Paper - Description of a Human Embryo of Twenty-two paired Somites

A Gurgis

<pubmed>17104111</pubmed>| PMC1249865

Historic Embryology

This is a slightly edited version of the original 1926 paper published in Journal of Anatomy. The full paper is still available as a PDF document through PubMed Central.

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Carnegie Staging Comparison: A 22 somite stage embryo would be similar to a Carnegie stage 12 (26 - 30 days), caudal neuropore closes, Somite Number 21-29.

Clinical History and Age

A human chorionic vesicle was kindly presented to me in November, 1923, by DrMahfouz Bey, Professor of Midwifery at Kasr-el-Eini Hospital,Cairo. He gave me the following short history without dates: "Copulation took place 2weeks after menstruation. Abortion occurred 5 days after the succeeding menstruation was due; haemorrhage two days before the abortion. The period between copulation and abortion is 18 days." Whether that was the only copulation between the two menstrual periods or the last before the abortion is not stated. Ifitwastheonlycopulation,thefertilisationageoftheembryo will be 17 days, or 15 days ifthe embryo ceased to grow after the haemorrhage whichoccurred2daysbeforetheabortion. Ifcopulationhadtakenplace preceding the one mentioned inthe history, we falback on the menstruation age for estimating the age of the embryo. This would be 37 days, taking the 2 weeks starting from the end of menstruation and adding 5 days, being the average period of flow.

The greatest length of the embryo measures 2-9mm. and according to Mall'sagecurve,anembryoof3mm. longhas41daysmenstruationageand 30 days copulation age, which is the probable age of this embryo when com- paredwithotherembryosofmoredefiniteage. AccordingtoHis'scurve,an embryoof3mm. longhascopulationageof17days,whichagreeswiththeage giveninthehistory.

Peter Thompson, in describing an embryo of 23 somites and 2-5 mm. long, says that "it resembles in many ways His's embryo L.G. which was 2-15 mm. in length and estimated to be about 15 days old."

Davis described an embryo of 20 somites in which three copulations have taken place during two menstruations, and from his data he works out three copulation ages, the first 17 days, the second 24 to 27 days and the third 31 to37days,andhebelievesthatthelastistherightageofhisembryo. Hesays:

Thefirstcopulationage(17days)istooyoungtomeritseriousconsideration, for by subtracting one day, as suggested by Triepel (1914) and Bryce and Teacher (1908), the fertilisation age would be 16 days, just one day older than the Bryce-Teacher specimen. Moreover, this coition occurred during the period in which, according to Siegel (1915) and Issmer (1889), intercourse is least likely to be fruitful. The probable fruitful coition, therefore, is reduced to the second or to the third preceding one. From the second we obtain a copulationageof24to27days,andfromthethird31to37days. According totheagecurveofMall(1918)a3mm. embryoshouldhaveamenstruation age of 40 to 41 days. By comparing the data at hand with this age curve, it is clear that the menstruation age of 42 days is probably the correct one. The copulationageaccordingtoMall'schartwouldbe30days. Thisfalsbetween the possible copulation ages of 27 and 31 days, as shown in Table I, and may, therefore, be regarded as very close to the actual age of the embryo.

Johnson describes an embryo of 24 somites and he says the age of the specimen is uncertain from the data obtained, but it corresponds very closely to an embryo of 28 days as estimated by Mall.

Van den Broek describes an embryo of 22 somites but mentions no age.

The above-mentioned four embryos, Thompson's, Davis', Johnson's and Van den Broek's, resemble verycloselythis embryo, as willbe shown later,and according to Mall's age curve they range in age between 28 and 30 days, which is more probable than the age of 15 to 18 days given to them by His's age data.

Technique

The vesicle, which had been kept in spirit for some time before I received it, is oval in shape with a broad and a narrow pole.. It measures 18mm. inlengthand13mm. indiameter. Itisevenlycoveredwithvili excepting a small area on one side which is scantily covered. The embryo was attached to the inner surface on the side opposite this area. The vesicle was opened at the slightly villous area and the embryo with the attached part of the vesicle was cut out and transferred to formalin, then graded up through the alcohols, cleared in cedar-wood oil and embedded in paraffin.

The embryo measures 2-9 mm. in greatest length. It was cut transversely into 329 sections of 1Ou each. The sections were stained with haematoxylin and eosin.

The following observations were made in the Institute of Anatomy, Uni- versity College, London, under the guidance of Professor J. P. Hill, to whom my gratitudeisdueforhisadviceandcriticism,andkindnessinallowingme to work in his Department.

Threemodelsweremade bythewax platemethod,oneofthewholeembryo magnified 200 diameters with the left lateral wall removed, another of the brain and a third of the pharynx.

External Form

Fig. 1, of the left lateral view of the embryo, shows that the head is large and slightly flattened cephalo-caudally and inclined to be pointed, in which it resembles that of Thompson's embryo.

Caudal to the head there is the large swelling of the heart separated from the head by the cleft-like mouth. The dorsum of the embryo gives the outline of a well-marked curve which can be divided into three portions. The first, the dorsal flexure, is the largest and extends from the head to a level caudal to the yolk stalk, with its convexity directed dorsally; the second (ventral flexure) extends from the caudal limit of the first to a level caudal to the body stalk; it is the smallest and its convexity is directed ventrally. This will place the ventral flexure at a level caudal to that of the yolk stalk, agreeing in this respect with Davis' and Johnson's embryos, and disagreeing with the descrip- tionofHis,who placestheventralflexureattheleveloftheyolkstalk.The third curve extends from the caudal limit of the second to the tip of the tail; it is intermediate between the other two in size and its convexity is directed dorsally.

The yolk sac isvery large, nearly the same size as the embryo and isdirected cranially and to the right side of the embryo, which appears to lie on it. The bodystalkisthickandbendscaudalwards.Theamnioncanbeseenenveloping the embryo and there is a space between them, especially at the head end. This spaceisabsentinVan denBroek'sembryo,wheretheamnionisappliedclosely to the embryo.

Inthemodeltheabovefeaturescanbeseen. intheregionoftheheadthe optic vesicles are seen as two swellings, one on either side of the cephalic end of the head. Viewed laterally there are to be seen the three ectodermal grooves of bronchial pouches, 1, 2 and 3. They are graduated in size, the 1st having the greatest vertical extent. These grooves mark out three visceral arches which are also graduated in size, the most cephalic or mandibular arch being the largest. The 4th visceral pouch, which is present in this embryo, has no correspondinggrooveonthesurface,aconditionalsofoundinThompson's embryo.

In apparent continuity with the dorsal ends of the Ist and 2nd arches there are two small swellings, one to each arch. These swellings correspond to the ganglia of the trigeminus and acoustico-facialis, the former related to the 1st andthelattertothe2ndarch. Caudaltotheswellingoftheacoustico-facial ganglion and close to it, there is the small opening of the otic vesicle which is in line with the second ectodermal groove. The branchial region appears normal and resembles the corresponding region in Johnson's embryo (24 somites), Thompson's embryo (23 somites), Van den Broek's embryo (22 somites), and Davis' embryo (20 somites).

A shortdistancebehindthelastectodermalgroove,the1stsomiteappears as a bulging from the lateral wall of the embryo near the dorsal middle line. This is followed by regular swellings of the subsequent somites. The first three are large but not distinctly marked out on the surface. The rest become reduced in size towards the tail.

The yolk sac was accidentally detached from the embryo during the process of dehydrating. The yolk stalk is a very wide canal connected with the mid-gut.

Atthetailend,theposteriorneuroporeiswidelyopen. Ontheventral surface of the embryo, at the tail end, there is a depression representing the anal pit and at the bottom of it the ano-cloacal membrane.

Thebodystalkcomesoutfromthecaudalthirdoftheembryo. Itisof large size and is bent caudally and to the right side of the embryo.

The embryo is twisted longitudinally with the head turned towards the right and the tail towards the left. The plane of the twist is in the middle of themid-gut.

Integument

Theintegumentisgenerallyofonelayerofcubicalectodermalcels. Itis thinonthedorsalsurfaceovertheneuraltubewherethecellsareflattenedin shape. There is no indication of the lens primordium opposite the optic vesicles and athinlayerofmesenchyme stilintervenesbetween theopticvesiclesand the ectoderm overlying them. The ectoderm, which has folded in to form the walloftheoticvesicle,isformedofathicklayerofnarrowcolumnarcels,and joins the surface ectoderm round the opening of the otic vesicle.

In the region of the bronchial arches, the ectoderm is thickened and the celsarecolumnarinshape.

Intheregionoftheoralcavity,theectodermisslightlythickened,forming the superficial layer of the bucco-pharyngeal membrane, which is perforated intwoplaces. Intheroofoftheoralcavity,the ectodermis in close apposition with the primitive infundibular recess of the fore-brain.

The ectoderm over the pericardial cavity is composed of one layer of flattened epithelium.

The Nervous System

The nervous system consists of the brain with its three main divisions, the gangliaoftheVth,VIIth,VIIIth,IXth,andXthcranialnerves,thespinalcord and the ganglionic crest. The whole system lies underneath the ectoderm in thedorsumoftheembryoandfollowsitscurvature. Apartfromalongitudinal slit which runs through the whole length of the neural tube, obviously an artifactduetoshrinkage,thetubeisclosedexceptatitscaudalend,wherethe posteriorneuroporeisstilpatent. Inthisfeatureitagreeswiththeembryos of Davis (20 somites), Van den Broek (22 somites), Thompson (23 somites) andJohnson(24somites),butitdisagreeswiththeJanosikembryo(24somites), which shows a patent anterior and closed posterior neuropore, and Bremer's embryoof4mm. longwhoseneuraltubeisstilopeninfrontandbehind. From thisitappearsthattheorderofclosureoftheneuroporesvaries,butin the majority of embryos the anterior neuropore closes first; and the stage at whichclosuretakesplaceisat20to24somitesfortheanterior,and30somites fortheposteriorneuropore. Whetherthedelayofclosureoftheanterior neuroporeorthereversaloforderofclosureisduetosomeabnormalcondition of the embryos in which this occurs, or a variation of a normal condition, cannotbedefinitelystated. Davisbelievesthatclosureoftheanteriorneuro- pore first is the normal condition, and he looks upon the failure of its closure as a delay of the normal process or possibly the result of a complete arrest of development.

The Brain

Theprimarydivisionsofthebrain(fig.2)arewellmarked. The fore-brain is a simple vesicle separated from the mid-brain by a slight grooveon theoutersurface. A smallareaatitscephalo-dorsalborderisfused with the overlying ectoderm, marking the last point of closure of the anterior neuropore.

The optic vesicles are large somewhat dorso-ventrally flattened outgrowths which project, one from either side of the anterior part of the fore-brain. They occupy practically the entire lateral walls of the anterior region of the fore- brain, and have not yet begun to be constricted off from the latter. Their cephalic borders pass over directly into the front wall of the fore-brain, whilst caudally each vesicle is marked off from the lateral wall of the same by a crescenticgroove. Eachvesiclecommunicateswiththefore-brainventricle by a large opening in front of a crescentic posterior margin.

Theectoderm,whichoverlieseachvesicle,isnotthickened,andisseparated from the vesicles by a thin sheet of mesenchyme.

The subdivision of the fore-brain into telencephalon and diencephalon is indicated by a slight groove on the dorsal wall of the brain, practically on a level with the hinder borders of the optic vesicles. Corresponding to this groove there is present on the inner surface a slight ridge which runs down on the lateral wall, behind the opening of the optic vesicles. This ridge probably represents the velum transversum.

Below and behind the openings of the optic vesicles, and on the ventral surface of the fore-brain is a well-marked depression, forming the primitive infundibular recess, the projecting floor of which produces a bulging on the roof of the buccal cavity.

The wedge-shaped mid-brain is the shortest of the three divisions and is marked off by two constrictions from the fore and hind-brains, the anterior constriction best marked dorsally, the posterior constriction coinciding with theregionofgreatestflexure. Itshowsnoevidenceofsubdivision,asdescribed byWatt,inayoungerembryo,andGage,inanembryoof29somites. Inthis respect itresembles the mid-brain ofJohnson's embryo of24 somites, Thomp- son's embryo of 23 somites, Van den Broek's embryo of 22 somites and Davis' embryo of 20 somites.

The hind-brain is the largest of the three divisions; it is indeed about one- thirdofthetotallengthofthewholeneuraltube. Itisconnectedwiththe mid-brain by the isthmus and fades gradually into the spinal cord. There is a marked thinning of its roof, but no depression as in Van den Broek's embryo. On its lateral walls six pairs of neuromeres can be seen. They appear in the modelofthebrainaswedge-shapedbulgings,soarrangedthatthebasesofthe 1st, 3rd and 5th, are directed dorsally, and those of the 2nd, 4th and 6th are directed ventrally. The 1st pair has no definite limit in front from the rhombo- mesencephalic groove. The 2nd and 4th pairs of neuromeres correspond with definite down bulgings of the floor of the hind-brain, that related to the 4th pair being more prominent than that of the 2nd pair.

The number of neuromeres recorded in embryos of about the same stage asthisisasfollows:

Thompson's embryo of 23 somites has 7 neuromeres. Davis' , 20 , 9 VandenBroek's, 22 , 5

Johnson states that the number of neuromeres in his embryo cannot be ascertained.

Lying in relation with the neuromeres are the following structures: The ganglion of the trigeminus in close relation with the 2nd neuromere, the gang- lion of the acoustico-facialis with the 4th neuromere (the acoustico-facialis is the largest ganglion present and can be traced to the 2nd bronchial arch), and theganglionoftheglosso-pharyngeusliesinrelationwiththe6thneuromere. This arrangement agrees with that described by Gage, Johnson, Peter Thomp- son and Davis, and with Bartelmez, who shows in a table the relation of preotic,oticandpostoticprimarysegmentsofthehind-braintothesecondary and definitive neuromeres.

The most marked of the neuromeres of this embryo is the 4th or facial which corresponds with the otic neuromere of Bartelmez, and the least distinct is the 6th, which is at a level cranial to the 1st somite.

The ganglionofthevagus isseeninthesectionsasasmallclusterofcels caudal to the ganglion of the glosso-pharyngeus.

The otic vesicle lies in relation with the 5th neuromere and close to the ganglionoftheacoustico-facialis. Itisalargepear-shapedvesicle,withits long axis in the dorso-ventral direction, its broad end being directed dorsally.

Itswallisthickandthevesicleisstilopenltotheexterior;itsopeningissituated at its dorsal broader end rather on the lateral aspect than on the summit, and the edges of the opening are continuous with the surrounding ectoderm.

Thebrainissharplyflexedatthejunctionofthemid-brainandtheisthmus, the mid-brain forming the most cephalic part of the embryo. The longitudinal axes of the fore and mid-brains form approximately a straight line which makes an angle of rather more than 90' with the longitudinal axis of the cephalic half of the hind-brain. This flexure corresponds to the primary cephalic flexure in other embryos and involves the anterior end of the notochord. There is a slightflexureofthehind-brainimmediatelybehindthedown-bulgingrelated to the 4th pair of neuromeres, and on a level with the otic vesicles.

These two flexures resemble those described by Peter Thompson and Van den Broek in embryos of about the same stage of development as this. Thomp- son says: "They are so different from those universally regarded as primary cerebral flexures, that one hesitates to go further than simply place them on record." He ends by saying: "Is it not possible that there may be certain flexures of a temporary character, which precede the primary flexures usually described?" VandenBroekexpressesasimilarview. Since the publication of Thompson's and Van den Broek's papers, Low, who described Pfannenstiel III embryo of 13-14 somites, finds a similar con- dition which agrees very closely with that of Thompson's description. Willin also finds a similar flexure in a brain of an embryo of 13 somites, and states: "The brain flexures do not agree with the His models of this stage but cor- respond more to the older embryos described by Thompson and Van den Broek."

Hochstetteralsofindsasimilarconditioninanembryoof3*34mm., somewhatolderthanThompson's. Hestates:"Thereisaflexureontheventral aspect of the hind-brain resembling that described by Thompson though not so marked. This disagrees with the condition described by His." He regards His's embryos, L.G., B.B., E.B., as abnormal or else not well preserved.

These flexures are probably due to exaggeration of the usual primary flexures. The flexure between the mid-brain and isthmus corresponds very closely with the primary cephalic flexure, and involves the hinder part of the mid-brain.Theslightflexureinthehind-brainisprobablyduetotheexagger- ated dorsal flexure of the body of the embryo (as seen in Plate I) extending towards the hind-brain and involving its hinder part.

Spinal Cord

Thespinalcordextendsfromthecaudalendofthehind-brain to the tail. The cephalic part of the tube is of the same character as the caudal portionofthehind-brain,whereitiscompressedlaterallyandthelongaxisof itslumenisdorso-ventralindirection. Itbecomesmorecylindricalcaudalto thedorsalflexure. Itissegmentedthroughmostofitslength,thesegments being separated from each other by circular constrictions which involve its entire circumference, so resembling the segmentation described by Watt and Johnson, and differing from that of Davis' embryo where they only appear on the lateral surface. These segments are very distinct in the region of the dorsal flexure. Eightdistinctsegmentscanbeseeninthemodelinthatregion. Each neural segment lies between two consecutive somites and opposite each segmentthedorsalaortagivesoffadorsalsegmentalartery.Thelateralwallsof the tube are thicker than its roof and floor; the roof is thinner than the floor and lies in contact with the dorsal ectoderm.

In cross-section (fig. 4), the lateral walls at the level of the dorsal flexure aredifferentiatedintobasalandalarlaminaeandthelumenoftheneuralcanal is lozenge-shaped. This differentiation gets less and less marked towards the tail end where the lumen is circular in shape.

Ganglionic crest

The ganglionic crest as a definite wedge-shaped structure

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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding. (More? Embryology History \| Historic Embryology Papers)

The information below was not part of the above original historic article.

Carnegie Stages: 1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | 9 | 10 | 11 | 12 | 13 | 14 | 15 | 16 | 17 | 18 | 19 | 20 | 21 | 22 | 23 | About Stages | Timeline

Carnegie Stage Table

Weeks shown in the table below are embryonic post ovulation age, for clinical Gestational Age (GA) measured from last menstrual period, add 2 weeks.

Stage	Days (approx)	Size (mm)	Images (not to scale)	Events
1	1 (week 1)	0.1 - 0.15		fertilized oocyte, zygote, pronuclei
2	2 - 3	0.1 - 0.2		morula cell division with reduction in cytoplasmic volume, blastocyst formation of inner and outer cell mass
3	4 - 5	0.1 - 0.2		loss of zona pellucida, free blastocyst
4	5 - 6	0.1 - 0.2		attaching blastocyst
5	7 - 12 (week 2)	0.1 - 0.2		implantation
6	13 - 15	0.2		extraembryonic mesoderm, primitive streak, gastrulation
7	15 - 17 (week 3)	0.4		gastrulation, notochordal process
8	17 - 19	1.0 - 1.5		primitive pit, notochordal canal
9	19 - 21	1.5 - 2.5		Somitogenesis Somite Number 1 - 3 neural folds, cardiac primordium, head fold
10	22 - 23 (week 4)	2 - 3.5		Somite Number 4 - 12 neural fold fuses
11	23 - 26	2.5 - 4.5		Somite Number 13 - 20 rostral neuropore closes
12	26 - 30	3 - 5		Somite Number 21 - 29 caudal neuropore closes
13	28 - 32 (week 5)	4 - 6		Somite Number 30 leg buds, lens placode, pharyngeal arches
Stage 13/14 shown in serial embryo sections series of Embryology Program
14	31 - 35	5 - 7		lens pit, optic cup
15	35 - 38	7 - 9		lens vesicle, nasal pit, hand plate
16	37 - 42 (week 6)	8 - 11		nasal pits moved ventrally, auricular hillocks, foot plate
17	42 - 44	11 - 14		finger rays
18	44 - 48 (week 7)	13 - 17		ossification commences
19	48 - 51	16 - 18		straightening of trunk
20	51 - 53 (week 8)	18 - 22		upper limbs longer and bent at elbow
21	53 - 54	22 - 24		hands and feet turned inward
Stage 22 shown in serial embryo sections series of Embryology Program
22	54 - 56	23 - 28		eyelids, external ears
23	56 - 60	27 - 31		rounded head, body and limbs
Following this stage Fetal Development occurs until birth (approx 37 weeks)