraser '15).


One point, however, in the ontogenesis of the eye-muscles from the head-cavities still remains in dispute. While most investigators agree with Marshall in deriving the external rectus muscle from the third (hyoid) cavity, Dohrn ('04) and the writer ('09) have asserted that the second (mandibular) cavity also participates in its formation. Neither, however, published any figures or other evidence to support his assertion. The first, question, therefore, to which we may well turn our attention is, How many head-cavities participate in the formation of the external rectus muscle?



Fig. 1 A camera drawing of a parasagittal section of a 7 mm. Squalus embryo (Series IFF-2-2-16) showing the head cavities. The anterior cavity, not seen by Marshall but later discoverd by VanWijhe, is also shown. It soon degenerates while the other cavities differentiate into the eye muscles. A, anterior head cavity; 1, 2, 3, first, second and third head cavities; VII. ac, acustico-facialis nerve anlage; cl.crs.n, neural crest cells; gn.V, trigeminal ganglion; ot, otic capsule; sp, spiracular pouch; tb.n, neural tube.



Miss Piatt ('91) was the first to observe that in Elasmobranch embryos a muscle which she calls 'muscle E' arises in such intimate connection with the external rectus muscle that for some time she believed that the mandibular cavity took part with the third in the formation of the external rectus muscle." Subsequent observation has confirmed this observation of Miss Piatt, There is disagreement only concerning the supposition that the mandibular component ('muscle E') degenerates. Does this 'muscle E' — the mandibular component of the embryonic external rectus muscle — degenerate?


In answering this question Miss Piatt compared two stages ('91, figs. 5 and 6, pi. 5) which correspond quite closely with text figures 6 and 8 of this paper. She says (p. 86) :

This section (sect. 5) also shows the peculiar relation existing between the external rectus muscle, now forming in the third head cavity, and the mandibular muscle, mus. E. If this cross section be compared with a similar section through an older embryo, represented in sec. 6, it will be seen that were the cells of the mandibular muscle (mus. E.) to fuse with those of the third head cavity (ext. rec.) at the stage represented by sec. 5, the resulting muscle would closely resemble in shape the external rectus of sec. 6. I am convinced, however, that such a fusion does not take place, for the limiting wall of the third head cavity can be traced until the muscle here formed comes to occupy the entire place once occupied (sec. 5) by the cells of the two muscles (ext. rec. and mus. E.). The cells of the mandibular muscle (mus. E.) gradually yield their place to those of the third head cavity and are ultimately lost in the general mesoderm. Thus a muscle, the rudiment of which appeared in the walls of the mandibular cavity prior to the origin of any of the eye muscles, completely disappears, although in the embryo of 22 mm. it is still relatively large as compared with the eye muscles.

In the description of a 27 mm. embryo of Squalus she goes on to say (p. 87) : "The cells of the rudimentary muscle (mus. E.), so closely related to the external rectus, are now indistinguishable from the surrounding mesoderm, and the superior oblique muscle represents all that is left of the walls of the dorsal part of the mandibular cavity." Of the histological changes manifested by degenerating muscle cells Miss Piatt presents no evidence whatever.


Of Miss Piatt's 'muscle E' Lamb ('02, p. 195) says:

"This latter muscle has now (in a 19 mm. embryo of Squalus) reached its maximum development. The anterior end curves not only outward but upward as well, sp that the direction of the muscle is approximately dorso- ventral. From now on this muscle undergoes degeneration at as a 26 mm. stage scarcely a trace of it remains."


Proof of its degeneration, however. Lamb does not give. That Lamb is confused regarding the fate of the muscle is shown by the fact that in his figure 9, p. 185, 'muscle E,' which is correctly so labelled in the drawing, is incorrectly described in the paper as "prohferated from the hyoid somite," while it is named "the external rectus muscle!" Such contradictions are unfortunate in a paper which is otherwise a valuable contribution to the literature.

Johnson ('13, p. 161) apparently assumes the degeneration of the so-called muscle E (which occurs in Reptile embryos in the same relations as in Elasmobranchs) wdthout taking the trouble to inquire into the evidence. He agrees with Miss Piatt and Lamb that it degenerates and, like them, fails to prove the assertion. Miss Eraser ('15), whose paper is the latest dealing with the problem of the ontogenesis of the eye-muscles, is more cautious in her statements. She is willing to admit the possibility (p. 341) that in marsupials the second myotome "may contribute towards the formation of the m. externus rectus as in some fishes (Dohrn '04, Neal '09, '14)," but she adds "we have no direct evidence of this in Trichosurus."

Dohrn ('06) was the first to assert the persistence of the mandibular component of the external rectus muscle. He states in a foot-note (p. 243):

"bei Scyllium kann man sich mit. der grossten Sicherheit davon iiberzeugen, dass von einem Zugrundegenen des mandibularen Antheils des Rectus externus keine Rede ist, da man Schritt fiir Schritt die starkere Verdickung der Masse und die Bildung der einzelnen Fasern innerhalb diesser Masse constatiren kann, wahrend gleichzeitig die aus der III Kopfhohle stammenden Muskelfasern immer naher an die der Mandibularhohle aufriicken und zugleich von hinten her sparsamer werden, bis schliesslich die ganze Muskelmasse keinen Unterschied mehr darbietet."




Figs. 2 to 8 Semidiagrammatic camera drawings of certain stages in the ontogenesis of the external rectus muscle as seen in Squalus embryos of 18 mm. to 29 mm. length. The mandibular component of the external rectus muscle (Miss Piatt's muscle E) is shown in black with unshaded nuclei, while the hyoid component is drawn unshaded with black nuclei. Head-cavities 1, 2, and 3 are shown in topographic relation to the eye-ball only in figure 2. The anlage of the external rectus alone is shown in the remaining figures (3 to 8).

Fig. 2 The double-bimeric-origin of the external rectus muscle. The two components are in intimate contact from this stage on. The figure is drawn from parasagittal sections of a 20 mm. Squalus embryo. The division of the head cavities to form the six eye muscles has already begun.

Fig. 3 The anlage of the external I'ectus muscle in a cross section of an 18 mm. embryo of Squalus. The mandibular component (Mus. E. ) appears as a differentiation of the mandibular cavity, the lateral wall of which has already begun to disintegrate into mesenchyme. The multiplication of embryonic muscle cells in the median wall of the third head cavity has begun to obliterate the lumen of that cavity. In a 20 mm. embryo the conditions remain essentially unchanged (fig. 4).


The evidence which has convinced the writer of the persistence of the mandibular component of the external rectus muscle is summarized in text figures 2 to 8 of this paper. In earlier papers ('09, '14) the fact of its persistence was asserted, in agreement with Dohrn ('04), but no evidence was presented. The facts are as follows: In Squalus embryos of eighteen to twenty-four millimeters the anlage of the external rectus muscle shows two easily distinguishable elements, one (anterior) derived from the myotome of the mandibular cavity and which is recognizable as Miss Piatt's 'muscle E' the other (posterior) formed from the myotome of the hyoid cavity {mytm. 3) The two elements differ, not only in their staining properties, but the distinction between the two may also be made out, as Miss Piatt has stated, through the presence of a limiting membrane bounding the myotome of the third (hyoid) head-cavity. As a result, however, of the gradual disappearance of this membrane as development goes on it becomes increasingly difficult to distinguish the two elements. The difficulty is further increased because of the forward growth of myotome 3 (the hyoid element of the external rectus anlage), which comes eventually to lie above the mandibular element (mus. E.) Consequently, in embryos of 28 to 30 mm. it is possible to distinguish the two elements clearly only in cross sections of the muscle anlage. In still later stages the bounding membrane disappears altogether. A slight difference however in the direction of the long axes of the muscle fibers of the two elements makes it possible, even after the disappearance of the limiting membrane, to distinguish the two in cross sections. We see therefore that what disappears is not the mandibular element but the limiting membrane bounding the hyoid element, making it increasingly difficult and finally impossible to distinguish the two. Of the disintegration or degeneration of the muscle cells of 'mu-scle E' there is not the sHghtest evidence. On the contrary, in the stages during which degeneration has been said to occur, the embryonic muscle cells of both elements of the external rectus muscle undergo similar progressive differentiation as elongated spindle-shaped muscle fibers. In both, myofibrillae are visible in Squalus embryos of forty-five millimeters and transverse striae in embryos of one hundred milUmeters.



Fig. 5 The external rectus muscle as it appears in a 24 mm. embryo in frontal section. The muscle has thickened and elongated and the lumen of the third has disappeared. Cross sections of embryos at this stage show the muscle anlage much as in frontal sections (fig. 6).


Figs. 7 and 8 The external rectus is cut lengthwise in frontal (horizontal) sections of 26 mm. and 29 mm. Squalus embryos. In these stages it becomes increasingly difficult to distinguish the two components of the muscle, especially in frontal sections. The persistence of the mandibular component, however, is undeniable. Id, 2d, dorsal moieties of the first and second head cavities; Iv, 2v ventral moieties of the same; 3v, the third (hyoid) cavity; .E, mandibular component (mus. E) of the external rectus muscle; ch. chorioid layer of the optic vesicle; ep. epidermis; L, lens; ar, dividing line between dorsal and ventral moieties of the head-cavities.




Fig. 9 A camera drawing of a parasagittal section of a 5 mm. Squalus embryo (Series ICC 1-2-1) showing VanWijhe's somites 1 to 6. They are seen to be dorsal segments of the mesoderm and their segmentation to be independent of the visceral arches. A, the anterior cavity; 1, 2, S, Jf., 5, 6, VanWijhe's somites 1 to 6; F.B., forebraiu vesicle; g.s.' , first gill-pouch; M.B. midbrain vesicle; sp. spiracular pouch.


Concerning the ontogenesis of the other eye-muscles there is no difference of opinion. All later observers, including the writer ('98), have confirmed the results of Marshall ('81). It is quite unnecessary, therefore, in this paper to repeat the description of what is so well known. In the light of the evidence presented in this paper, however, it seems necessary to revise the well-known text-book formula for the ontogenesis of the eye-muscles as follows : From the first or pre-mandibular headcavity arise the muscles innervated by the oculomotor nerve, namely the recti superior, anterior and inferior, and the inferior oblique; from the second or mandibular myotome are differentiated the superior oblique muscle and the lateral portion of the external rectus; from the third head cavity develops the median portion of the external rectus muscle. A comparison of the old and new formula may be made in tabular form:

The old formula for the ontogenesis of the eye-muscles


SOMITE

Myotome 1.

My tome 2.. Myotome 3.

MUSCLES DERIVED

Rectus superior Rectus internus Rectus inferior Obliquus inferior Obliquus superior Rectus externus

Oculomotor Oculomotor Oculomotor Oculomotor Trochlearis Abducens

NUMBER

III III III III

IV VI

Revised formula for the ontogenesis of the eye-muscles

Myotome Id.

Myotome Iv.

Myotome 2d. Myotome 2v. Myotome 3v.

Rectus superior Rectus internus Rectus inferior Obliquus inferior Obliquus superior Rectus externus Rectus externus


Oculomotor Oculomotor Oculomotor Oculomotor Trochlearis Abducens

III III III III IV VI


But, however interesting and however important from the embryological point of view such an account of the ontogenesis of the eye-muscles in Squalus may be, it tells us little that is morphologically significant. The questions still remain unanswered — What is the morphology of the 'head cavities?' What has been their past history! To the answer to these important questions we may now turn our attention.'

The true morphology of the head cavities and the first reliable clue to the phylogenesis of the eye-muscles was revealed by VanWihje ('82) who showed that the head cavities are members of a series of mesodermic segments (somites) which, in Elasmobranch embryos, extend without interruption throughout head and trunk. He was thus able to demonstrate in craniote embryos an acraniote stage and to strengthen the conviction of morphologists that, in the ancestors of vertebrates, head and trunk were undifferentiated just as they are in Amphioxus today. The repeated confirmation of the presence of VanWihje's mesodermic segments in vertebrate embryos of widely divergent groups such as Cyclostomes (Koltzoff '01), Elasmobranchs (VanWijhe '82, Hoffman '95, Neal '96, Sewertzoff '98, Johnston '09, Braus '99), and Amphibia (Miss Piatt '97) and the demonstration that they are serially homologous with those of the trunk has finally established the long-contested fact that the eye muscles are members of the series of lateral trunk myotomes.

The proof of this conclusion is complete. , All of the objections formerly raised against the homology of pre-otic and postotic mesodermic somites (VanWijhe's) have been adequately answered, and a brief summary shows how convincing is the evidence in favor of their serial homology with those of the trunk: — VanWijhe's somites are continuous with those of the trunk; beginning with the neck region, their differentiation is progressive; they differentiate into myotome and sclerotome, the former coming from the median wall as in the case of trunk somites; like trunk myotomes they are innervated by somatic motor nerve fibers; their segmentation is quite independent of that of the visceral arches; and they are dorsal in relation to the notochord and dorsal aorta.

Their ontogenesis in Elasmobranchs shows that the differentition of the three anterior myotomes into the six eye muscles involves, primarily, the splitting of the myotomes into dorsal and ventral moieties. The process is exactly similar to the splitting of the post-otic myotomes of Petromyzon dorsal and ventral to the ear, and the facts suggest that in the ancestors of craniotes the lateral segmental muscles of the head region, in the course of phylogeny, became divided into dorsal and ventral elements as the result of a longitudinal splitting along the series of lateral line sense organs. Possibly, as many morphologists have thought, the lens and the otic capsule were at once time members of the series of lateral line sense organs. The dorsal and ventral moieties of the first myotome subdivide again, thus forming the four muscles innervated by the oculomotor nerve. The dorsal element of the second myotome forms the superior oblique muscle, while the ventral unites with the third myotome to form the external rectus muscle. While, in Petromyzon, the following myotomes split above and below the ear and persist in the adult, in elasmobranchs the myotomes of the fourth, fifth and sixth disappear in ontogeny, leaving an hiatus between the eye muscles and those of the trunk and bringing about their characteristic isolation as a group of muscles in the adult (figs. 17 to 20).



Fig. 10 A camera drawing of a parasagittal section of an 8-day (Naples) Petromyzon embryo, showing the mesodermic segmentation. The auditory placode lies just posterior to the third somite. Except for the absence of the anterior cavity, the mesodermic segmentation is comparable with that of Squalus fig. 8). Ent, entoderm; Ot, auditory placode; Som. 1, Som. 2, Som. 3, Som. 4 Som. 5, Som. 6, mesodermic somites 1 to 6; Sp. spiracular pouch; Spl. splanchnic mesoderm; Tb.N. neural tube (forebrain).


The morphological and phylogenetic significance of these facts is plain. Instead of being relatively young muscles which have not arisen directly from the segmental muscles (as asserted by Ziegler '08), and instead of heing post-otic muscles which have secondarily migrated into the preotic region (as suggested by McMurrich '12), the eye muscles are seen to be persistent portions of the pre-otic lateral trunk musculature which owe their persistence to a functional connection with the eye-ball. Their separation from the lateral trunk muscles and their isolation in the adult vertebrate are correlated with the great enlargement of the ear-capsule. Their presence in the pre-otic region therefore strongly suggests that in the ancestors of vertebrates the myotomic segmentation extended unbroken throughout the entire length of the body. Amphioxus is just such a form.


That the ancestor of vertebrates was Amphioxus-like is a very generally accepted conclusion of morphologists. In this connection the mesodermic segmentation discovered by Koltzoff ('02) in Cyclostomes (Petromyzon) is especially significant and important, since in this animal, according to KoltzofT, the segmentation of the cephalic mesoderm is primarily total and complete as in Amphioxus embryos and, moreover, the anterior mesodermic segments develop, as in Amphioxus, as dorsolateral diverticula of the entoderm. Furthermore, the lumen of each diverticulum is connected with the enteron just as in •Amphioxus larvae. If Koltzoff's observations be correct, Cyclostomes stand in this, as in other respects, intermediate between Amphioxus and Elasmobranchs. Koltzoff 's observations, however, have not been confirmed.


The importance of this evidence in its bearing on the past history of the vertebrate head has led me to examine sections of Petromyzon embryos in those early stages before hatching in which Koltzoff finds the mesodermic segmentation most clearly expressed. In at least two series of sections of eight-day (Naples) Petromyzon embryos the evidence presented seems to bear out Koltzoff's contention that the mesodermic segmentation in Cyclostomes is comparable with that of Elasmobranchs. While the 'anterior' cavities are wanting (just as in some genera of Elasmobranchs), the preotic mesoderm shows a series of divisions, the relations of which to adjacent organs are comparable with those of VanWihje's first, second and third somites. These are shown in text figures 10 and 11. If Koltzoff be correct in asserting that the eye-muscles of Petromyzon are differentiated from the walls of the first three mesodermic segments, their comparability with the first three somites of VanWihje is indisputable.



Figs. 11, 12, 13 Semidiagrammatic camera drawings of sections of Petromyzon embryos, showing the mesodermic segmentation in the region of the head. Figure 11 is from a parasagittal section of an 8-day embryo (Harv. embryol. coll. A, sect. 35-36). The topographic relations (and their later development according to Koltzoff '02) of the first three somites show them to be homologous with the first three somites in elasmobranchs.

Fig. 12 Cross section of an i8^day Petromyzon embryo through the region of somite 2 (fig. 11). The similarity of the somite to the mesodermic pouches of .linphioxus is obvious.

Fig. 13 is a cross section of a slightly older Petromyzon embryo cut in the region of the fourth somite, showing the differentiation of somatic and splanchnicmesoderm. 1, 2, 3, 4, Somites 1-4; cd.d. notochord; en<, enteron;o<, auditory placode; sp. spiracular pouch; spl, splanchnic mesoderm; Ih.n. neural tube.


I regret that my own observations are not sufficiently extended to enable me to confirm Koltzoff's statement, but I know of no reason for doubting his conclusions. If they are correct, Petronyzon resembles an Acraniote in having all of its myotomes persist in the adult. In all other Craniotes at least some myotomes in the ear region degenerate in embryonic stages. Koltzoff's discovery consequently now puts us in a position to compare a larval Craniote with a larval Amphioxus and thus to carry the history of the eye-muscle back to an Amphioxus stage, that is, to a stage before eyes were differentiated. Here, however, we are confronted with the difficulty of exact homology between the myotomes of Amphioxus and those of Craniotes.


The absence in Amphioxus of eyes, ears and serial brain vesicles deprives the morphologist of the accustomed fixed points of comparison. The considerable divergence of opinion regarding the metameric homologies of Amphioxus is, therefore, not surprising. The most reasonable conjecture appears to the writer to be the assumption that the first permanent myotome (VanWijhe's 1st) of Craniotes is exactly homologous with the first permanent myotome of Amphioxus. This supposition is strengthened by the relations to the 'anterior cavities.' For, in both Amphioxus and Craniote embryos, are found mesodermic masses or paired cavities anterior to the first permanent myotomes. These are the 'anterior entodermic diverticula' of Amphioxus and the 'anterior head-cavities' of Craniotes (Elasmobranchs and Ganoids) . The exact homology of these mesodermic cavities is based, not only on their relation to the first permanent myotomes, but also on the important circumstance that in Ganoids (Amia) the anterior head-cavities open to the exterior by an external opening, just as do the anterior entodermic diverticula of Amphioxus, in which the left cavity opens to form the pre-oral pit. In Amia (Reigard '02) they open to form the suckers of the Ganoid larva. Similarly in Balanoglossus, it will here membered, theanterior (proboscis) cavities open to the exterior by the proboscis-pore, which is sometimes right and sometimes left in its position. -Since these cavities are the most anterior in the chordate body, since they lie immediately anterior to the first permanent myotomes and since they open — or at least one of them opens — to the exterior in Amphioxus and a Craniote (Amia), and since they are peculiar in this respect, their exact homology seems not unreasonable and strengthens the assumption of the homology of the first permanent myotomes in Craniotes and Acraniotes.


Figs. 14, 15, 16 Diagrams of acraniote stages of cyclostome and elasmobranch embryos in comparison with a larval Amphioxus. All three show an homologous mesodermic segmentation. 1, 2, 3, 4, etc., somites 1, 2, 3, 4, etc; a, anterior cavities;c.s.^., club-shaped g\a.nd;end, endostyle;^.s.°, first (transient) gill-pouch; g.s.' first (permanent) gill-pouch; hyp. hypophysis; L, lens; M, mouth; N, nasal pit; n'ch, notochord; ii'p. neuropore; ot, otic capsule; sp. spiracle; th'r, thyreoid.




Assuming, therefore, on the basis of this evidence, the exact homology of the latter, the history of the eye-muscles may be seen to be the history of the transformation of the first three myotomes of an Amphioxus-like ancestor into the definitive six eyemuscles of man. This history may be very briefly summarized: Primarily, as in Amphioxus, the three anterior myotomes were members of an unbroken series of segmented muscles extending throughout the entire length of the body. When lateral line organs and enlarged cranial ganglia associated with them made their appearance, the anterior myotomes became split lengthwise into dorsal and ventral moieties. Further separation and displacement followed the enlargement of the optic and otic vesicles. In this way eventually two sets of muscles, one dorsal and one ventral, were brought in close proximity to the enlarging optic vesicles with which they finally became functionally associated (figs. 17 and 18).


How these two sets of muscles became gradually transformed into the eye-muscles is revealed by their ontogenesis in Elasmobranchs. Each of the divisions (dorsal and ventral) of the first myotome divides again, thus forming the four muscles innervated by the oculomotor nerve. The second myotome undergoes no further subdivision. Its dorsal moiety becomes the superior oblique muscle and is innervated by the trochlearis nerve. Its ventral portion, however, unites with the third myotome to form the external rectus muscle and becomes imiervated by the abducens nerve. The dorsal moiety of the third myotome does not differentiate muscle fibers. Like the myotonies of somites four, five and six, it has disappeared phylogenetically, leaving the eye muscles as an isolated group unconnected with the postotic myotomes (figs. 19 and 20).


During the phylogenetic transformation of the eye muscles noteworthy changes occur in their nerve connections. Since, however, these have been discussed at considerable length in earlier papers by the writer ('09, '12, '14), and since no facts are presented which are irreconcilable with the conclusions stated above, it seems unnecessary to do more than refer to them here. While the first myotome retains throughout phylogenesis its primitive nerve relations to the oculomotor nerve, the somatic motor nerve of the second myotome (the trochlearis) acquires a dorsal chiasma and retains connection only with the dorsal moiety of the muscle. The ventral portion, uniting with the third myotome, becomes innervated by the abducens nerve, the somatic motor nerve of a more posterior metamere. The conclusion that such modified metameric nerve relations may have occurred through a process of nerve substitution or piracy is in harmony with what we now know of the method of nerve histogenesis (Harrison '11) and of the primary independence of nerve and muscle (Parker '10). Consequently the modified metameric nerve relations of the eye muscles present no serious objections to the phylogenetic conclusions reached in this paper.



Figs. 17, 18 Pre-gnathostome stages in the history of the eye muscles. Diagrams based upon the myotomic relations in Amphioxus and Petromyzon embryos. All of the mj^otomes persist in Petromyzon (Koltzoff) as in Amphioxus, but they split into dorsal and ventral moieties in the case of the five anterior ones. Abbreviations the same as in figures 14 to 16.


Figs. 19, 20 Diagrams showing two later stages in the phylogenesis of the eye muscles, based upon their ontogenesis in elasmobranchs The myotomes which degenerate in ontogeny are indicated by dotted lines. In figure 19 the anlagen of the six eye muscles are already differentiated. Their relation to the dorsal and ventral moieties of the myotomes is indicated. The adult relations of the muscles are seen in figure 20. They remain essentially the same m man. Id, dorsal moiety of the first myotome; li\ ventral moiety of the first myotome; M, 2v, dorsal and ventral moieties of the second myotomes; Sv, ventral moiety of 'the' third myotome; a, anterior cavities; 7, seventh myotome; g.s.\ first gillslit; hijp.m, hypoglossus musculature; .1/, mouth; N, nasal i)it; ol, otic capsule sp, spiracle; Ih'r., thyreoid.



Objection to the foregoing description of the phylogenesis of the eye muscles may be raised on the ground of the uncertainty that Amphioxus represents a form ancestral to vertebrates. To some this will seem a serious objection. But that Amphioxus embodies more completely than any other existing animal the general characteristics of the chordate type from which the Vertebrates have sprung, is an opinion held by the great majority of vertebrate morphologists. Familiarity with embryonic and larval stages of Amphioxus, Cyclostomes, and Elasmobranchs greatly strengthens the conviction that this opinion is sound. The evidence presented in this paper is in full accordance with the belief.


An attempt to carry the history of the eye muscles back into pre-chordate stages leads eventually to the problem of the origin of the segmental musculature — in other words to the problem of the origin of the mesoderm. The logic of the previous discussion would lead to the conclusion that originally the eye muscles w^ere metameric diverticula of the invertebrate intestine. Further than this we could scarcely proceed.

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