Paper - On the development of the human diaphragm (1901)

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Mall FP. On the development of the human diaphragm. (1901) Johns Hopkins Hospital Bulletin 12: 158-171.

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On the Development of the Human Diaphragm

Franklin Mall (1911)
Franklin Mall

By Franklin P. Mall.

Professiir of Anatomy. Johns Hopkins University.

In a paper on the development of the human cadoni, puljlislicd several years ago, I was not able to give a detailed description of the separation of the body cavities from one

' Mull, Jour, of Morph., vol. la, 1897

another, because the specimens at my disposal did not include all the necessary stages. For that study I used 19 human embryos between 2 and 2-1 mm. long, in which various stages of the development cf the body-cavities were shown, but a number of the important stages were missing.

During the past three years the collection of human euihryos in the anatomical laboratory has grown very rapidly anil all the missing stages for the study of the formation of the body-cavities have been supjilied. The following table gives a list of these embryos. It will be seen from it that




between tln' be^innill;:' or tbe la.-^t period and



lenji:th in mm.

of the seetion.


iin whom obtained.

the abortion.



41 days



Ellis, Elkton, Md.


3 . .5







3S days



Hoen, Baltimore.

I.XXVI. ..

4.. 5



.Vliteliell, Cliieago.

LXXX ...








.56 days




Halifax, N. S.



5.5 days




SpringHeld, 111.



53 days



C. O. Miller,






Gray, Washington.



5 weeks



Lamb, Washington.

CXIV ....




Gray, Washington.













XLiir ....










Irving Miller,


the series from 2 mm. upward is very complrir with the e.\ception of stages between 11 and 14 mm. long. Fortunately, the missing stages are not important. All the embryos given in this talile are practically perfect, the imperfect ones liaving been excluded. The present study is based u|hiii !•") embryos, only 3 of which are included in the 19 specimens considered ill (he earlier communication.

Il has often been stated thai Ihe development of lln diaiihrngin, i'S]i('cial]y in the Inmian embryo, is one ol' III!' iiiiisl (liHiciill |ii'ol)lenis of embryology, fiarty because (if the dilliciilty ill obtaining the iiecessaiy s|ii'ciiiii'ns ami partly heeaiisi' there are no fixed points rioni whiih In enleulate. Ill its (h'\i'loi)ment the wliole ilia|ilii'aeiii wiuiilers rrom the head (o the abdomen, passing Ijy as well as iiinilil'vino the structures and organs along the way. Sn. while vmi Baer recognized that the diapjliragm wandered in its development, picking up its nerve in so doing, a fairly clear pic tiiiv of the whole process was not given until Ilis studied eaicfiilhthe develo|iiiieiit of the iieelc, heart, lungs and intestine. In his studies His recognized the Aiihiijc of the diaiihiagin in a mass of tissue located with thi' liearl ainniiesl struct iiics lieloneing to the head and eonlaining within it the \'eiiis to the heart as well as the An/age of the liver, 'i'his mass of tissue ITis termed tbe septum transversuni. Ilis's studies

were made ui)on the human embryo, mainly by the method of reconstruction, and .shortly after they were published Uskow made a very careful study of the further growth of the septum transversuni. Uskow recognized the great importance of two additional structures in the formation of the pericardium and adult dia])hragm from the septum transversum; these he termed the iileuro- pericardial memhranc, containing the phrenic nerve, and the pillars which form the dorsal ends of the diaphragm. The pillars of Uskow have been termed the plcuro-periioncal memhranes by Brachet, and as the lattiT lei'in is more appropriate than the former I shall employ it in the present paper.

j\ly own studies show that the pleuro-pericardial and pleuroperitoueal membranes arise from a common structure, which extends from the lobe of the liver along the dorsal wall of the ductus Cuvieri to the dorsal attachment of the mesocardium. Ijater this structure grows towards the head to complete the jileuro-pericardial memlirane and then towards the tail to complete the pleuro-peritoneal mendirane. This stiiietnre, which I shall term the pulmonary ridge, is located in the sagittal plane of the body-cavity with cephalic and eandal horns on its dorsal side. The ductus Cuvieri lies between these horns (Fig. 29).

The purpose of this paper is to follow carefnlly the fate of the septum transversum and the origin and fate of the liulmonary ridge in the human embryo. In so doing il is of course necessary to consider the division of the body-cavity into the pericardial, pleural and peritoneal cavities. According to liis, the body-cavity in early embryos is divided into the Parietallwhle and Bumpflwhlen. The communicati-ou between these spaces he has also termed the recessus parietalis. The parietal cavity from its earliest appearance contains the heart and is destined to form the pericardial cavity. T shall term it the pericardial coelom. A portion of the recessus ]iarietalis forms the pleural cavity; it surnninds the lung bnd throughiuit its development and I shall term it the pleural eoeloin. The revnainder of the recessus |iai-ielalis to the origin of the liver has developed in it the liver and stomach; this is added to the general peritoneal cavity and I sliall term it the periloneal cculom. In the early embryos the whole eieloni lies far out of place; in F.mbryo XII nearly Ihe entire cadoin lies in the region of the head and iieek ami in the further develn|inieut of these parts the cadom with Ihe surrounding organs wanders away from the head to its |iermanent location. .\s long as the serous cavities arising from the codom are in tlu' process of wandering and are mil fnlly separated from one another I shall term them ]ileuial, pericardial and peritoneal coelom: when they are fnlly established I shall call tlieiii cavities.

Ill Embryo .\li, lig. 1, the cceloni of the embryo forms a fi'ee s|iaee eueiicling the heart and extending on either side of the body over the om|ihalo-mesenterie veins to the root of till' nmhilieal vesicle. This canal of commuuieation has ile\ elo|ieil wil hill il t he lung, stomaeh and li\'er, nml I hroiighoni its eai'lier ile\elo|iiiienl it measures in length ahoiit one-fourth of thai of Ihe hoilv (iMiibrvos XII, (IXLVIII, LXXVI,



[JJos. 121-122-123.

LXXX,, II and C'J.Xlll). The appearam-i' of the lun,;;- and liver marks the sul)divit;ion of the (•(I'loni iiiio the jileural and jjeritoiieal cadojii. W'ilh tlie dexeldpnient of tlie liver, limy and stomacli tlie e(eliini einilainiiiL;- them gradually dili:te>' until the emhryo is ahout !• nun. long, when the canal evaginate.s, so to speak, and Inrns the liver and stcnnaeh ont into the general pei'iloiienl cavity. The Wolllian liody, which (iniqiiod the dorsal A\all of this canal, gradnally degenerates and the Inng takes its place. From these statements it is readily inferred that the canal extending from the pericardial cceloni, Ilis's recessns parietalis. gives rise to the ]ilenral codoni on its dorsal side and to the peritoneal cielom on its ventral side. The line of division is formed hy the plenro-jieritoneal memlirane extending from tlic ductus ( 'uvieri to the adrenal.





Fig. 1. — Pniiilc recmistnictiou of tliu eiiibryo 2.1 mm. loug. No. XII X liT times; m/i, amnion; iii\ optic vesicle; nc, auditory; vesicle hc, umbilical vesicle; h, lieart ; I'om, omi>lialo-meseuteric vein; mr, septum trausversum ; Oj, tUird occipital myotome; t'j, eiglitli cervical myotome.

The earliest emhryo in my collection in which the sejitum transversnm is well formed is No. XII, 2.1 mm. long, and about two weeks old." The specimen is very valuable for the .study of the beginning of so many structures that it also Ijecomes a good starting [loinl fur I lie study of the dcNclnpment of the diaphragm.

Figs. 1 and 2 give the external fcuin and oulline id' Ihe neural tube and alimentary canal drawn from a reconstruction. It is seen that the c(el(nH sends two canals into the

■-' Ditfereut pictures of this emliryo will be fimiul in the; .ImiiiiMl of Morpli., vol. 13; Ilis's Arcliiv, IS'.lT; .lolins Iloplviiis Hospital Hnllctin, IS'.IS; and the Welch Festschrift, .lohus llopkius Hospital Heports, vol. '.I.

head on either side of the neck which comniuiiicate with each dlhei- ill tile immediate neighliorhood of Ihi' nKUith. This U-slia|ied canal is sepaialed fidiii the exocielom on its ventral side by a Ijridge of inesodermal tissue connecting the umbilical vesicle with tlij embryo at the juncture of the head with the aiimion. It follows that this liridge of mesodernial tissue, the sepliim transversuni, is also U-shajied, as is shown in l-'igs. 1 an<l 2, iST and ilA//. ll forms a jiortion of the ventral wall of the pericardial cadom and sn]iports the omphalomesenteric and nmliilical veins. Sections of it are shown in Figs. 3, 4 and 5, which are from three sections through the head end of this embryo in the neighborhood of the first cervical myotome. The Aiilage of the liver is shown in Fig. t. which is located in this stage in a region belonging to the head.




Fui. 2. — Parlial dissection of the reconstruetiou of the embryo 2.1 mm. long. No. XII x 37 times; dm, amnion; m, mouth; Hi', Br", lirst and second braneliial pockets; /, thyroid; p, pericardial coelom ; .■i^ septum transversuni ; I, liver; kc, nQibilical vesicle; /«•, neurenteric canal.

Figs. G to 9 are from an emhryo (CLXIV) slightly more advanced in development than No. XII. The embryo is from an ovum measuring 1 T x 17x111 mm., found in the uterus at an W'lii'ii the uterus was cut o])en the knife entered the ovum and |Hissil)ly distorted tlie emliryo, for when it came into my hands it was foimd that the emliryo was lloating in the cavity nf Ihe ovum Imt il was still adherent to its walls. This mechanical injury iindoiilitedly caused the body nf the embryo to straighten and at the attachment of the iiiiibilical vesicle the body <if the embryo is bent towards the \entral side, as is the case in a number of the His embryos (for instance, I'>H). The ventral wall over the heart, was also slightly torn. The entire uterus and ovum had been

ArRIL-MAY-JuXE, 1901.



liTcservod on ice fni' 2[ linurs, mid wlicn it was jiiven io iiie Iiy l»r. ^lacCalhiiii tiic i.'iitiic s|MMiiiic'i\ was iila<Til in sti-on>^ formalin. The si't-tioiis dl' tlic ciiilirvo sliiiw thai the tissuesi ore slightly iiiaceiTited Imt in i^cncral they arc well ]ire?orv<'(l. The spinal ecinl is (■l(ise<l ihnui.uhont its extent Iml thi' iiourcniore is still open. The thyi'oiil iiland. ii]i(ic and otic



Fig. o. — Section tlirougU tlic lirad <if tlie embryo '2.1 mm. loiii;-. No. XII X 50 times; rue, coelom ; /</i, pluiryiix ; /, liver; xl, seiitum transversura ; irr, vesicle.

vesicles, heart and veins, are but slightly more developed than ill N^o. XII. If this enihryo were curled up as No. XII it would measure froni 2.5 to 3 mm., whih' if the two had lunn hardened in the same way (Xo. \ll was hardciicil in ahohdl) they would ])rolialily measure alike.

Fig. 4, — Section tlnnnu'li tlie tliird occipital myotome of the cmhryo 2.1 mm. Ions. -"I mm. nearer llic lail tlian Fii;. 11 x .">(! times; (l.j, tliirel occipital myotome ; c«c, coelom ; /■, vein ; .■</, septinn transvcrsnm ; !, liver; pli, pharynx; "c, umbilical vesicle.

The figures given sliow the general relation as sei'ii in I'lmliryo .Xll with e;u-h id' the st laict ui'cs hut slightly iuhaiii-ed. The septum transversum is much the same as it is in .Xll, while the pericardial co'lom is puslied more to the ventral side of it and (he diverticidinii to tnini the liver is more marked. The iindiilical vein has extended somewhat (Fig. 9) and the jugular vein has made its appearance (Fig. T).

The tissue of the septum transversum in the two embryos is formed of irregular round cells, between which there are numerous vessels, of irregular diameter, which commnnicate freely with the veins to the heart.

The next stage of the develupment of the septum trans

'A ' ' !'


Coe ;'



Fig. 5.— Section throusli the first cervical myotome of the embryo

i.l mm. lonic, .'IS mm. nearer the tail than Fiir. 4 x .iO times ; f\ lirst cervical myotome; toe coelom ; ;■», umbilical vein; ;"'/», omplialo-mesenterie vein; iiiiib, umbilical vesicle.

versnm is found iu an embryo 4.3 mm. long (CXLVII), obtained from llr. Iloen.' The specimen is perfect and normal, as it was obtained through uiechanic;il means. The entiro


Fig. (i. —Section throun-h the head of the embryo 3. .5 mm. long. No. CLXIV X .'iO times; y</(, pharynx ; i«, bullius aortae ; cc/j/, ventricle.

ovum was hardened in S(i |ier cent alcohol shortly after it was expelled from the uieiais. This of course fi.xed the embryo in its natural shape, as was the case with No. XII. iioth embryos are cnrved, but in the emliryo 4.3 mm. long the lii-aiiehial region occupies relatively more space than it

'A photograph of this embryo is given in the Welch Festschrift.



[Nds. 121-122-123.

does in the embryo 2.1 mm. long. In proportion to the length of the embryo.? this distance h;is inerensed 3 times, Tlie pericardial cfrlom has receded i'roni the head in |)r()]iortion to the inerenso of the growth of the branchial arches. In the emliryo 2.1 mm. long i\\v kead end of the |ici-ieardiai crelom is oiiimsHe (he otic vesicle, while in the end)rvo 1.3

Fig. 7. — Section tlirdiiuli tlu' embryo o..5mm. loiiir. .14 mm. nciirur the tail Fis;. x ."'O t mcs ; p/i, jiljai-ynx; lui, auricle; rent, venfiicle; .■it, septum tr.ansversum ; <;/, jugular vein ; /'», umbilical veiu.

mm. it is o])]iosite the first occipital myotome. The puint u\' comnnmication between the peritoneal coelom (encircling the liver) with the exococlom has also receded. In the embryo 2.1 mm. lung it is opposite the second cervical myotome; in embryo 4.3 mm. long opposite the second tlioraeie myotome

Fig. S.— Section tlirougb the embryo S.6 mm. long, .'2 mm. nearer the tail than Fig. 7 x .50 times ; I, liver; wiit, ventricle ;.«»■, siuus renuieus; coc, coelom.

(compare Figs. 1 and lU). Ilis's embryo Lr (4.2 mm. Imig) is intermediate between the t\V(i embryos just compaicil. In Lr (see liis's Atlas, Pis. IX and XI | llie ]ierieardial. |ileural and peritoneal creloni encircling tlie liver extends from tlie first occipital myotome to the sixth cervical, and the omphalomesenteric veins jirotrnde into these canals of the co'lmn. The liver has extended into the septum transversnm but does not yet encircle the omphalo-mesenteric veins as it does in

my embryo 4.3 mm. long. This detailed descri])tion is given to show the fate of the ccelom ' of the hea<l and neck. It gives rise to the pericardial and ]iit'ural cavities, and tliat portion of the ]U'ritoneal cavity encircling tlie liver of (he adult. Sections of the embryo 4.3 mm. lung ( Xo. C.XIjVIII. Figs. 11 and 12) show the livei' sprouts growiiio' in all dii'cc

FiG. 9. — Section through the embryo 3..'> mm. long, .is mm. nearer the tail than Fig. S x .50 times; rvw, coelom; ii:l, intestine; rum, (^mphaln-mcsenteric vein ; /■//, umlulical vein.

tious tlinuigli the sejitum transversum. encircling and ramifying through the omphalo-mesenteric veins, making a condition slightly in advance of that in Ilis's embryo Lr. The sections of this embryo show clearly that the heart, lungs, liver and li'Wer peritoneal cavity arise in tissues surrounded by that portion of the cadom extending into the head in Embrvo XII,

Fig. 10. — Outline of the embryo 4.:! mm. long. No. CXI.VIII x 1.5 times. ,, first cervical myotome; r',, ei!?t cervical myotome, 'llie line imlieates tlie dii'ection of the sections.

Fig. 1. Fig. 11 is taken from a section through a plane cutting the root of tlie arm and the otic vesicle, and can readily lie placed in the outline, I'ig. 1(1. It is seen that the lung.-arise wlicre the pericardial ecelom goes over into the pleural, /. ('. high up in tlie region of the head. Immediately on the dorsal side of them is the beginning of the lesser ]ieritoiieal

' Kopfbohle ; ITalsboble; I'arietallioblc ami recessus |i;n-iel:ilis.

Ai'hil-May-June, 1901.]



cavity, and the intestinal tnbe struck in this section is the stoniacli. All these stnietnrcs lie on the cephalic side of the first cervical myotome. Projecting into the peritoneal ccelom, encircling and penetrating the omphalo-mesenteric veins are the projections of the liver. Figs. 11 and 13, L. The two lohes rrai-h I'rom the tip of the Inngs ami the foramen of Winslow to the point wliere the entodermal cells of the liver arise from





Via. 11. — Section tlirougb the embryo 4.3 mm. Innsr x 2.5 times; T,, lirst tlioracic myotome; C, C,, and (\, cervical myotomes; .s', stomacli ; fti, brdnchus; /i, heart; (, thyroid; /<■•, pericardial cavity; I, liver; />, foramen of Winslow.

llic aliinentaiy canal, or in this ease the iluodcimm. The lobes of the liver lie entirely within the canals of the coelom on either side of the head. The caudal ends of these coelom canals have migrated from opposite the second cervical myotome ill Emliryo XII, Fig. 1, to opposite the second thoracic

.. ^T^


UV /




L *


Fig. 12.. — Section throush the embryo 4.:i mm. loun, .4 mm. deeper than Fis;. 11 x 2.") times; /, thoracic myotomes; ;, intestine; /, liver; /', ventricle; bii, bulb of the aorta; nm, amnion; iii\ umbilical vein.

myotome in Embryo CXLVIII, Fig. 10. It has moved towards the tail eight segments, while the cephalic end of ilie canal, the ]iericardial ccelom, has been kinked over to correspond with the bending of the head, has dilated to correspond with the growth of the heart, and has receded from the otic vesicle to (lie extent of the gi'owlb of I he linincliial arches. We have in this embryo the necessary stage to Imnte tlie organs which arise in the neighborhood of tin; sepiiim tiaiW'

versnni, as well as to give the fate of the ccelom in their immediate neighborhood.

A stage somewhat in advance of CXLVIII is ]A.\^M. The embryo is slightly larger, measuring 4.5 mm. in greatest length. It was obtained from the uterus 7 hours after death. The entire ovum was placed immediately in aljsolute alcohol.

Fig. 13. — Section through the embryo i.n mm. long. No. LXXVI x 2.5 times; /'c, cardinal vein; l/jc, lesser peritoneal cavity; <lc, ductus Cuvicri; xc, sinus vcnosus.

It was impossible to obtain a picture of the embryo before it was cut. but the specimen proved to be an excellent one. The direction of the sections is more nearly transverse than



Fig. 14 Section llirougli the embryo 4.5 mm. long, .il nnn. deeper

than Fig. IS x 25 times; we, cardinal vein; u, aorta; nnii. omphalomesenteric vein; fii, umbilical vein; /i, heart.

in CXLVIII. In CXLVIII the neuropore is closed with a thickening of the e|iidermis just over the point of closni'e; the umbilical vein entei's the liver and its direct connection with the ductus ('ii\ieri through the body wall is cut oil'. In LXXVI the neiiid|ioic is completely closed and the eiiilii'yo is somewhat lai'ger than hefore (compare Figs. i:i and I I with II and 12); the umliilical vein, however, coiiiniiinieates with I ill- (liictus Cuvieri tiirough the body-wall on the left



[Nos. 121-1^2-123.

side. This Ls an instaiifc nf rctardcil (li'vclii|inii'nt of a part, as tlie left iimliilical vein t^liniild lia\r \alli^lu■d liy lliis time. Fig. 13 gives a seel ion lliniiigli llie tdi-anien nf Winslow imniediately on tlie caudal side (if tlie lung liuds. as shown in a lateral view of the nuidel of the eniljvyo. Fig. 1-"). The

Fig. I.

se]ituni transversuui and liver have increased in fpiantily. as a e(nn|iarison of tlie dilVerent tigui'es will show. In tliis

Fig. 1G.

Figs. 1.5 .iiul Ifi. — Riirlit aud left views o( ,t roconst ruction of the embryo 4.. T mm. long x 2n times; n, aort.i ; ph, pli;ir\ii\ ; Im, hulbus aort;e ; me, coelom ; /), purieardiiil coeloin ; /, lung'; li, liver; Wb, Wolffian body ; ■«, stomach ; ./>, foramen of Winslow ; .«■, sinus veuosus ; "I, septum transversum.

stage we have the extreme bending of the head, which throws 'the heart to its most ventral ])oint with the septum transversum aliout parallel witli long axis of the embryo. The


Fig. it. — Lateral view of the reconstruction of an ciuliryo .5 mm. long. No. LXXX x 17 times; I, hinir; li, liver; s, stomach: dc, ductns Cnvieri ; pr, pericardial coelom which communicates fully with pi euro- peritonea I coelom.

position of the heart, lungs, liver and their relation to the cadom is much the same as in the younger embryo with the

exception of the lesser ]ieritoiieal cavity, which is now more to the i-audid side i.if the limits.

While ill the embryo 4..'! uini. long llie niyoiomes were well formed and hollow, in the iMuliryo 4..") they are solid and contain embrvonic muscle ii'nes. The dorsal ganglia are also


Fin. Its. — Section through the nceU and heart of embryo LXXX x 2.T times; ,, fourth cervical nerve: iv, cardinal vein; </(-, ductus Cuvieri; Of, oesoi>liagus ; //-, ti'achea : .sr, sinus renniens.

more developed. In the I'lubiyos ."i mm. long (LXXX and ('.XXXVI) the myotomes are still further difTerentiated with nerve tiimks. composed of lioth dorsal and ventral roots, which are growing into the body-walls of the embryo. Figs. IT-.'O give the general form of this embryo, in reconstruction

Fig. 111. (Section through embryo LXXX .:.'•_' mm. deeper than Fig.

IS X ;i.") times; C, fifth cervical nerve ; fv, cardinal vein ; .i, subclavian vein; ih; ductus Cuvieri ; I, lung; pli, phrenic nerve.

as well as in section. The se]itum transversum is not as perpendicular as in either younger or older stages (LXXVI and II), but in general this embryo is intermediate between them. A separation between the jiericardial and ]ileural ca^lom now Viegins to make its appearance by means of a constriction in its walls, the ductus Cuvieri encircling the cwlom at this point. The hing buds hang free into the pleural ccelom,

Apkil-May-June, 1901.]



iiiul the liver and stomacli into the peritoneal eo'lmii. Tli.^ dnctus t'livieri lieb in a riilue of tissue eneirclini;- tiie lanal di coniniunieatitin lictween the pericardial and pleiiial iddniii. In this eniliryo the ridge has no mesentery, as descrilied by His {V\g. 18), hut in sagittal sections of the same stage (CXXXVI) tlie mesentery is yiresent. As yet there is no

KiG. 20, — Section tlirousili embryo LXXX, .2(i mm. deeper tli;iii Fiij. li) X 2.5 times; <',.,. si.xlli cervieiil myotome; <i, aorta; iv, eardiual vein; .«, stomach; ", iiinljilical vciii ; //«•, lower peritoneal cavity.

indication of a line of se|iai'ation between the plciiial and peritoneal cceloni in LXXX. Imt in ('XXX\'l ihei-e is an elevation on the d(ii>;d wall (d' llie |il('iiial cii'lniii, lig. 21, wliieh encircles the long ami joins the dnrsal end of the s('|itnni li'ansversniii, 'i'his is one of the ]iillars of Uskow

FiG. :ll. — Sa'jiltal section tliroii2;li an embryo, ."> mm. lonii;. No. CXXXVI X 2'} times; /i, lieart; i-i\ cardinal vein; xl, septum transversuni ; ', hoii;-; .s, stomacli; k, arm; jir, pulmonary rid:;'e.

(ir the beginning <>( a ridge which I shall term the juiliiioiiiiri/ ridi/e.

Fig. 20, coni]iared with Kig. 1o. shows that tlu> foramen ol" Winslow has moved more lapidlv Inwards liie tail than the Iieart. A section through it strikes the heart sqnarely in one case, while in the nther it does not tmieh the heart hwi strikes the li\cr mily. This is in [lai't i\\tt' ti> the direction of the sectiiiii in thi' Iwd specimens, and in |iiii'l to the shifting of till.' fdrameii uf Winslow with (lie recession of the

stomach. The cervical nerves are sefiarated in No. LXXX with the exception of an anastomosis lielween the fourth and the liltli. j-riim this piiint the pliri-nic nerve arises. Fig. 19, and passes to the lateral side of the parietal ccelom and lung. In a later stage it reaches the se])tum transversum through the plenro-]iericardial menilirane of I'skow.

I have now followed the transformation of the relatively sim]ile C(el(iiii of the head and neck from the time it is well I'diiiied ill an embryo of the end id' the second week to the end of the tiiird week. During this time tiie pericardial cadom has moved away from the head and the pericardial cavity is well lUitlined. but the membranes which divide the ccelom intii pcriearilial. pleiiial and jieritnncal spaces have not yet

FiQ. 'J2. — Rccoustnictiou of embryo No. II x 30 times; 7>, bronclins; X, liver; P/i, plirenic; 1, ,?, ,?, 4 branchial pouches.

appeared. During the foui'th week both of these membranes a]ipcar, but llicy are not well delined iiiilil the fifth week.

Fig. 22 is from a profile rcconslniclinn of I'hnbryo 1 1, showing the relation of the organs to tme another. A cast of the colon of this embryo is given in Fig. 23. The extreme ventral kinking of the heart is shown in this stage and from now on it begins to sink more and more into the body as the liver recedes, 'i'lie cinnmunieation lictwecii I lie pericardial cielniti and the |ilciiral eoelom is reduced to a narrow slit lietween the Cephalic end of tlie lung bud and I lie iliictus Cuvieri. It a)i]iears as if a simple adhesion of the walls of the slit would. com|ilctr the closure of the pericardial space. Fig. 24 is a .section Ihroiigh this space, striking the seventh cervical myo



[Nos. 121-123-123,

tome and the tip of the phrenic nerve. It shows that the nttachnient of the ductus Cnvieri is no longer hroad, as in rnibrvd IjXXX, Ijiit is narrow, formino- a mesentery as de

fiG. 23. — Cast of coelom of embryo II x 20 times; /', perieiirclhil coelom ; L, coelom encircling to liver.

scribed by His. On the dorsal side of the ductus there is a ridge wliicli liegins as tlie ductus projects into the coelora and gradually I'luis over into tlie lobe of the liver. Tliis ridge is very pi-ononiiced and is also well shown in llu> sections of



Fig. 24. — Section tlirousb the seventh cervical segment of the embryo 7 ram. long. No. II x 2.5 times; ('., seventh cervical myotome; rv, cardinal vein ; ili; ductusCiivieri ; ?<)•, brachial iilexus; /(/•, pnlmi>?i;ny ridge; ///(, jihrenic nerve; h, bronchus; h, heart; hn, bulbns aorta'.

His's emljryos. A and 1>, as given in his Alhix. The relation of this ridge to tlie phrenic nerve as well as its form in older endiryos makes of it the Anlfuje of both the pleuro-])ericardial and pleuro-pcritoneal membranes. It lies in the sagittal plane

of the coelom and as it passes the region of the fourth and fifth cervical noi-ves receives into its substance the phrenic nerve which ]iasses on tlie caudal side of the ductus Oiivieri. Soon the lung bud grows against this ridge, causes it to bulge. and with the rotation of the liver towards the head the ridge

Fig. 35. — Section through the embryo 7 ram. long, .6 ram. deeper than Fig. 24 X 2.5 tiraes ; T,, first thoracic myotome ; ci\ cardinal vein: Tl'fi, Wolffian body; .<:, stomach; Ipc, lesser peritoneal cavity; ?, liver; //, heart; kI, septum transversum.

is divided into two parts; (1) the cephalic end which retains the phrenic nerve and ductus Cnvieri and forms the pleuropericardial membrane, and (2) the caudal end which remains attached to the tip of the dorsal end of the septum trans

Ph :'^





, ^ Li.

Fig. 26. — Sagittal section through the embryo (>..5 mm. long. No. CXVI X 25 limes; /jA, ]>haryn\; /j/-', first branchial arch; 6'(, bulbns aorta'; (f, auricle; /'. ventricle; ^ Inng ; //, liver; />i\ pulmonary ridge.

\ersum and the liver mi the one hand, tlie body-wall on the other, til f<iriii the ]ilcui(i-|ieritoneal membrane.

Figs. 26-28 show tliis ridge in sagittal sections in Embryo rXVI. a specimen not (piite as large as No. II, but somewJiiit

Ai'eil-May-June, 1901.]



more advanced in developnu'iit. In P^ig. 26 its cephalic end a])])ears as a broad menibiaiie which in a section nearer the middle line extends to the liver on the ventral side and'



^ L'.v





Fig. 27.— Section tliiougli tlic embivo 6..5 mm. louir, .1 mm. deeper than Fig. 26 x 2.5 times, /i/i, pbarvux ; <(, arm; pi; ijulmonary ridge ; I, luug.

it begins to widen at its dorsal end hand in hand with tlu rotation of the liver. Fp to this time the se]itnm transversnm is pai-allel witli the vertebral eohimn. with the heart




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Fig. 28. — Section tlirough tlae embryo 6..5 mm. long, .13 mm. deeper tliau Fig. 27 x 2.5 times; <«■, oesophagus; n, aorta; I, lung; li, liver; 11'/), Wnltliuu body ; jir, pulmonary ridge.

Fig. 29. —Lateral view of the iniliiionary membrane and surrounding parts of the embryo 7 nun. long. No. II x 30 times; «, auricle; , ventricle; /, lung; /(, liver; II A, Wolllian body; ///•, pulmonary ridge; ., eighth cervical myotome.

aecoiMpaiiics the ductus Cnvieri to the body-wall mi tlic dorsal side, I""ig. 21, pr. Stil more towards the midlino the ridge ends as a decided elevation iiuiiicdiately to the eainhd side of the ti]) of the lung.

After the lailnionary ridge is well formed (as in I'hnbryo IT)

on its venti-al siiU' ami tlie liver on its dorsal side projecting into the ]ici-itoiieal eodom, as shown in No. H. This eondition was hruught about at the time of the bending of tln' head when the viscera were forced towards the tail and into this position. The cejihalie end of the pericardial crelom



[Nos. 121-122-123.

is tluis Lent over the septum transversum but the nuiin part of the head (•<vloiii remained parallel with the si)iiial eoliiiiin on either .side ol' llie liody. This process may he termed tlu: rolling over of the heart.

In the next stage the heart rolls in a dorsal diret-lioii and the liver in a ventral direi-lion. 'i'his process has already hegnii in endiiyo CLXIII and C^XllI. In so doing the lung buds become Ijuried deeper in the body of the embryo and the liver gradually changes its |iosilion from the dorsal side

Fig. 30. —Lateral view of the pulinoniiry membraue and siinomuliii!;parts of tlie embryo '.I mm. lont;; No. CL.XIII x 13i.< times, (\, eiiihtli cei-vical myotome; //.liver; I, liiuir; ■■-■, stomach; 1I'6, Wolfliaii botly ; y>/(, plirenic nerve; y«', pleuro-perieardial membrane ; ^/yj. pleuro-peritonuMl mcnihraue.

of the septum transversum to its ventral side. The septum transversum undergoes almost a half-revolution. The cudom containing the liver lobe evaginate.s and becomes incorporated with the general ahdiuniual ca\ity.

I'"iii. 31. — Section through the filth cervical myotome of the embryo '.I mm. Icing, No. CLXIII x l-}^ times; (',,, llfth myotome; (•<■, cardinal vein; tir, ductus cuvieri ; br, brachial ple.xus; jih, phrenic nerve; /ir, cephalic end of the pulmonary ridge forming the beginning of the pleuro-pericardial membrane.

\\'itli (lie rolling of the heart the cielom connecting the pericardial with the pleural space is kinked at the points of juncture between these cavities. At this point the duct of ( 'uvier enters the heart. Soon fi-om its dorsal boi'iler the ]nihnonary ridge arises which is semicircular in form and reaches from the liver to the dorsal walls of the credom as ilescribed under I'hid.iyo II. It is shown in section in Fig. 'H, and in a lateral reconstruction in Fig. 20. The pulmon

ary ridge is really an extension of the septum transversum from the lobes of the liver to the tij) of the AVolffian body. ,Vs the heai-t nio\'es in the dorsal direction and the liver in the ventral dii'ection it is the dorsal end of the septum trans

'^•^'HCoc/— -^ ^^e^, — ' — Ph


Fig. 33. — Section through the embryo '.I nun. louir, -Wi mm. deeper than Fig. 31 x 12,'.; times; ('„, si.xth cervical myotome; •■/•, cardinal vein; p/i, phrenic nerve; jjc, pleuro-pericardial membrane; ////, plcuroperitoneal membrane; pl-cve, pleural coeloni ; /j-mc, peritoneal coelom.

versum which moves most ra])idly in the cbrection of the tail. In so doing the pulmonary ridge grows rapidly and divides at its dorsal end into two memtiranes, one containing the

Fig. 33 Section through the embryo '.I mm. long, .10 mm. deeper

than Fig. 33 x 13)^ times; C^, eighth cervical nerve; pp, pleuro-peritoueal mcmbi-anc.

Fig. 34.— Section through the embryo !) mm. long, .84 mm, deeper than Fig. 33 x 13).^ times; y,,, third thoracic myotome; //«■, lower peritoneal cavity ; 117), Wolfliau body.

duct of Chivier ;ind phrenic nerve, and the other still encircling the lung bud. In this division we have the beginnings of the jdeuro-pericardial memhrane of ITskow, and tlie pleuroperitoneal mendjrane of Brachet.

Apiul-May-June, 1901. J



'Pill' iiiiliiiiiiiary ridpo is well formed in Embryo II. It appears as a ridge of tissue passing towards the head from the lobe of the liver on tlie dorsal side of the ductus Cnvieri and then aloui;- th.e dorsal walls ol' the rcrhim to the meso



Fig. 3.5. — Sagittal section tlirnuijli the unibrvo s nini. loiii:. No. C'XIII x 10 times; J, lower jaw ; .s-^z-uc, siuus lu-aecervicalis ; ;, fouitli cervical nerve, /)/(, phrenic nerve; st, septum transversuin; ih\ iluctus Cuvieri ; /)<•, pleuro-pericarilial membrane; pp, pleuro-peritoiieal membrane; /, lunif; ,v, stomach; 'yjr, lower peritoneal cavity ; T'/i, Wolffian body.

(■ai-(liuiii. \\liere it ends in the pillars of Uskow. As the einhryi) gidws larger tlie ductus t'uvieri separates more and mnic friiiu the latei'al liody-^all. and in a incasurt' sliifts intn the [lulmonary ridge, whieh at its nidst emne.x point grows in the form of a ridge towards the heart. This secondary ridge, which is present in C'LXIII. linally se|)arates the ]ilenral from the pericardial cavities and comiiletes the jilcnro-pericardial membrane.

Ki<i. :i(I. — Section through the embryo S mm. lony nearer the mitldlc line tliau Fiif. 3.5 x 10 times; ;/'■, ductus Cuvieri; I, lung; .«, stomach; Pli, pleuro-peritoncal membrane.

Tile piilniiiuary ridges from thcii' beginning to tlieir separation into the pleuro-pericardial and pK'urn-pri'itcnu'al niemliranes a]ii)ear as two ears to the se[)tum transversiun, c-\tending along the ducts of Cuvier in tlie sagittal plane id' the body and at right angles to the phiiie of tlie septum trnnsversnm. Judging by tlie relatimi n\ the phrenic iier\c to the ])ulmonary i-idge tlie poi'tion (d' it I'n tlie dorsal siih' (if the ductus Cu\ieri Clint, Lining the phrenic nerve, the pnrtimi containing the ductus Cuvieri. and the sccimdaiy ridge nf the

ventral side of tlie ductus Cuvieri, form the pleuro-pericardial membrane, 'i'he portion of the pulmonary ridge on the caiuhil side nf tlie ]ihrenic nerve gives rise to the pleiirnperitiiiie;d mend ii a lie. In so doing it gradually shifts over



Fig. S7.— Sagittal section through the embryo 10 mm. long. No. CXIV X 10 times; /(/j, pleuro-peritoneal membrane.

the lung hulls and iinally t'omplctely separates the jileuial rriiui the peritoneal cavities.

The growth of the plenro-pericai'ilial meiiihr;ine towards

Fig. 3S. -Lateral view of the embryo 11 mm. long, showing the pleuro-pericardial and pleuro-peritoneal membranes. No. CIX x S.'.j times; /-, lirst rib; /, lung; 11, liver; p/i, phrenic nerve in the pleuropericardial memljrane; .s, stomach; ir6, Wollliau body; (ip. pleuro-peritoncal membrane which is not quite completed.

the head ami the ]ilenro-peritoneal towards the tail widens the dorsal projection of the septum transversuin and iiiin this wide hasi' the lung Ijurrows throwing the jileuro-ii.'ricard-ial membrane with the phrenic nerve to its medial side. The fate of the pulmonary ridge is shown in Fig. 3(1. which is from lOmbryo CL.XIII. Sections of this embryo are shown in l-'igs. 31 to 31. They show again that the pulmonary ridge reaches rroiii the diietus Cuvieri to the ti|i of the lung, and the phieiiie nerve. It is readily seen from Figs. 30 and



[Nos. iai-122-123.

o2 liow the ])lirenic nerve is pushed to its permanent position liy the further rotation and recession of tlie septum (ransversum and livei'. ajid the lateral growth of the lungs to encircle the heart.

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Fig. 30. — Section through the body of the embryo 11 mm. long. No. CIX X 10 times; /i/i, plirenic nerve; yjc, pleuro-pericardial membrane; .s7, septum transversum ; //. humerus; .;, tirst rib; .', second rib; /, third rib.

Figs. ;J.j and 3lj are from sagittal sections of iMnlu-yo (.'XIII, which is of the same stage as CLXIII. The iihrenic nerve is shown throughout its whole course from the fifth cervical nerve to the pleuro-])ericardial memhrane. The nerve receives a second hi'anch a few sections deeper frmn the sixth cervical which unites with the main trunk hefore it enters


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Fio, 40. — Section through the embryo 11 mm. Ion;;; .IS mm. deeper than Fig. .39 x 10 times; /;/<, phrenic nerve; st, septum transversum; P'-, pleuro-pericardial membrane; pjj, pleuro-periloneal membrane; J, ,.-', ,)', 4, ribs.

the pleuro-pericardial nienil)rane. Hanging from the pleuropericardial memhrane is a section of the pleuro-|ieritoneal, which in Fig. 36 unites with the dorsal wall of the cndom at the head end of the Wolffian body.

About this time the portion of the ])ulinonary ridge des

tined to heconii' the plcuro-]ieiicardial membrane unites with the root of the lung hud and com]iletely closes the pericardial cavity, Fig. 37. By this union the course of the duel us Cnvieri is from the body-wall to the heart throtigh the pleuropericardial mendirane, and the plane of the pleuro-pericardial

Fig. 41 Section through the embryo 11 mm. long, .46 mm. deeper

than Fig. 40 x 10 times. The pleuro-peritoueal membrane is incomplete on one side, .;, j, .7, i:, ribs.

membrane is jiractically that of the septum transversum, the two together being transverse to the body of the embryo. The phrenic nerve at this time is in the plane of the septum transversum and reaches its dorsal tip through its projection, the pleuro-pericardial membrane.

Immediately aftei the completion of the pleuro-pericardial



Fig. 42. — Sagittal section through the embryo 14 mm. long. No. CXI.IV X 10 times, ///>, phrenic nerve; /'/, tenth rib; .s, stomach ; /,-, kidney; 11', Wolllian body.

membrane the rotiition id' the liver and septum transversum is accelerated, and by the time the embryo has grown to be 11 mm. long (CI.X). tlie liver is practically in its adult position. The rapiil rotation of the liver, especially at its dorsal end, has elumged the relation of the planes between the

April-Mat-June, 1901.]



pleuro-pericardial membrane to tlie septum transversiim from parallel to right angles. Now the septum transversum is in ^ the plane of the plenro-peritoneal membrane (Fig. 38). With' the recession of the septnm transversum, especially at its


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Fio. 43. — Section tlirough tbe opening between tlie pleur-il and peritoneal cavities in the embryo 14 mm. long x .'50 times; .s, stomach; I, hing; /<p, pleuroperitoneal membrane; nr?, adrenal.

dorsal end, the evagination of the co?lom containing the liver and stomach is complete, throwing them into the general peritoneal cavity.

Figs. 39, 40 and 41 are sections through the plenro-peri

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Fio. 44 Sagittal section through the body of the embryo 10 mm.

long. No. XLIII X 10 times; .9, ninth rib.

cardial and plenro-peritoneal membranes of Embryo CIX, Fig. 38. They give the relation of the pleuro-pericardial and plenro-peritoneal membranes to the surrounding structures. The heart is now in its permanent location in the thorax and

the liver is in the abdominal cavity. The septum transversum with its extension, the pleuro-peritoneal membrane, stretches across the body from the tips of the embryonic ribs. But in the thorax lie the lungs, and their further growth into the lateral walls of the embryo and septum transversum will make them encircle the heari:, thereby enlarging the pleuropericardial membranes and changing j)osition of the phrenic nerves.

After the heart, lungs, liver and stomach are located in their permanent positions the plenro-peritoneal membrane grows rapidly and soon closes the opening between the pleural and peritoneal cavities. Fig. 42 is from a section lateral to the opening showing the phrenic nerve throughout its greatest extent. In this specimen the marked growth is in the pleural cavity. Fig. 43 is from a section through the opening on a larger scale, including also the adrenal. A stage slightly more advanced is shown in Fig. 44. In this specimen, as in the one above, both pleural cavities communicate with the peritoneal. In Embryo LXXIV, Fig. 4."i, the iileum

FiG. 4.5. — Transverse section through the embryo 14 mm. long. No. LXXIV X 10 times; 7, seventh rib. The plenro-peritoneal membrane ; pp, is incomplete on one side.

peritoneal nienibrane is complete on the right side and incomplete on the left side. The reconstruction of this embryo shows that the opening is very large and extends from the seventh rib towards the tail. It may be an instance of retarded development, because in embryos 19 mm. long the membranes are as a rule complete on both sides of the body. To what extent the permanent diaphragm is formed from the pleuro-peritoneal membrane it is difficult to determine. Undoubtedly the portion of the diaphragm on the caudal and dorsal sides of the pleuro-pericardial membrane is formed from the pleuro-peritoneal membrane. That portion of (lie diaphragm on the cephalic side is formed from the septum transversum. Itut the diaphragm is greatly extended on the lateral sides of the heart after the embr}'o is 20 mm. long by the extension of the pleural cavities around it. It appears from the models that this portion of the diaphragm is also formed directly from the periphery of the septum transversum.



[Nos. 121-122-123.

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