The Prootic Somites of Heterodontus andof Amia.

By

G. R. dc Beer, B.A., B.Sc, F.L.S.,Fellow of Merton College, Demonstrator in Zoology and Comparative

Anatomy, University Museum, Oxford.

With 16 Text-figures.

1. HETERODONTUS.

THAT the prootic somites in the head of the vertebrate giverise to the muscles actuating the eyeballs is a fact so wellknown as to require no comment. As the result of the workof Marshall (7) it was understood that the eye-muscles, ofwhich there are six, arise in three groups, each group fromone prootic somite. The first group, consisting of the superior,internal, and inferior recti and the inferior oblique, arise fromthe first or premandibular somite, and are innervated by theoculomotor nerve. The second, to which the superior obliquealone belongs, is produced by the second or mandibular somite,its nerve being the pathetic. To the third, consisting of theexternal rectus, the third or hyoid somite gives rise, and it isinnervated by the abducens. Neal (8), in a recent and carefulwork on S qua I n s , has, however, slightly modified thisscheme. According to him the external rectus muscle hasa double origin. Part of it is formed from the hyoid somiteand part from the mandibular. The element contributed bythe mandibular is in his opinion the posteriorly directed processof the mandibular somite named muscle E by Platt (10), itsdiscoverer. While it is generally supposed to disappear,Dohrn (3) was of the opinion that muscle E persisted, and NeaJ

NO. 209 C

I S 0. H. DE BEER

asserts that it is actually incorporated in and forms part of theexternal muscle.

The eye-muscles of S q u a l u s have also been, studied byLamb (6), according to whom muscle E vanishes at a stagewhen the embryos are 26 mm. long. The external rectus wouldtherefore be independent of the mandibular somite in itsdevelopment. I have examined preparations of the appro-priate stages of S q u a l u s , but failed to be convinced thatmuscle E persists. Nevertheless I regarded the matter asbeing in an unsatisfactory condition, and when through thegenerosity of Mr. P. D. P. Murray I came into possessionof a series of embryos of H e t e r o d o n t u s p h i l i p p i , Iinvestigated the development of the eye-muscles in this inter-esting and comparatively little-known form.

In my earliest stage (11 mm.) the prootic somites are stilllarge and contain spacious cavities. The mandibular somiteretains connexion with the general coelom through the mandi-bular arch. Posteriorly the mandibular somite runs obliquelyventrally,so that the hyoid somite overlaps it for a short distancefrom behind and above ; the two somites are just in contact.Immediately lateral to the point of overlap of the somites isthe large ganglion of the trigeminal nerve. All these structurescan be discerned in a transverse section (Text-fig. 1). Areconstruction as seen from the left side is given in Text-fig. 7, a.

The premandibular somite lies ventral to the main body ofthe mandibular somite, which position it owes to the curvatureof the head. Not much attention will be paid to its laterhistory, since its further development is typical and thereis no controversy as to the muscles to which it gives rise.

At the next stage (14 mm.) the mandibular somite has lostconnexion with the general coelom, and forms an elongatedstructure lying horizontally. Posteriorly it is still overlappedby the hyoid somite, the cavity of which has shrunk as thewalls become thickened. The two somites are in contact butthe limiting membranes separating them are plain (Text-figs. 2 and 7, b).

Lateral to the somites at this point there is, as before, the

PROOTIC SOMITES 19

ganglion of the trigeminal. The profundus ganglion is joinedto the trigeminal by a connexion which passes down medianto the mandibular somite. This somite is therefore externaland dorsal to the profundus, a condition which persists in theadult where the superior oblique to which the mandibularsomite gives rise is dorsal to the ramus ophthalmicus pro-fundus (Text-fig. 3). The hyoid somite at this stage is still

TEXT-FIO. 1.

H e t e r o d o n t u s p h i l i p p i , 11mm. transverse section, showingthe hyoid somite overlapping the mandibular.

Explanation of lettering of Text-figs. 1-7.ab, abducens ; exr, external rectus ; / , facial; hy, hyoid somite;

infr, inferior rectus ; inob, inferior oblique ; inr, internal rectus ;m, mandibular somite; oc, oculomotor; opn, optic nerve;p, profundus ganglion ; pa, pathetic ; pm, premandibular somite ;top, ramus ophthalmicus profundus ; ro>, combined superficialophthalmic nerves; ros V, ramus ophthalmicus superh'cialistrigemini; ros VII, ramus ophthalmicus superfieialis facialis ;sudb, superior oblique; sur, superior rectus ; tm, thick mesen-chyme ; tr, trigeminal.

largo, and the greater part of it is still posterior to the trigeminalganglion. The superior ophthalmic branches of the trigeminaland facial nerves are formed, but there are as yet no ventralroots.

c 2

20 G. R. DE BEER

TEXT-FIG. 2.

m -^=r^r

lmm.

O ,-v- ft-r-

Hetorodontus, 14 mm. transverse section.

_ f

tr--U-

- -ros V

Hete rodon tus . Reconstruction of 14 mm. stage seen from above.The brain has been cut horizontally and the upper part removed.

PROOTIC SOMITES

TEXT-FIG. 4.tr hb

21

mEsob

Hete rodon tus . Longitudinal vertical section, 21 mm. stage.

TEXT-FIG. 5.

He te rodon tus . Transverse section, 22 mm. stage. The muscle Eis very small.

22 G. R. DE BEER

A vertical longitudinal section at a stage 21 mm. long(Text-fig. 4) shows the mandibular somite extending forwardsclose to the profundus ganglion. The cavity of the somite islateral to the section ; the walls are beginning to take on theform of muscle. The anterior portion of the somite is madeup of cells densely packed together and staining deeply. This

TEXT-FIG. G.

hb-- - ros VII

H e t e r o d o n t u s , 25 mm. transverse section. Muscle E hasdisappeared.

is the rudiment of the superior oblique muscle. The posteriorportion is composed of cells which are looser, and constitutesmuscle E. This can be seen to underlie the hyoid somite fora short distance. The cavity in the hyoid somite has becomemuch reduced, and the rudiment of the external rectus muscleis forming. It is not easy to decide whether there is a mixtureof the elements of the two somites at the point of overlap.The membrane surrounding the hyoid somite is still visible,and muscle E appears to show signs of degenerating. Nealcontests that no proof of any such degeneration has been given,

PROOTIC SOMITES 23

and indeed it is not easy to give, but its cells are less tightly-packed than in the external rectus rudiment, and they are hotorientated in any particular direction. In transverse sectiona very similar stage (22 mm., Text-fig. 5) shows muscle E asa thin plate of cells lying beneath and slightly to the outsideof the hyoid somite, and just touching it.

The mandibular and hyoid somites are during this timemoving forwards. The rudiment of the superior obliquemuscle extends anteriorly over the ramus ophthalmicus pro-fundus and over the eyeball (Text-fig. 7, c). The hyoid somiteno longer lies behind the trigeminal ganglion, but the posteriorends of both are at about the same level. The abducens hasarisen slightly behind the facial, very close to the middle line,and extends forwards to the hyoid somite. The oculomotor,passing ventral and median to the ramus ophthalmicus pro-fundus and the superior oblique, innervates the premandibularsomite.

From now onwards comes the critical point in the elucidationof the problem of the fate of muscle E. Already small at 22 mm.r

I cannot find it at later stages at all. The hyoid somite, whichmust now be called the external rectus muscle, appears to behomogeneous all through. There is no trace of the incorpora-tion of foreign elements, which should be discernible if present.The anterior extremity of the.external rectus lies close to theeyeball and the layer of denser mesenchyme which surroundsit. As this is the region which muscle E occupied at previousstages, it is my opinion that it breaks down into mesenchymohere. This mesenchyme, cut tangentially in a transversesection of a 25 mm. stage, is shown in Text-fig. 6. Whethermesenchyme cells originally forming part of muscle E are,after disappearance of the latter as such, incorporated in theexternal rectus I cannot tell; but even if this were so it wouldnot justify the statement that the external rectus arises fromthe somatic musculature of two segments. After breakingdown into mesenchyme the elements of muscle E must losetheir somitic value.

The superior oblique continues to move forwards until it is

24 G. R. D E BEER

TEXT-FIG. 7.

inob

H c t c r o d o n t u s . Reconstructions seen from the loft sideshowing the development of the eye-muscles in embryos of11 (A), 14 (B), 21 (c), 37 (D), and 70 (E) mm.

PHOOTIC SOMITES 25

the most anterior of all the eye-muscles (Text-fig. 7, d, 37 mm.stage). It is innervated by the pathetic, which passes downbeneath the superficial ophthalmic. The premandibularsomite, which at a previous stage had developed a pair ofdorsally and a pair of ventrally projecting buds, has now com-pletely split up into its muscles. The superior and internalrecti extend dorsally over the optic nerve and the ramusophthalmicus profundus, the inferior oblique and inferiorrectus extend forwards ventrally beneath the optic nerve.

In Text-fig. 7, e, a reconstruction is given of a 70 mm. stagein which the conditions cannot be very different from whatthey are in the adult. The external rectus, which extendslaterally in front of the trigeminal, has been followed by itsnerve, the abducens. The abducens follows the wanderingsof the hyoid somite, for which reason it passes forwards medianto the facial and trigeminal nerves and emerges from theskull anterior to the maxillo-mandibular branches of thelatter. Thus, although it is the ventral root of the thirdsegment, it passes in front of the dorsal root of the secondsegment.

The oculomotor has divided into two branches, of whichone supplies the internal and superior recti, the other passesround behind the superior rectus, under the ramus ophthal-micus profundus, in front of the external rectus, and innervatesthe inferior rectus. Passing still further forward beneath theoptic nerve it innervates the inferior oblique.

The relations of the eye-muscles to the ophthalmic nerves arenot constant in Selachians. In He te rodon tus the internalrectus passes over the profundus and thus lies dorsal to it.In Squalus the profundus passes dorsal to the internalrectus (Norris and Hughes, 9) which is precisely the opposite.In ScyIlium the profundus while it persists is ventral tothe internal rectus, and similarly in Amia (Allis, 1). InMustelus and Galeus (Allis, S) the profundus passesthrough the internal rectus.

With regard to the superior rectus, the profundus passesventral to it in He te rodon tus , Squalus, Po lyp te rus ,

26 O. R. DB BEER

and A mi a ; it passes dorsal to it in Galeus, and through itin Scyll ium.

The internal reetus passes above the optic nerve in Hetero-dontus , below it in A mi a and Salmo.

The only constant relations are those between the superioroblique and the profundus, the latter being always ventral tothe former. That this should be so is understandable from thedevelopment, for the mandibular somite lies over the profundusfrom the earliest stages. The positions of the other musclesare not fixed until much later, and there is no reason why therudiments of the superior or internal recti should not grow andextend to one side or the other of the profundus, or straighttowards the nerve so that the latter comes to be enclosed bythe muscle. Variations in relations between muscles can beaccounted for in this way without violating the principle thatventral roots remain faithful to their segment's muscles andfollow them about in changes in ontogeny.

It is precisely this principle which would be violated if theexternal reetus were partly composed of muscle E. This wouldmean that some musculature belonging to the second segmenthad been abandoned by the pathetic nerve and captured bythe abducens, for there is no question of the pathetic or anybranch of it having anything to do with the innervation ofthe external reetus. Pacts must of course not be made sub-servient to principles, but in such a case as this the persistenceof muscle E in the external reetus must be established by strongevidence. I have not been able to find such evidence inHe te rodon tus . The inclusion in the external reetus ofisolated mesenchyme elements derived from the degenerationof muscle E is another matter. It is possible that this occurs,but even then, in the absence of evidence to the contrary,I believe that in Hete rodontus at any rate the externalreetus is not made up of two somites.

2. AMIA.

In young specimens of Amia in which the trunk somiteshave not yet specialized to form muscles, the line of somitesis not continuous right up to the front of the head, as it is in

PROOTIC SOMITES 27

Selachians for example. The earliest stage investigated wasthat in which the embryo lies completely on the surface of theyolk and occupies about 220 degrees of the circumference ofthe yolk. There are visible at this stage one prootic head-cavity, a line of postotic somites starting just behind therudiment of the vagus nerve, and the adhesive organ. The

TEXT-FIG. 8.

ado

Longitudinal vertical section through an embryo of A m i a c a 1 v a ;early stage showing adhesive organ and the single head-cavity.

Explanation of lettering of Text-figs. 8-10.<xh, abducens ; adm, adductor muscle; ado, adhesive organ; cs, con-

necting stalk of head-cavities ; dw, dorsal wall of gut; ep, epithe-lium ; epart, efferent pseudobranchial artery; exr, externalrectus ; fb, fore-brain ; fg, fore-gut; g, gut; k, hypophysis ;lib, hind- brain ; he, head-cavity; ;', infnndibulum ; ig, isolatedganglion; infr, inferior rectus; inob, inferior oblique; inr,internal rectus ; mb, mid-brain ; n, notochord ; oc, oculomotor ;ol, occipitale laterale cartilage; opn, optic nerve; ov, opticvesicle ; pa, patheticus ; pm 1, first permanent myotome ; rsur,rudiment of the superior rectus ; tm 1, first transient myotome ;tr, trigeminal; sg 1, first spinal nerve ; suob, superior oblique ;sur, superior rectus ; v, vagus ; vr 1, first ventral root; vr 2,second ventral root ; y, yolk.

space between the head-cavity and the postotic somites isoccupied by mesenchyme not showing a trace of segmentation.The head-cavity and the adhesive organ are shown in Text-

28 G. R. DE BEER

It is puzzling that there should be only one head-cavity,,and it is improbable that earlier stages, had they been available,would have revealed other somites in this region, for Eeighardand Phelps (11), who have studied the development of theadhesive organ from the earliest stages, state that in their

TEXT-FIG. 9.

-y

A m i a . Reconstruction of a o-o mm. embryo. The head is repre-sented as cut transversely, and the observer is looking forwardsat the posterior face of the anterior part. The other organs areseen by transparency.

investigations no trace could be found of any other prooticsomites.

The question arises as to which somite the head-cavity ofAmi a represents. A pair of sacs lying behind and betweenthe optic vesicles and lateral to the infundibulum, they fill upmost of the space between these structures and the mid-brainat a stage 5-5 mm. in length. A diagrammatic reconstruction

PROOTIC SOMITES 29

of the front portion of the head as seen from behind is shown inText-fig. 9, a transverse section through the head-cavity inText-fig. 10, and a reconstruction from beneath in Text-fig.14, a.Immediately posterior to the infundibulum the two cavities,one on each side, communicate by a cord of cells which becomeshollowed out into a tube.

TEXT-FIC. 10.

~adm

A m i a . Transverse section, 5-5 mm. stage, showing the head-cavityand the oculomotor nerve.

In other chordates, the only segment in which the rightand left somites communicate is the premandibular or first.This communication is in a precisely similar position, viz.behind the infundibulum and in front of the end of the noto-chord. It looks then as if the head-cavity of Amia were thepremandibular somite, and this conclusion is confirmed by thefact that in the stage referred to above the oculomotor nervecan be seen clearly, issuing from the brain and going to the head-cavity (Text-fig. 10).

30 G. R. DE BEER

It is clear then that the remaining prootic somites, i.e. man-dibular and the hyoid, must not be looked for in front of thehead-cavity. Two possibilities are open. Either they occurredbehind the head-cavity and have broken down early intomesenchyme, or else the single head-cavity, as well as repre-senting the premandibular somite, contains the mandibularand hyoid somites also, all fused together. In this connexionI may quote from Reighard and Phelps : ' In one specimen ofthis stage, although the cavity was continuous on the left side,it consisted on the right side of three isolated cavities containedin the common sheet of mesoblast.' I have also observed this,and in Text-figs. 11 and 12 are diagrams of some sectionsthrough the heads of two specimens, with reconstructions ofthe head-cavities represented as seen from beneath with theventral walls removed. It is at once apparent that not onlyare the subdivisions incomplete, but they differ in the twospecimens and on both sides of the same specimen. In oneof them there is apparent subdivision into three, and in the otherinto two. In the majority of specimens there is no subdivisionat all. Further, the connecting stalk from one side to the otheris not associated with the anterior subdivision, but with thesecond. If the anterior subdivision alone represents thepremandibular somite, the connecting stalk should be foundthere.

The conclusion is, therefore, that the head-caA'ity representsonly one somite, and that the rnandibular and hyoid somiteshave broken down into mesenchyme and are not recognizableas such. The apparent subdivisions of the head-cavity haveno significance. The proof of this conclusion is to be found inthe development of the eye-muscles. For if the head-cavityrepresents only the premandibular somite, only four of the sixmuscles can arise from it, viz. recti superior, inferior, internal,and the inferior oblique.

The earliest differentiation to appear is that of the rudimentof the superior rectus (Text-fig. 13) at the posterior end of thehead-cavity.

At 6 mm. in length the superior rectus rudiment is distinct

TEXT-FIG. 11 .—A m i a. a to h, longitudinal vortical sections through early stage, showing apparent subdivision of the head-cavity.i, Reconstruction of the latter seen from below with the ventral surface removed.

1mm

.

TEX

T-FI

G. 1

2.—

The

sam

e as

Tex

t-fig

. 4 in

ano

ther

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en.

Th e

sub

divi

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s of

the

hea

d-ca

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are

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con

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PBOOTIC SOMITES 3S

and the rest of the head-cavity extends forwards. Behind itand separate from it the external rectus has appeared, in-nervated by the abducens (Text-fig. 14, b). There is noevidence of the external rectus having been budded off fromthe head-cavity, and there is no visible somite from which it

TEXT-FIG. 13.

A m i a . Transverse section, 6 mm. stage, showing the rudimentof the superior reotus muscle arising from the head-cavity.

arises. It must therefore be formed by condensation of themesenchyme which exists in that region, and which representsthe broken-down hyoid somite.

At 7 mm. (Text-fig. 14, c) the rudiments of the previous stagehave become more distinct, and the inferior oblique is separate.The remainder of the head-cavity, apart from the superiorrectus, represents the rudiments of the internal and inferiorrecti. These two muscles are distinct at 11 mm. (Text-fig. 14, d),

NO. 269 D

34 G. R. DE BEER

and also the superior oblique has appeared, innervated by thepathetic. It also has no connexion with the head-cavity.

Of the six eye-muscles, therefore, four (innervated by theoculomotor and arising from the premandibular segment)are formed from a definite somite ; the other two, representingthe somites of the mandibular and hyoid segments, are formedfrom mesenchyme. In those forms in T e l e o s t s where no

TEXT-FIG. 14.

A m i a . Reconstructions of the head-cavity and eye-muscles, a 5-0 mm..6 6 mm. from below ; c 7 mm., d 11 mm. from the left side.

prootic somites can be distinguished, presumably all the eye-muscles must arise by the latter method. It is interesting thatAmia should retain the primitive method only for onesomite, the premandibular.

It is of interest to compare the relations of the eye-musclesof Amia, a Teleostome, with those obtaining in Sela-chians such as He te rodon tus . The relations of the

PROOTIC SOMITES 35

muscles of both groups to the optic nerve are constant exceptfor the internal rectus. This in He te rodon tus (andSqualus and presumably all Selachians) extends forwardsdorsal to the optic nerve, whereas in Arnia (and Salmo andTeleosts) it lies beneath the optic nerve.

There is also a variation in the distribution of the oculomotornerve. In Hete rodontus it divides into two branches,the dorsal of which innervates the internal and superior recti;the ventral branch goes to the inferior rectus and oblique.In Ami a I find, in agreement with Allis (1), that the oculo-motor divides into two branches, the dorsal of which suppliesonly the superior rectus ; the internal rectus is not innervatedby this branch but by the ventral one which passes in frontof the external rectus, beneath the inferior rectus which itinnervates, and then forwards to the inferior oblique supplyingthe internal rectus on its way.

The eye-muscles of Amia and Hete rodon tus cannothave been independently developed, but must have been derivedfrom those of a common ancestor. Whatever the relations inthis ancestor may have been, they must have been such as tobe capable of modification into either of these two types, if onewas not derived from the other. The possibility of thesemodifications lies in the facts that the muscles grow andextend during their development, and so may come to beardifferent relations to the relatively fixed structures such asthe optic nerve, and that the nerve is not connected with themfrom the beginning but grows freely towards them. The changeneed not be attended by any functional discontinuity, becausethe fibres supplying the internal rectus may change theirposition of exit from the oculomotor nerve and yet retainconnexion with the internal rectus without having to passthrough any other structures. Intermediate stages in thetransition from Hete rodontus to Amia, or vice versa,or from an intermediate condition to either, are shown inText-fig. 15.

The fact that a number of somites has broken down intomesenchyme prevents the possibility of counting the number

D 2

36 G. R. DE BEER

TEXT-FIO. 15.

sur

infr

Diagrams of the relations to the oculomotor nerve of the superior,internal, and inferior recti muscles in A, H e t e r o d o n t u s ; Band c, hypothetical stages in the passage from one to the other orfrom an intermediate condition to either showing that thetransition can be effected without functional discontinuity;D.Amia.

PROOTIO SOMITES 87

of segments included in the head of A mi a. In the occipitalregion, with Schreiner (12), I find four somites anterior tothe one innervated by the first ventral root behind the occipi-tale laterale cartilage, which marks the posterior limit of theskull. This is one more somite than Allis (1) describes. Ofthese four somites the first two, which have no ventral roots,degenerate. There are then two permanent myotomes infront of the occipitale laterale. These segments are z and «,

TEXT-PIG. 16.

A m i a . Reconstruction of the occipital region from the right side, 11 mm.

according to Fiirbringer (4). Actually which segments theseare cannot be told without the complete series of somitesbetween the prootic and postotic regions.

In discussing the prootic somites of Ami a it is perhapsnecessary to mention the adhesive organ. This organ (Text-fig. 8) arises as a pair of lateral pouches of the fore-gut. Thereis no doubt that it is a structure which develops muscle anteriorto and separate from the premandibular somite, but this doesnot prove that it is of somitic value. It is regarded by Reighardand Phelps as homologous with the anterior head-cavity ofS q u a l u s , but the somitic value of that has not been demon-strated satisfactorily (see Goodrich, 5).

3 8 G. E. DE BEER

SUMMARY.

1. The external recfcus of He te rodontus is not partlycomposed of the mandibular somite.

2. The only prootic somite recognizable as such in A mi ais the premandibular.

3. The muscles representing the mandibular and hyoidsomites arise from mesenchyrne in A m i a .

4. The relations of the eye-muscles to the optic nerve andthe distribution of the oculomotor differ in Amia andHete rodon tus .

LIST OF LITERATURE.

1. AUis, E. P.—" The cranial muscles and nerves in Amia ", ' Journ.Morph.', 12, 1897.

2. " Lateral sensory canals of Muatelus ", ' Quart. Journ. Micr.Sci.', 45, 1901.

3. Dohrn, A.—" Die Mandibularhohle ", ' Mit. Zool. Stat. Neapel', 17,1904.

4. Fiirbringer, M.—" Uber die spino-occipitalen Nerven ", ' Festschr. vonGegenbaur.' Leipzig, 1896.

5. Goodrich, E. S.—" Proboscis pores in Vertebrates ", ' Quart. Journ.Micr. Sci.', 62, 1917.

6. Lamb, A. B.—•" The development of the eye-muscles in Acanthias ",' Am. Journ. Anat.', 1, 1902.

7. Marshall, A. M.—:' On the head-cavities and associated nerves ",' Quart. Journ. Mier. Sci.', 21, 1881.

8. Neal, H. V.—" The histoiy of the e3^e-muscles ", ' Journ. Morph.',30, 1918.

9. Norris, H. W., and Hughes, S. R.—"Nerves of Squalus ", 'Journ.Comp. Neur.', 25, 1920.

10. Platt, J. B.—" A contribution to the study of the vertebrate head ",' Journ. Morph.', 5, 1891.

11. Reighard and Phelps.—" The development of the adhesive organsof Amia ", 'Journ. Morph.', 19, 1908.

12. Schreiner, K. E.—" Einige Ergebnisse iiber den Bau, etc., von Amia "',' Zeit. wiss. Zool.', 72, 1902.