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=A Contribution to the Embryology of the Fore-Limb Skeleton=


Journal Of Anatomy And Physiology 
By N. C. Rutherford, M.B., F.R.C.S.


==Introductory==


{{Ref-Rutherford1914}}
THE concise account of the development of the human skeleton recently published in the Keibel and Mall Tecct-boo/c of Human Embryology forms the standpoint of present knowledge of and opinion on the subject. Regarded from this standpoint, certain observations of some importance resulting from a study of the development of the shoulder girdle and forelimb skeleton in man, recently undertaken by the writer, seem worthy of publication as supplementing the account of the cardinal features in the growth of these cartilages and giving an account of the early phenomena of the ossification of the scapula. In considering the observations made on the development of the skeletal arch which overhangs and strengthens the shoulder-joint, its origin from one of a smaller perimeter will be the chief subject of discussion. The embryonic material employed consists of human embryos and foetuses of from 10 to 30 mm. in greatest length, reconstructions of the fore-quarter skeletons being made in two cases, one a 20-millimetre and the other a 30-millimetre specimen. The specimens cited in comparison are in the Museum of the Royal College of Surgeons. As it is on the reconstructions that the initial Observations were made and round them that the whole work centres, a short description of them forms the first part of this paper.


Rutherford NC. [[Paper - A contribution to the embryology of the fore-limb|A contribution to the embryology of the fore-limb]] (1914) J Anat Physiol. 48: 355-377.


Technical Note. — In making the drawings of the cartilaginous skeleton, care was taken to indicate exactly the margins of the fully differentiated cartilage as contrasted with the transitional perichondrial layers in all cases except that of the clavicle in which the easily followed enveloping layer was shown. VOL. XLVIII. (THIRD SER. VOL. IX.)—JULY 1914. 25 356 4 A Mr N. C. Rutherford


A Contribution To The Embryology Of The Fore-Limb
==Descriptive==
Skeleton. By N. C. Rutherford, M.B., F.R.C.S.


INTRODUCTORY.
Model of the Fore-quarter Skeleton of a, 20 mm. Human Embryo (figs. 1 and 2).


THE concise account of the development of the human skeleton recently
This model includes :— Twelve vertebrae of which the upper two are cervical, nine complete and two incomplete ribs, one lateral half of the sternum, all the elements of the limb and girdle skeleton.
published in the Keibel and Mall Tecct-boo/c of Human Embryology forms
the standpoint of present knowledge of and opinion on the subject.
Regarded from this standpoint, certain observations of some importance
resulting from a study of the development of the shoulder girdle and forelimb skeleton in man, recently undertaken by the writer, seem worthy of
publication as supplementing the account of the cardinal features in
the growth of these cartilages and giving an account of the early
phenomena of the ossification of the scapula. In considering the observations made on the development of the skeletal arch which overhangs and
strengthens the shoulder-joint, its origin from one of a smaller perimeter


will be the chief subject of discussion.
, The vertebrae are represented by their bodies, and continuous with these are the neural arches of the right side; cartilaginous continuity around the notochord exists between the bodies. They form a markedly arched series, the dorsal convexity being so great as to bring the two upper ones each rather ventral to the succeeding member of the series than on top of it; these two cervical vertebrae have procoelous bodies of approximately tetrahedral form, apex directed caudo-ventrally. The neural arches, imbricated above and in linear series below, show small lateral projections at their dorsal extremities representing demispines; the seventh cervical vertebra shows a separate chondral element, its costal process, which is in close articulation with the body.
The embryonic material employed consists of human embryos and


foetuses of from 10 to 30 mm. in greatest length, reconstructions of the
fore-quarter skeletons being made in two cases, one a 20-millimetre
and the other a 30-millimetre specimen. The specimens cited in comparison are in the Museum of the Royal College of Surgeons. As it is
on the reconstructions that the initial Observations were made and round
them that the whole work centres, a short description of them forms the


first part of this paper.
Fig. 1. Wax-plate reconstruction from human embryo 20 mm. greatest length. Magnification in figure about x 8'5.


Technical N 0te.—In making the drawings of the cartilaginous skeleton,
care was taken to indicate exactly the margins of the fully differentiated cartilage as contrasted with the transitional perichondrial
layers in all cases except that of the clavicle in which the easily


followed enveloping layer was shown.
The disproportionate length of the ribs and the approximately horizontal ‘position each occupies give to . the whole thoracic skeleton an  appearance of marked inspiration. In general the cross-section of each rib is circular, but in front there is dorso-ventral flattening, whilst behind the flattening is from above downwards; the anterior extremities of ribs I. to V. articulate with a delicate sternal bar of cartilage which merges above partly in the cellular nonchondral interclavicular mass; VI. and VII. meet and support each other caudal to the other extremity of this bar ; all turn slightly dorsally, and I. to V. then acutely caudally in contact with the sternal bar. Like VI. and VII., VIII. IX. X. and XI. bend forward and so aredisposed as in the adult.
VOL. XLVIII. (THIRD SER. VOL. IX.)—JULY 1914. 25
356 4 A Mr N. C. Rutherford


DESCRIPTIVE.


Model of the Fore-quarter Skeleton of a, 20 mm. Human Embryo
The clavicle is represented in its inner four-‘fifths by a very stout bar prolonged as to its outerfifth in the form of a flattened plate by bevelling at the expense of its costal aspect. The curve of the lateral part of the adult bone is practically absent. The cellular, constitution can be well seen in fig. 6; it is made up of two ossific centres on the point of coalescence within a matrix of young cartilage cells, the whole being surrounded by a very dense cellular periosteum; this last is prolonged into (1) a cellular mass surrounding the tip of the acromion, (2) a similar mass at the opposite end, the inter-clavicle, and (3) a" tract or band connecting behind the coracoid with the pre-scapula in which there is an appearance of early chondrification. The wedge of cartilage described by Professor Fawcett and assumed by him to be associated with the formation of the deltoid tubercle is well shown in fig. 6. In this figure the deltoid is not associated with it.
(figs. 1 and 2).


This model includes :—Twelve vertebrae of which the upper two are
cervical, nine complete and two incomplete ribs, one lateral half of the
sternum, all the elements of the limb and girdle skeleton.


, The vertebrae are represented by their bodies, and continuous with these
are the neural arches of the right side; cartilaginous continuity around the


F10. 1.—Wax-plate reconstruction from human embryo 20 mm.
fiG. 2. Wax-plate reconstruction from human embryo 20 mm. Schematic representation of scapula and limb skeleton. Magnification in figure x 7'14.
greatest length. Magnification in figure about x 8'5.


notochord exists between the bodies. They form a markedly arched series,
the dorsal convexity being so great as to bring the two upper ones each
rather ventral to the succeeding member of the series than on top of it;
these two cervical vertebrae have procoelous bodies of approximately tetrahedral form, apex directed caudo-ventrally. The neural arches, imbricated
above and in linear series below, show small lateral projections at their dorsal
extremities representing demispines; the seventh cervical vertebra shows
a separate chondral element, its costal process, which is in close articulation
with the body.


The disproportionate length of the ribs and the approximately
The scapula is as yet incompletely merged with the coracoid, as indicated by the Width of the scapular notch and by a line of division “across the glenoid cavity rather below its middle. The blade is irregularly diamond-shaped; its upper limit lies opposite the caudal extremity of the body of the sixth cervical vertebra, and its surfaces are parasagittal.
horizontal ‘position each occupies give to . the whole thoracic skeleton an
A Contribution to the Embryology of the Fore-Limb Skeleton 357


appearance of marked inspiration. In general the cross-section of each
rib is circular, but in front there is dorso-ventral flattening, whilst behind
the flattening is from above downwards; the anterior extremities of ribs I.
to V. articulate with a delicate sternal bar of cartilage which merges above
partly in the cellular nonchondral interclavicular mass; VI. and VII. meet
and support each other caudal to the other extremity of this bar ; all turn
slightly dorsally, and I. to V. then acutely caudally in contact with the
sternal bar. Like VI. and VII., VIII. IX. X. and XI. bend forward and
so aredisposed as in the adult. .


The clavicle is represented in its inner four-‘fifths by a very stout bar
The coracoid is a bulbous mass of cartilage joined with the scapula by a narrow neck and having a short cornuate process projecting upwards above the greater tuberosity of the humerus and a long one directed caudoventrally in the neighbourhood of the lesser tuberosity, considerably below the clavicle.
prolonged as to its outerfifth in the form of a flattened plate by bevelling
at the expense of its costal aspect. The curve of the lateral part of the
adult bone is practically absent. The cellular, constitution can be well




fiG. 2.—Wax-plate reconstruction from human embryo 20 mm. Schematic representation of scapula and limb skeleton. Magnification in figure x 7'14.
The acromion is a delicate bar showing an approximately right angle bend just above its root and a gentle curve beyond that to its tip, which projects slightly beyond the lateral extremity of the clavicle. Its root is immediately behind the edge of the scapular part of the glenoid cavity.


seen in fig. 6; it is made up of two ossific centres on the point of coalescence within a matrix of young cartilage cells, the whole being surrounded
fiG. 3. Wax-plate reconstruction from human embryo about 30 mm. greatest length. Magnification about x 8'5. Ossific plate shaded.
by a very dense cellular periosteum; this last is prolonged into (1) a
cellular mass surrounding the tip of the acromion, (2) a similar mass at
the opposite end, the inter-clavicle, and (3) a" tract or band connecting
behind the coracoid with the pre-scapula in which there is an appearance
of early chondrification. The wedge of cartilage described by Professor
Fawcett and assumed by him to be associated with the formation of the
deltoid tubercle is well shown in fig. 6. In this figure the deltoid is not
associated with it.


The scapula is as yet incompletely merged with the coracoid, as
indicated by the Width of the scapular notch and by a line of division “across
the glenoid cavity rather below its middle. The blade is irregularly
diamond-shaped; its upper limit lies opposite the caudal extremity of the
body of the sixth cervical vertebra, and its surfaces are parasagittal.


The coracoid is a bulbous mass of cartilage joined with the scapula by
There is complete absence of the spine, but, on the other hand, there is present a distinct supraspinous element (which for reasons which will appear I will call the “ prescapula”), separated by a slight interval. near the middle of its length from the main part of the blade or “ postscapula ” and by a junctional zone dorsally to this. This prescapula is inclined at a slight angle to and occupies a more medial plane than the postscapula, as in fig. 5; a prominent ridge which lies on the superficial surface of the post-scapula, caudal to the interval between the two elements of the blade, indicates the future basis of support for the spine. By reason of this arrangement there exist two notches in this region, one which for my present purpose may be called coraco-prescapular, and becomes the future incisura scapularis, and the other which I will call acromio-postscapular, a temporary feature later filled up by the growth of the spine. Between these two notches is the narrow area of origin of the supraspinatus muscle which occludes on one aspect the interval between the two parts of the blade.
358 T ‘ Mr N. C. Rutherford


a narrow neck and having a short cornuate process projecting upwards
above the greater tuberosity of the humerus and a long one directed caudoventrally in the neighbourhood of the lesser tuberosity, considerably below
the clavicle.


* The acromion is a delicate bar showing an approximately right angle
The roots of the acromion and coracoid, and most markedly that of the prescapula, are invested by a thick layer of cells which surrounds the origin of supraspinatus and forms the scapular extremity of the previously mentioned band or cellular condensation which reaches behind the main mass of the coracoid to be continuous" with the periosteum of the outer segment of the clavicle (fig. 6).
bend just above its root and a gentle curve beyond that to its tip, which
projects slightly beyond the lateral extremity of the clavicle. Its root is
immediately behind the edge of the scapular part of the glenoid cavity.


fiG. 3.—Wax-plate reconstruction from human embryo about 30 mm. greatest
length. Magnification about x 8'5. Ossific plate shaded.


There is complete absence of the spine, but, on the other hand, there is
fiG. 4. Wax-plate reconstruction from human embryo about 30 mm. Schematic representation of scapula and limb skeleton. Magnification about x 6.
present a distinct supraspinous element (which for reasons which will
appear I will call the “ prescapula”), separated by a slight interval. near
the middle of its length from the main part of the blade or “ postscapula ”
and by a junctional zone dorsally to this. This prescapula is inclined at
a slight angle to and occupies a more medial plane than the postscapula, as
in fig. 5; a prominent ridge which lies on the superficial surface of the
post-scapula, caudal to the interval between the two elements of the blade,
indicates the future basis of support for the spine. By reason of this
arrangement there exist two notches in this region, one which for my
present purpose may be called coraco-prescapular, and becomes the future
A Contribution to the Embryology of the Fore-Limb Skeleton 359


incisura scapularis, and the other which I will call acromio-postscapular, a
temporary feature later filled up by the growth of the spine. Between
these two notches is the narrow area of origin of the supraspinatus muscle
which occludes on one aspect the interval between the two parts of the
blade.


The roots of the acromion and coracoid, and most markedly that of the
The humerus has a very remarkable shape. The shaft is bent outwards and forwards so as to form a salient angle opposite the deltoid insertion; its proximal half is arched outwards and its distal half backwards. Neither extremity in its relation to the axis of the shaft occupies a position corresponding to that of the adult bone; the proximal end is rotated somewhat outwards, and its articular surface is divided by a groove into two flattened condyles corresponding with the coracoid and scapular segments to which it is applied; the distal end occupies a plane such as might result from a great exaggeration of that angle between the axis of the trochlea and the long axis of the shaft which is characteristic of the adult. By reason of this the inner lip of the trochlea forms the distal extremity of the humerus, and the capitulum lies on the lateral aspect at a higher level. A delicate outgrowth from the perichondrium of the shaft near its lower end ventro-lateral to the median nerve indicates the position of the entepicondylic spine (fig. 7).
prescapula, are invested by a thick layer of cells which surrounds the
origin of supraspinatus and forms the scapular extremity of the previously


fiG. 4.—Wax-plate reconstruction from human embryo about 30 mm.
Schematic representation of scapula and limb skeleton. Magnification about x 6.


mentioned band or cellular condensation which reaches behind the main
What has been said of the distal articular surfaces of the humerus conveys equally the relative position of the contiguous extremities of the radius and ulna. These two cartilages lie parallel, one above the other, but not quite in the same plane, owing to what may be ‘described as a very slight degree of pronation. There is present between their distal ends an independent cartilaginous nodule embedded in a thickly crowded mass of cells. This may represent the intermedium.
mass of the coracoid to be continuous" with the periosteum of the outer
segment of the clavicle (fig. 6). '


The humerus has a very remarkable shape. The shaft is bent outwards
and forwards so as to form a salient angle opposite the deltoid insertion;
its proximal half is arched outwards and its distal half backwards. Neither
extremity in its relation to the axis of the shaft occupies a position
corresponding to that of the adult bone; the proximal end is rotated
somewhat outwards, and its articular surface is divided by a groove into
two flattened condyles corresponding with the coracoid and scapular
segments to which it is applied; the distal end occupies a plane such as
360 . Mr N. C. Rutherford


might result from a great exaggeration of that angle between the axis of
the trochlea and the long axis of the shaft which is characteristic of the
adult. By reason of this the inner lip of the trochlea forms the distal
extremity of the humerus, and the capitulum lies on the lateral aspect at a
higher level. A delicate outgrowth from the perichondrium of the shaft
near its lower end ventro-lateral to the median nerve indicates the position
of the entepicondylic spine (fig. 7). T r


i What has been said of the distal articular surfaces of the humerus


‘\ ‘ . T,
fiG. 5. Coronal section, human mbryo about 30 mm. Prescapa and postscapula, ossifying pine of scapula and trapezio-deltoid intersection.
.4 ‘., \ _ .c ,
- . . ~ , , . ,‘ '74


4 V.
f ‘- \.o'V


fiG. 5. -001-onal section, human mbryo about 30 mm. . Prescapa and postscapula,
Of the carpal cartilages those on the postaxial side are far in advance of those on the pre-axial side of the wrist; the same is true of the metacarpals and phalanges, the three digits of the ulnar side being almost equal in length and slightly longer than the index. End plates to the terminal phalanges are just recognisable by their dark staining and plexiform character. A Contribution to the Embryology of the Fore-Limb Skeleton 361
ossifying pine of scapula and trapezio-deltoid intersection.


1 -_.~‘. - “,' I. .3‘
Model of Fore-quarter Skeleton of 30 mm. Human Fcetus (figs. 3 and 4;).
‘\ XV ' 'f . .§fl"‘
conveys equally the relative position of the contiguous extremities of the


radius and ulna. These two cartilages lie parallel, one above the other,
This reconstruction shows ten half-vertebrae, of which three are cervical, four complete, and three incomplete costal arches, the manubrium sterni, and representatives of three sternebrae and all the elements of the limbgirdle and free limb.
but not quite in the same plane, owing to what may be ‘described as a very
slight degree of pronation. There is present between their distal ends an
independent cartilaginous nodule embedded in a thickly crowded mass of


‘cells. This may represent the intermedium.
The position of the vertebrae has altered owing to the decrease of the spinal curve, and the demispines on the extremities of the neural arches are now more marked. The ribs are now much more slender, except dorsally, where they are very massive and show commencing angulation.


Of the carpal cartilages those on the postaxial side are far in advance
of those on the pre-axial side of the wrist; the same is true of the metacarpals and phalanges, the three digits of the ulnar side being almost equal
in length and slightly longer than the index. End plates to the terminal
phalanges are just recognisable by their dark staining and plexiform
character.
A Contribution to the Embryology of the Fore-Limb Skeleton 361


Model of Fore-quarter Skeleton of 30 mm. Human Fcetus
(figs. 3 and 4;).
This reconstruction shows ten half-vertebrae, of which three are cervical,
four complete, and three incomplete costal arches, the manubrium sterni,
and representatives of three sternebrae and all the elements of the limbgirdle and free limb.
The position of the vertebrae has altered owing to the decrease of the
   


fiG. 6. —Horizontal section through shoulder of 20-mm. embryo.
fiG. 6. —Horizontal section through shoulder of 20-mm. embryo.
Line 227: Line 90:
sc., scapula; Acr., acromion; H., humerus; Co., coracoid; CL, clavicle; M., supraspinatus; and P., prescapulo-clavicular band shown attached dorsally where scapula is covered by thick cellular layer.
sc., scapula; Acr., acromion; H., humerus; Co., coracoid; CL, clavicle; M., supraspinatus; and P., prescapulo-clavicular band shown attached dorsally where scapula is covered by thick cellular layer.


spinal curve, and the demispines on the extremities of the neural arches are
now more marked. The ribs are now much more slender, except dorsally,
where they are very massive and show commencing angulation. _
The marn/abrial cartilage is pierced by a small hole, and there is a median
cleft in the third sternebra.
The clavicle has developed rapidly, and_ has now almost the adult form
with two curvatures; the outer extremity is, however, not so flattened as
in the adult. ‘ ' l T
The scapula reaches headwards to the level of the caudal border of the
seventh cervical vertebra; its diamond shape is still preserved, but the
length of that border which runs from the coracoid to the upper angle has
increased disproportionately; it follows that T the “ prescapular ” bar is
362 Mr  C. Rutherford p _
greatly increased‘ in size, the slit separating it from the postscapula has
lengthened, and there is- quite a marked groove indicating the boundary
between the two elements and extending from the slit to the dorsal border,
which it notches. The growth of the prescapula’ has greatlyexceeded that
of the postscapula in the 20-30 mm. period, and it now bears a greater
proportion to the whole blade than does the resulting supraspinous part of
the blade in the adult.
F_IG. 7.-i—'Horisontal section, human embryo 20 mm., to show :
H., humerus ; 1%., radius in cartilaginous continuity; Med., median nerve with entepicondylic
process of perichondrium on its lateral "aspect (*).
The coracoicl is little changed, being only rather smaller relatively.
The glcnoid surface is now concave and undivided; it seems to have
increased relatively in its lower blade part. b
sThe' acromion has grown considerably and become flattened and
spatula-like, so that the acromial angle of the. adult. is now recognisable.
The tip of the process projects considerably ventral to the outer end of the
clavicle. The right-angle bend near the root described in the previous


stage is now a sharp projecting elbow or spur of cartilage connecting with
The manubrial cartilage is pierced by a small hole, and there is a median cleft in the third sternebra.


a tract of young, actively growing cells which passes backwards over the
The clavicle has developed rapidly, and has now almost the adult form with two curvatures; the outer extremity is, however, not so flattened as in the adult.  
dorsum scapulae, under cover of the small-celled fibrous intersection between
trapezius and deltoid, nearly to the vertebral border. This tract represents
A Contribution to the Embryology "of the Fore-Limb Skeleton 363


the developing spine, and in it, especially . near. the L acromial elbow,
ossification is well advanced (fig._.8). The ossifying region is shaded in the
figures of the model, and it can be seen to extend into a projection at the
scapular notch, over the edge of which it is continued on to the medial
surface of the blade. The cells in which the ossification takes place "are


fiG. 8.—Coronal section, human embryo 30 mm. Shows elbow
The scapula reaches headwards to the level of the caudal border of the seventh cervical vertebra; its diamond shape is still preserved, but the length of that border which runs from the coracoid to the upper angle has increased disproportionately; it follows that T the “ prescapular ” bar is  greatly increased‘ in size, the slit separating it from the postscapula has lengthened, and there is- quite a marked groove indicating the boundary between the two elements and extending from the slit to the dorsal border, which it notches. The growth of the prescapula’ has greatlyexceeded that of the postscapula in the 20-30 mm. period, and it now bears a greater proportion to the whole blade than does the resulting supraspinous part of the blade in the adult.


. of acromion and ossification of spine (*).
FIG. 7. Horisontal section, human embryo 20 mm., to show : H., humerus ; 1%., radius in cartilaginous continuity; Med., median nerve with entepicondylic process of perichondrium on its lateral "aspect (*).


derived from the mass which in the 20-mm. stage clothed the roots of the
postscapula, coracoid, and acromion. ’


The humerus is constricted in the region of spreading ossification, and
The coracoid is little changed, being only rather smaller relatively. The glcnoid surface is now concave and undivided; it seems to have increased relatively in its lower blade part. The acromion has grown considerably and become flattened and spatula-like, so that the acromial angle of the. adult. is now recognisable. The tip of the process projects considerably ventral to the outer end of the clavicle. The right-angle bend near the root described in the previous stage is now a sharp projecting elbow or spur of cartilage connecting with a tract of young, actively growing cells which passes backwards over the dorsum scapulae, under cover of the small-celled fibrous intersection between trapezius and deltoid, nearly to the vertebral border. This tract represents the developing spine, and in it, especially . near. the L acromial elbow, ossification is well advanced (fig._.8). The ossifying region is shaded in the figures of the model, and it can be seen to extend into a projection at the scapular notch, over the edge of which it is continued on to the medial surface of the blade. The cells in which the ossification takes place are derived from the mass which in the 20-mm. stage clothed the roots of the postscapula, coracoid, and acromion.
is gently curved convex backwards. The two curvatures seen in the
earlier stage are much less prominent in this later one owing to the great
increase in length of the humerus, but both are easily identifiable still.


. The upper end is now only slightly out-turned as compared with that


of the adult bone, and the lower end has assumed, in the inclination of
fiG. 8.—Coronal section, human embryo 30 mm. Shows elbow of acromion and ossification of spine (*).
its axis to that of the shaft, a position intermediate between that in
364 Mr N. C. Rutherford


the earlier model and that representing the average of the two sexes
in adult bones.


The radius and ulna likewise show constrictions in the ossifying zones.
The humerus is constricted in the region of spreading ossification, and is gently curved convex backwards. The two curvatures seen in the earlier stage are much less prominent in this later one owing to the great increase in length of the humerus, but both are easily identifiable still.
They are now very decidedly crossed. The ulnar styloid seems to be
prolonged into the chondrifying discus articularis, and the same is true of
the ulnar side of the lower extremity of the radius: between the two
prolongations is a dense, unchondrified cell-mass. The contrast_ between
this condition and that described for the 20-mm. stage is remarkable. '


fiG. 9.—Corona.1 section, human embryo 30 mm.
0., centrale continuous through faintly staining zone with N., navicular.


The caxr-pal elements, especially those of the distal row, are well forward
The upper end is now only slightly out-turned as compared with that of the adult bone, and the lower end has assumed, in the inclination of its axis to that of the shaft, a position intermediate between that in the earlier model and that representing the average of the two sexes in adult bones.
in development, and there is visible, both on the palmar and dprsal aspects
of the wrist, a distinct centrale; on that side it lies between navicular,
lunar, and trapezoid, and on this between navicular, capitatum, and
trapezoid; its surface isolation does not correspond with the conditions
in the depth of the articulation, where it is continuous, through a faintly
staining transitional zone, with the navicular (fig. 9). The navicular is
in only narrow contact with the trapezium, which seems isolated at the
radial end of-the distal row and is slightly smaller than the trapezoid still.


The metacarpals and phalanges of the free digits are so disposed as to
suggest that the hand is grasping a globe of small diameter. The end
plates of the terminal phalanges are very broad.
A Contribution to the Embryology of the Fore-Limb Skeleton 365


COMPARATIVE.
The radius and ulna likewise show constrictions in the ossifying zones. They are now very decidedly crossed. The ulnar styloid seems to be prolonged into the chondrifying discus articularis, and the same is true of the ulnar side of the lower extremity of the radius: between the two prolongations is a dense, unchondrified cell-mass. The contrast_ between this condition and that described for the 20-mm. stage is remarkable.


In discussing the features of the models described, the opportunity of
reference to other human embryos in the collection at the London Hospital
will be made use of. These embryos comprise .8-mm., 10—mm., l5°5-mm.,


24°5-mm., and 25-mm. stages, the measurements being in all cases those of
greatest length. i _


The Vertebrce.—The position and the curious form of the cervical
fiG. 9. Corona1 section, human embryo 30 mm. 0., centrale continuous through faintly staining zone with N., navicular.
vertebrae in Model I. led me to seek in earlier stages for an explanation of
the pointed caudal projection of their bodies. It is only in the cervical
vertebrae that this condition is very ma_rked,.and at first it was thought to
be purely a positional moulding. Naturally shape and position are related
features in ontogeny, a fact which in this instance is confirmed by the


The caxr-pal elements, especially those of the distal row, are well forward in development, and there is visible, both on the palmar and dprsal aspects of the wrist, a distinct centrale; on that side it lies between navicular, lunar, and trapezoid, and on this between navicular, capitatum, and trapezoid; its surface isolation does not correspond with the conditions in the depth of the articulation, where it is continuous, through a faintly staining transitional zone, with the navicular (fig. 9). The navicular is in only narrow contact with the trapezium, which seems isolated at the radial end of-the distal row and is slightly smaller than the trapezoid still.


fiG. 10.—Human embryo 10 mm. Trans. section costo-hypochordal part of vertebral blastema shown stretching between
the ventro-lateral myotome buds in front of chords.


further observation that a much less and rapidly diminishing degree of- the
The metacarpals and phalanges of the free digits are so disposed as to suggest that the hand is grasping a globe of small diameter. The end plates of the terminal phalanges are very broad.  
same moulding is visible in the upper thoracic bodies. Still, it seemed
only reasonable to expect that the shape of the cervical and upper thoracic
bodies in the adult, with their prominent ventro-caudal lips, would require
for its production something more than a process of purely adaptive growth
of the scleroblastema of what may be called the typical centrum. It remains
to explain the two correlated features by means of some material organic
addition to these vertebrae during their development; such an organic
addition is provided for in the 10-mm. stage when there is present connecting the costal elements of all the upper vertebrae a hypochordal bar of


condensed cellular tissue (fig. 10) into which the chondrification of the body _


can extend in a caudo-ventral direction. This extension will be facilitated
==Comparative==
by the positional relations of the upper vertebrae, which here form a more
sharply curved arch than those lower in the series, where the hypochordal
element is less easily identifiable. Lewis, in touching upon the hypochordal
366 Mr N. C. Rutherford


element, limits it to the upper three cervical vertebrae and connects it, not
In discussing the features of the models described, the opportunity of reference to other human embryos in the collection at the London Hospital will be made use of. These embryos comprise 8-mm., 10—mm., l5.5-mm.,
with the costal, but with the neural arches. Bardeen notes its presence as
low as the thoracic region.


The R7lbs.——Apart from the excessive length of the ribs in relation to
24°5-mm., and 25-mm. stages, the measurements being in all cases those of greatest length. i _
their average cross-section, the curve of the costal arches and the shape
of the thoracic cavity resulting are noteworthy, since, in both models, the
proportion between the depth and breadth of this is reversed as compared
with the adult form; further, the cylindrical form of the earlier stage is
seen to be transformed into a truncated cone in the later, the profile view
of which shows it to be much blunter than after completion of its. full
growth and expansion. In Model I. the ventral ends of the ribs are free,
with the exception of the first, which is fused with the sternal bar, whilst
the second, third, fourth, and fifth turn caudally alongside it, being
accommodated in fossae on its lateral aspect; in Model II. these have fused
with the side of the sternum. The cartilaginous sternal bar ends, in the
20-mm. stage, opposite thelfifth rib, and the ventral extremities of the
lower ribs turn headwards, the sixth and seventh ending in a condensed
blastema continuous with the cartilaginous sternum. It would thus appear
that the thoracic skeleton is furthest advanced in development at its inlet,
and that the fusion between rib and sternal cartilages is a secondary process,
like the fusion of the sternebral halves, as seen occurring in the third
body sternebra of the 30-mm. stage. The use of the term “sternebra” in
blastemal and cartilaginous stages is of course unjustifiable, but it has been
employed for convenience sake to designate those parts of the continuous
bar or bars which correspond to the bony segments of later stages.


The C'la/mZcle.—The form of the clavicle in Model I. is very striking by
===The Vertebrae===
reason of the absence of that curvature which characterises its outer
The position and the curious form of the cervical vertebrae in Model I. led me to seek in earlier stages for an explanation of the pointed caudal projection of their bodies. It is only in the cervical vertebrae that this condition is very ma_rked,.and at first it was thought to be purely a positional moulding. Naturally shape and position are related features in ontogeny, a fact which in this instance is confirmed by the further observation that a much less and rapidly diminishing degree of- the same moulding is visible in the upper thoracic bodies. Still, it seemed only reasonable to expect that the shape of the cervical and upper thoracic bodies in the adult, with their prominent ventro-caudal lips, would require for its production something more than a process of purely adaptive growth of the scleroblastema of what may be called the typical centrum. It remains to explain the two correlated features by means of some material organic addition to these vertebrae during their development; such an organic addition is provided for in the 10-mm. stage when there is present connecting the costal elements of all the upper vertebrae a hypochordal bar of condensed cellular tissue (fig. 10) into which the chondrification of the body can extend in a caudo-ventral direction. This extension will be facilitated by the positional relations of the upper vertebrae, which here form a more sharply curved arch than those lower in the series, where the hypochordal element is less easily identifiable. Lewis, in touching upon the hypochordal element, limits it to the upper three cervical vertebrae and connects it, not with the costal, but with the neural arches. Bardeen notes its presence as low as the thoracic region.
segment in Model II. and in the adult. In the 10-mm. stage, which may
be taken as the equivalent of that, '£.e. 106 mm., described by Lewis, the
blastematous clavicle extends inwards only one-third of the distance to the
ventral end of the first rib, which it reaches in the 15°5-mm. stage.
Arrived at this stage in its growth, the clavicle is therefore represented
only by that part which, if form be any criterion, is the equivalent, in the
adult, of its inner two-thirds at most; at this stage it seems to halt until
a short time before that represented in Model I. ; then begins a further and
distinct stage in growth coincident with the onset of ossification, one in
which the lateral third of the clavicle of the adult is evolved from the
cellular mass at the distal end (fig. 11). In this way the clavicle achieves
its full development, arriving at the condition seen in Model II. The
striking difference in the two stages of the development of a bone whose
two parts are just as strikingly different in the adult, separated as those
A Contribution to the Embryology of the Fore-Limb Skeleton 367


stages are by a considerable period of time, seems to warrant that any
theory of the growth of the clavicle should take full cognisance of the
causal facts that in the first stage the growth is axipetal, in the second,
axifugal. It may be contended that the axifugal growth of the outer
segment here emphasised is undeserving of emphasis, since it is equalled


fiG. 11. —Horizontal section, human embryo 15 '5 mm.


01. clavicle continuous laterally with suprahumeral cell mass (S.H.M.) ;
15r., prescapula; Sc., postscapula; Acr., acromion; 0.H., omohyoid.


by contemporary axipetal growth of the inner segment; but it must be
fiG. 10. Human embryo 10 mm. Trans. section costo-hypochordal part of vertebral blastema shown stretching between the ventro-lateral myotome buds in front of chords.
remembered, on the contrary, that the proportionate increase of the two
growing ends differs widely and remains in favour of the outer, otherwise
no such change in shape as occurs between that in Model I. and that in
Model II. would take place.


The Scapula.—Tl1e most striking features of the growth of the scapula,
as brought out by the two models, are the development of the supraspinous
portion, of the blade and the late appearance and mode of origin of the
368 Mr N. C. Rutherford


spine. The partial separation of the growing cartilage which represents
the supraspinous part of the blade, to which the name prescapula has been
given, especially excites curiosity. This separation is first fully recognisable in the 15°5-mm. embryo (fig. 11), and reaches its greatest differentiation
in that represented by Model II. ; it is the more remarkable in that the slit
seen in the two models between pre- and postscapula is occupied only by
cells of the limiting membranes or perichondria of the two parts (fig. 5),
and is not a passage for vessels or nerve filaments. For this reason it is to
be considered a truly morphological separation, and not merely a casual
fenestration, such as is a noticeable feature of the cartilages of certain
amphibian and reptilian shoulder girdles. It is further especially to be
remarked that the prescapular segment is fully continuous with the rest
of the blade laterally, where it bounds the scapular notch, and that, at
its other extremity, it is marked off from the blade in both models by a
distinct groove and projects somewhat from the vertebral border, where it
forms a part of this; in the former situation also it has a decided ventral
projection clothed by a distinct cell-mass, among the surface layers of which
the fibres of origin of supraspinatus are interspersed. A comparable
condition. is found in the scapula of the dolphin, Delphinus delphis (fig. 12
(III.)), a condition made the more noteworthy by the absence of anything


(resembling a true acromion process. In the toothed whale, on the other


hand, an acromion process is seemingly present, but the prescapular
equivalent is absent to all appearances (fig. 12 (I.)), whilst in Mesoplodon
Grayii a condition is present which can be regarded as an intermediate
stage between the two; in it, to adopt the accepted terminology, the


acromium is bent backwards into a prescapular position, without, however,


becoming continuous with the blade at its vertebral extremity (fig. 12 (II.)).
===The Ribs===
Here, seemingly, are three stages in the formation of a prescapular element
Apart from the excessive length of the ribs in relation to their average cross-section, the curve of the costal arches and the shape of the thoracic cavity resulting are noteworthy, since, in both models, the proportion between the depth and breadth of this is reversed as compared with the adult form; further, the cylindrical form of the earlier stage is seen to be transformed into a truncated cone in the later, the profile view of which shows it to be much blunter than after completion of its. full growth and expansion. In Model I. the ventral ends of the ribs are free, with the exception of the first, which is fused with the sternal bar, whilst the second, third, fourth, and fifth turn caudally alongside it, being accommodated in fossae on its lateral aspect; in Model II. these have fused with the side of the sternum. The cartilaginous sternal bar ends, in the 20-mm. stage, opposite thelfifth rib, and the ventral extremities of the lower ribs turn headwards, the sixth and seventh ending in a condensed blastema continuous with the cartilaginous sternum. It would thus appear that the thoracic skeleton is furthest advanced in development at its inlet, and that the fusion between rib and sternal cartilages is a secondary process, like the fusion of the sternebral halves, as seen occurring in the third body sternebra of the 30-mm. stage. The use of the term “sternebra” in blastemal and cartilaginous stages is of course unjustifiable, but it has been employed for convenience sake to designate those parts of the continuous bar or bars which correspond to the bony segments of later stages.
out of what has been previously considered an acromion process—-an assumption which, in the absence of the clavicle and the scapular spine among
Cetacea must, for the moment, remain a doubtful quantity. There is,
then, in the development of the human scapula an element, the true morphological importance of which has hitherto been disregarded, and which I
have called the prescapula, whilst in the scapula of the adult dolphin a
similar element is separable which, in its turn, is to be compared with the
so—called acromion of Mesoplodon Grayii and of the toothed whale.
Turning to the development of the spine of the scapula, we find that
appearances indicate an origin for it in a cellular proliferation connecting


with the elbow or spur of the developing acromion process (as distinct from '


the adult acromial angle); this undergoes a precocious ossification (fig. 8)
===The Clavicle===
as it spreads dorsally under the trapezius-deltoid intersection from the
The form of the clavicle in Model I. is very striking by reason of the absence of that curvature which characterises its outer segment in Model II. and in the adult. In the 10-mm. stage, which may be taken as the equivalent of that, '£.e. 106 mm., described by Lewis, the blastematous clavicle extends inwards only one-third of the distance to the ventral end of the first rib, which it reaches in the 15°5-mm. stage. Arrived at this stage in its growth, the clavicle is therefore represented only by that part which, if form be any criterion, is the equivalent, in the adult, of its inner two-thirds at most; at this stage it seems to halt until a short time before that represented in Model I. ; then begins a further and distinct stage in growth coincident with the onset of ossification, one in which the lateral third of the clavicle of the adult is evolved from the cellular mass at the distal end (fig. 11). In this way the clavicle achieves its full development, arriving at the condition seen in Model II. The striking difference in the two stages of the development of a bone whose two parts are just as strikingly different in the adult, separated as those stages are by a considerable period of time, seems to warrant that any theory of the growth of the clavicle should take full cognisance of the causal facts that in the first stage the growth is axipetal, in the second, axifugal. It may be contended that the axifugal growth of the outer segment here emphasised is undeserving of emphasis, since it is equalled by contemporary axipetal growth of the inner segment; but it must be remembered, on the contrary, that the proportionate increase of the two growing ends differs widely and remains in favour of the outer, otherwise no such change in shape as occurs between that in Model I. and that in Model II. would take place.
A Contribution to the Embryology of the Fore-Limb Skeleton 369


region of the scapular notch. The nature of the cells is, from their
appearance alone, not easy to discern, but such characteristics as they


I


%
fiG. 11. Horizontal section, human embryo 155 mm.
//


fiG. 12.—I., Scapula of Physeter Macrocephalus ; II., Scapula. of
01. clavicle continuous laterally with suprahumeral cell mass (S.H.M.) ; 15r., prescapula; Sc., postscapula; Acr., acromion; 0.H., omohyoid.
Illesoplodon Grayii; IIl., Scapula of Delphinus delphis.


possess, coupled with their secondary continuity with the fully differentiated
cartilage of the acromial elbow, places them as derivatives of cartilage
cells. Perhaps the most striking fact brought out by the second model
370 Mr N. C. Rutherford


is the formation of a bony dorsal boundary to the scapular notch
===The Scapula===
through the agency of cells which in the 30-mm. stage are continuous
The most striking features of the growth of the scapula, as brought out by the two models, are the development of the supraspinous portion, of the blade and the late appearance and mode of origin of the spine. The partial separation of the growing cartilage which represents the supraspinous part of the blade, to which the name prescapula has been given, especially excites curiosity. This separation is first fully recognisable in the 15°5-mm. embryo (fig. 11), and reaches its greatest differentiation in that represented by Model II. ; it is the more remarkable in that the slit seen in the two models between pre- and postscapula is occupied only by cells of the limiting membranes or perichondria of the two parts (fig. 5), and is not a passage for vessels or nerve filaments. For this reason it is to be considered a truly morphological separation, and not merely a casual fenestration, such as is a noticeable feature of the cartilages of certain amphibian and reptilian shoulder girdles. It is further especially to be remarked that the prescapular segment is fully continuous with the rest of the blade laterally, where it bounds the scapular notch, and that, at its other extremity, it is marked off from the blade in both models by a distinct groove and projects somewhat from the vertebral border, where it forms a part of this; in the former situation also it has a decided ventral projection clothed by a distinct cell-mass, among the surface layers of which the fibres of origin of supraspinatus are interspersed. A comparable condition. is found in the scapula of the dolphin, Delphinus delphis (fig. 12 (III.)), a condition made the more noteworthy by the absence of anything (resembling a true acromion process. In the toothed whale, on the other hand, an acromion process is seemingly present, but the prescapular equivalent is absent to all appearances (fig. 12 (I.)), whilst in Mesoplodon Grayii a condition is present which can be regarded as an intermediate stage between the two; in it, to adopt the accepted terminology, the acromium is bent backwards into a prescapular position, without, however, becoming continuous with the blade at its vertebral extremity (fig. 12 (II.)). Here, seemingly, are three stages in the formation of a prescapular element out of what has been previously considered an acromion process—-an assumption which, in the absence of the clavicle and the scapular spine among Cetacea must, for the moment, remain a doubtful quantity. There is, then, in the development of the human scapula an element, the true morphological importance of which has hitherto been disregarded, and which I have called the prescapula, whilst in the scapula of the adult dolphin a similar element is separable which, in its turn, is to be compared with the so—called acromion of Mesoplodon Grayii and of the toothed whale. Turning to the development of the spine of the scapula, we find that appearances indicate an origin for it in a cellular proliferation connecting with the elbow or spur of the developing acromion process (as distinct from the adult acromial angle); this undergoes a precocious ossification (fig. 8) as it spreads dorsally under the trapezius-deltoid intersection from the region of the scapular notch. The nature of the cells is, from their appearance alone, not easy to discern, but such characteristics as they
with those ossifying under the acromion, and which are only represented
in the 20-mm. stage by the mass lying most thickly at the root of the
prescapula. The position and relations of this cellular proliferation are
very suggestive, especially in view of the ossific process which takes place
in it so early after its assumption of rapid growth. firstly, it overlies the
junctional zone between coracoid and scapula; secondly, it lies at the dorsal
extremity of a band of thickly crowded cells which passes medial to the
coracoid (figs. 6 and 11) to divide into three well-marked strands merging
with the periosteal layer of the outer segment of the clavicle; thirdly, this
connexion is identifiable in the 15°5-mm. embryo as a dense strand forming
the mesial boundary of a cell-mass which includes more laterally the
prechondral representatives of acromion and clavicle, the middle of which
is less condensed than its mesial and lateral margins. The mesial
margin is well seen in fig. 11, and can be traced dorsally to the nucleus of
chondrification representing the prescapular element and ventrally to the
clavicle, whilst the middle third of it gives origin to the omohyoid, just
lateral to the subclavian vein. The ossification of the scapula commencing
at a junctional zone is remarkable as a parallel phenomenon to that
described by Professor Fawcett in the ossification of the clavicle ; closer
examination may show even greater resemblance in the details of the
process; whilst further, in view of the importance of junctional zones as
centres of growth, brought out by the work of Professor Geddes on the
Vertebrate Limb, an even more widely generalised significance may be
attributable to this fact in the growth of the scapula. The cell strand
connecting prescapula and clavicle is so far differentiated in fig. 6 that it
represents the typical position of those ligamentous fibres which in many
adults pass along the upper part of the conoid ligament into the transverse


ligament; in this figure the omohyoid origin is not connected with these


fibres, a factwhich is referable to the dorsal migration of the origin towards
the scapula. T


The explanation of the observed facts bases itself mainly upon the
fiG. 12.—I., Scapula of Physeter Macrocephalus ; II., Scapula. of Illesoplodon Grayii; IIl., Scapula of Delphinus delphis.
presence of the large cell-mass in the upper shoulder region in the 15°5-mm.
stage. This mass is continuous with the acromion laterally, with the
prescapula _ dorsally, and with the outer extremity of the chondrifying
clavicular bar ventrally. It is in this mass that the specialisation of the
clavicle-acromion arch so closely related to the evolution of a freely movable
shoulder-joint must occur, and, since this specialisation is especially
important in man, the steps of its development may be expected to abound
in matter for comparison with the vertebrate girdles down even to those
A Contribution to the Embryology of the Fore-Limb Skeleton 371


of thereptilia. Taking into consideration the variety of forms among the
possess, coupled with their secondary continuity with the fully differentiated cartilage of the acromial elbow, places them as derivatives of cartilage cells. Perhaps the most striking fact brought out by the second model is the formation of a bony dorsal boundary to the scapular notch through the agency of cells which in the 30-mm. stage are continuous with those ossifying under the acromion, and which are only represented in the 20-mm. stage by the mass lying most thickly at the root of the prescapula. The position and relations of this cellular proliferation are very suggestive, especially in view of the ossific process which takes place in it so early after its assumption of rapid growth. firstly, it overlies the junctional zone between coracoid and scapula; secondly, it lies at the dorsal extremity of a band of thickly crowded cells which passes medial to the coracoid (figs. 6 and 11) to divide into three well-marked strands merging with the periosteal layer of the outer segment of the clavicle; thirdly, this connexion is identifiable in the 15°5-mm. embryo as a dense strand forming the mesial boundary of a cell-mass which includes more laterally the prechondral representatives of acromion and clavicle, the middle of which is less condensed than its mesial and lateral margins. The mesial margin is well seen in fig. 11, and can be traced dorsally to the nucleus of chondrification representing the prescapular element and ventrally to the clavicle, whilst the middle third of it gives origin to the omohyoid, just lateral to the subclavian vein. The ossification of the scapula commencing at a junctional zone is remarkable as a parallel phenomenon to that described by Professor Fawcett in the ossification of the clavicle ; closer examination may show even greater resemblance in the details of the process; whilst further, in view of the importance of junctional zones as centres of growth, brought out by the work of Professor Geddes on the Vertebrate Limb, an even more widely generalised significance may be attributable to this fact in the growth of the scapula. The cell strand connecting prescapula and clavicle is so far differentiated in fig. 6 that it represents the typical position of those ligamentous fibres which in many adults pass along the upper part of the conoid ligament into the transverse ligament; in this figure the omohyoid origin is not connected with these fibres, a factwhich is referable to the dorsal migration of the origin towards the scapula.
mammalia assumed by these portions of the skeleton, the cell-masses which
are their precursors in ontogeny must be regarded as possessing a remarkable degree of lability, and, for this very reason, as being likely to preserve
in the stages of their early development certain main features of their
common and very early precursors in phylogeny. The earliest form of
the human shoulder girdle, as figured by Lewis for a 10'5-mm. embryo,
is a rectangular mass of crowded cells representing a scapula ‘and situated
high in the cervical region, to all appearance a plate-like headward prolongation of the axial condensation of the free limb.‘ In it, again, according
to Lewis’s figure, there is a shallow furrow which may or may not be the
first indication of the slit found in the cartilaginous scapula of later stages;
if it be not, I am inclined strongly to the view that this rectangular mass
of cells represents rather the prescapula of the cartilage stages than the
postscapula, and from its caudo-lateral angle the postscapula may grow
out; this View would be little more than speculation if it were not that
the prescapula of a 15'5-mm. embryo shows a more advanced stage of
differentiation than does the rest of the scapula. This is, however, a point
on which the material at my disposal does not provide any further evidence
of conclusive value, and which is of minor importance for the further
development of the deductions made from the other facts observed in order
to elucidate the connexion of prescapula and clavicle. This connexion has
been fully described and figured, as has also the evolution of the so-called
acromion in the Cetacea, through which it becomes converted in Delphvlmos
delphis into a remarkable semblance of the human cartilaginous prescapula;
and it only remains, in the first place, to emphasise that the connexion of the
human prescapula with the clavicle is made at the mesial extremity of the
lateral segment of the clavicle, and, in the second place, to postulate that
the Cetacean so-called acromion connected with the clavicle of Cetacean
progenitors, in order to reach the conclusion that the labile substance of
the shoulder region can produce under evolution a mesial and a lateral
arch ; that one prescapulo-palaeoclavicular — possibly identifiable in
Cetacean ontogeny—this one acromio-neoclavicular in nature. In support
of this conclusion and of the one postulate furthering it are a number
of indisputable facts :—


1. That the ingrowth of the clavicle in stages from 10 mm. onwards
occurs, not from the region of the tip of the acromion (sensu stricto as here
applied), but from the ventral extremity of the strand of cells which forms
the mesial limit of the suprahumeral arch mass, the outer periphery of
which will later give rise to the outer segment of the clavicle ventrally and


to the acromion dorsally. This is beautifully demonstrated in fig. 11,
The explanation of the observed facts bases itself mainly upon the presence of the large cell-mass in the upper shoulder region in the 15.5-mm. stage. This mass is continuous with the acromion laterally, with the prescapula dorsally, and with the outer extremity of the chondrifying clavicular bar ventrally. It is in this mass that the specialisation of the clavicle-acromion arch so closely related to the evolution of a freely movable shoulder-joint must occur, and, since this specialisation is especially important in man, the steps of its development may be expected to abound in matter for comparison with the vertebrate girdles down even to those of thereptilia. Taking into consideration the variety of forms among the mammalia assumed by these portions of the skeleton, the cell-masses which are their precursors in ontogeny must be regarded as possessing a remarkable degree of lability, and, for this very reason, as being likely to preserve in the stages of their early development certain main features of their common and very early precursors in phylogeny. The earliest form of the human shoulder girdle, as figured by Lewis for a 10'5-mm. embryo, is a rectangular mass of crowded cells representing a scapula and situated high in the cervical region, to all appearance a plate-like headward prolongation of the axial condensation of the free limb.‘ In it, again, according to Lewis’s figure, there is a shallow furrow which may or may not be the first indication of the slit found in the cartilaginous scapula of later stages; if it be not, I am inclined strongly to the view that this rectangular mass of cells represents rather the prescapula of the cartilage stages than the postscapula, and from its caudo-lateral angle the postscapula may grow out; this View would be little more than speculation if it were not that the prescapula of a 15'5-mm. embryo shows a more advanced stage of differentiation than does the rest of the scapula. This is, however, a point on which the material at my disposal does not provide any further evidence of conclusive value, and which is of minor importance for the further development of the deductions made from the other facts observed in order to elucidate the connexion of prescapula and clavicle. This connexion has been fully described and figured, as has also the evolution of the so-called acromion in the Cetacea, through which it becomes converted in Delphvlmos delphis into a remarkable semblance of the human cartilaginous prescapula; and it only remains, in the first place, to emphasise that the connexion of the human prescapula with the clavicle is made at the mesial extremity of the lateral segment of the clavicle, and, in the second place, to postulate that the Cetacean so-called acromion connected with the clavicle of Cetacean progenitors, in order to reach the conclusion that the labile substance of the shoulder region can produce under evolution a mesial and a lateral arch ; that one prescapulo-palaeoclavicular possibly identifiable in Cetacean ontogeny—this one acromio-neoclavicular in nature. In support of this conclusion and of the one postulate furthering it are a number of indisputable facts :—
voL. XLVIII. (THIRD SER. voL. 1x.)—-JULY 1914. 26
372 Mr N. C. Rutherford


155, which, it will be remembered, comes from a stage 155 mm., in which
1. That the ingrowth of the clavicle in stages from 10 mm. onwards occurs, not from the region of the tip of the acromion (sensu stricto as here applied), but from the ventral extremity of the strand of cells which forms the mesial limit of the suprahumeral arch mass, the outer periphery of which will later give rise to the outer segment of the clavicle ventrally and to the acromion dorsally. This is beautifully demonstrated in fig. 11, 15.5, which, it will be remembered, comes from a stage 155 mm., in which the clavicle has reached to the ventral extremity of the first rib.
the clavicle has reached to the ventral extremity of the first rib.


2. That the variations in origin of the posterior belly of the omohyoid
2. That the variations in origin of the posterior belly of the omohyoid muscle almost never follow the lateral or acromio-clavicular, but nearly always the mesial or prescapulo-precoracoid arch.
muscle almost never follow the lateral or acromio-clavicular, but nearly
always the mesial or prescapulo-precoracoid arch.


3. That in the two-toed sloth, Uholwpus H0fi"ma'n/n/£7}, the prescapula and
3. That in the two-toed sloth, Uholwpus H0fi"ma'n/n/£7}, the prescapula and acromion are synostosed, and with the complete arch thus constituted from the periphery of the suprahumeral mass the clavicle articulates, which clavicle, to judge by its sole curvature, a ventral convexity, represents only the precoracoid portion of that bone (fig. 13). By reason of the primitive scale of general mammalian organisation found in the Edentata, and also by reason of the habits of the sloth, this fact supports both the conclusion I have come to and the postulate regarding the Cetacean clavicle necessary to its validity in the comparative sense.
acromion are synostosed, and with the complete arch thus constituted from
the periphery of the suprahumeral mass the clavicle articulates, which
clavicle, to judge by its sole curvature, a ventral convexity, represents only
the precoracoid portion of that bone (fig. 13). By reason of the primitive
scale of general mammalian organisation found in the Edentata, and also by
reason of the habits of the sloth, this fact supports both the conclusion I


(\I


fiG. 13.—Scapula. Clavicle of two-toed sloth, Cholaepus
Hofimannii, showing acromio-prescapular arch.


have come to and the postulate regarding the Cetacean clavicle necessary to
fiG. 13.—Scapula. Clavicle of two-toed sloth, Cholaepus Hofimannii, showing acromio-prescapular arch.
its validity in the comparative sense.


To summarise, the shoulder arch in man shows in its development a
fair epitome of the phylogenetic steps in its specialisation from a type which
would be fairly represented by the shoulder girdle of the toothed whale,
did this possess a clavicle, a type extant in both Ornithorhynchus and
Echidna. With advancing specialisation the original arch becomes converted to other uses; the primitive acromion becomes the supraspinous
plate, and a new acromion is evolved, whose earliest trace is possibly
identifiable in Echidna and whose intermediate form is exemplified in the
sloth, this new acromion having a wider sweep and necessitating an
addition to the primitive clavicle. Meanwhile the intermediate portion
of the original arch merges in, or specialises as the transverse and part
of the conoid ligaments of man.


This theory of the development of two arches in the mammalian shoulder
To summarise, the shoulder arch in man shows in its development a fair epitome of the phylogenetic steps in its specialisation from a type which would be fairly represented by the shoulder girdle of the toothed whale, did this possess a clavicle, a type extant in both Ornithorhynchus and Echidna. With advancing specialisation the original arch becomes converted to other uses; the primitive acromion becomes the supraspinous plate, and a new acromion is evolved, whose earliest trace is possibly identifiable in Echidna and whose intermediate form is exemplified in the sloth, this new acromion having a wider sweep and necessitating an addition to the primitive clavicle. Meanwhile the intermediate portion of the original arch merges in, or specialises as the transverse and part of the conoid ligaments of man.
girdle deserves a reference to the conditions in lower vertebrates. In the
reptiles the so-called clavicle often reaches far on to the dorsum of the
A Contribution to the Embryology of the Fore-Limb Skeleton 373


scapula, whilst as yet no acromion can be said to exist, indeed the dorsal
portion of the clavicle occupies a position on the reptilian scapula which is
only comparable with that of the scapular spine in man, or in other mammals
in which a truly homologous spine is developed. Such an extension of the
clavicle may reasonably be supposed, I think, to follow the line of our
prescapulo-precoracoid arch, and thus leads on to the hypothesis that that
cellular covering of the root of the prescapula (fig. 6) which ossifies to form
a bony spicule, the definitive dorsal edge of the scapular notch, and which
further extends to the root of the acromion and under the trapeziusdeltoid intersection to form the spine of the scapula, ossifying as it goes, is
the homologue of part’ of the original reptilian clavicle. This is only,‘
however, a hypothesis, but it has so many favourable features that it seems
worthy of the more exhaustive examination of embryonic and comparative
material necessary for its proof and acceptance as a well-grounded theory.


The secondary coalescence of spine and acromion would well account
This theory of the development of two arches in the mammalian shoulder girdle deserves a reference to the conditions in lower vertebrates. In the reptiles the so-called clavicle often reaches far on to the dorsum of the scapula, whilst as yet no acromion can be said to exist, indeed the dorsal portion of the clavicle occupies a position on the reptilian scapula which is only comparable with that of the scapular spine in man, or in other mammals in which a truly homologous spine is developed. Such an extension of the clavicle may reasonably be supposed, I think, to follow the line of our prescapulo-precoracoid arch, and thus leads on to the hypothesis that that cellular covering of the root of the prescapula (fig. 6) which ossifies to form a bony spicule, the definitive dorsal edge of the scapular notch, and which further extends to the root of the acromion and under the trapeziusdeltoid intersection to form the spine of the scapula, ossifying as it goes, is the homologue of part’ of the original reptilian clavicle. This is only,‘ however, a hypothesis, but it has so many favourable features that it seems worthy of the more exhaustive examination of embryonic and comparative material necessary for its proof and acceptance as a well-grounded theory.
for the proliferation which forms a spur on the acromial elbow in Model II.,
and a similar but more marked outgrowth in this junctional zone doubtless
results in the formation of a metacromion as found in certain rodents, and
markedly in the elephant. For particularly directing my attention to this
structure, I am indebted to Professor Wright.


The humerus in the forms in which it appears in Models I. and II. is a
very interesting object. Its curvatures are striking, and the torsion and
angulation of its upper and lower extremities are brought out in a way
which previously figured reconstructions have failed to indicate. This is
to be attributed to the method I have adopted of drawing only the limits
of the cartilage and avoiding the perichondrium, at stages in development
when the differentiation of that tissue has reached or slightly overstepped
its “ optimum.” The seeming contrast between the two forms is dispelled
on close examination of the second model, and the change is attributable
only to the enormously increased length of the shaft and its relatively
decreased girth in the region of the primary ossification. Distortions of
the shafts of long bones have been noted in embryo by Holl, Schomberg,
and others, and attributed to disproportionately rapid growth in length;
these are especially marked in hardened specimens and are therefore
probably artificial. Of such artificiality I see no trace in the developing
humerus, either in Lewis’s figures or my own material, and I consider that
both the described curvatures of the shaft are a phenomenon of correlated
growth during development of humerus and musculo-spiral nerve in the
first place, somewhat exaggerated by the shortness of the shaft and the
form of the unspecialised articular ends, and, possibly, later, by the related
deltoid insertion in the second place. That the spiral groove of the adult
. 374 Mr N. C. Rutherford


humerus is so much broader than the structures lying in it is merely an
The secondary coalescence of spine and acromion would well account for the proliferation which forms a spur on the acromial elbow in Model II., and a similar but more marked outgrowth in this junctional zone doubtless results in the formation of a metacromion as found in certain rodents, and markedly in the elephant. For particularly directing my attention to this structure, I am indebted to Professor Wright.


indication of the early date of its production, when the girth of the nerve ‘


relative to the length of the bone was much greater and separated the origin
The humerus in the forms in which it appears in Models I. and II. is a very interesting object. Its curvatures are striking, and the torsion and angulation of its upper and lower extremities are brought out in a way which previously figured reconstructions have failed to indicate. This is to be attributed to the method I have adopted of drawing only the limits of the cartilage and avoiding the perichondrium, at stages in development when the differentiation of that tissue has reached or slightly overstepped its “ optimum.” The seeming contrast between the two forms is dispelled on close examination of the second model, and the change is attributable only to the enormously increased length of the shaft and its relatively decreased girth in the region of the primary ossification. Distortions of the shafts of long bones have been noted in embryo by Holl, Schomberg, and others, and attributed to disproportionately rapid growth in length; these are especially marked in hardened specimens and are therefore probably artificial. Of such artificiality I see no trace in the developing humerus, either in Lewis’s figures or my own material, and I consider that both the described curvatures of the shaft are a phenomenon of correlated growth during development of humerus and musculo-spiral nerve in the first place, somewhat exaggerated by the shortness of the shaft and the form of the unspecialised articular ends, and, possibly, later, by the related deltoid insertion in the second place. That the spiral groove of the adult humerus is so much broader than the structures lying in it is merely an indication of the early date of its production, when the girth of the nerve relative to the length of the bone was much greater and separated the origin of the two humeral heads of the triceps at the time when they were acquiring a firm attachment to the ossifying tissue‘ of the shaft; for muscles never attach themselves to cartilage, but only to the perichondrial membrane, which is later incorporated with the periphery of the bone. The causation of the spiral groove of the humerus has no relation to the torsions about to be considered.
of the two humeral heads of the triceps at the time when they were acquiring
a firm attachment to the ossifying tissue‘ of the shaft; for muscles never
attach themselves to cartilage, but only to the perichondrial membrane,
which is later incorporated with the periphery of the bone. The causation
of the spiral groove of the humerus has no relation to the torsions about
to be considered. n


The changes of torsion and angulation of the articular ends which take
place between the 20-mm. and the 30-mm. stages are attributable in the
case of the upper extremity to the pre- and postnatal alteration of position
of the scapula, relative both to the axis of the humerus and to the curve of
the chest wall; in the one case the change is an approach of the axillary
border of the scapula to the humerus, and in the other it is a change due
to the increase in length and curvature of the ribs, causing the scapula to
migrate towards the vertebrae and the head of the humerus to rotate
inwards to accommodate itself to the altered aspect of the glenoid. The
alteration in the inclination of the distal articular surfaces to the axis of
the shaft is productive of the specialisation of the elbow-joint for pronation
and supination of the forearm bones. Lewis, in Keibel and Mallis T eastbook, p. 380, states that in an 11-mm. embryo, the forearm is midway
between pronation and supination. This statement is incorrect, in principle
and in detail, for, almost up to the 20-mm. stage, pronation and supination
as movements or as postures are out of the question, owing to the form of
the distal extremity of the humerus, the details of the skeleton showing
that the forearm bones are parallel T and the hand apparently fully supine
if the plane of the hand be projected upon the plane of the lower end of
the humerus; the right-angled elbow, parallel forearm bones, and paddlepostured hand make an exact reproduction of the palaeo-reptilian fore-limb.
The sex difference which is characteristic of the limb in the adult would
seem to rest upon a less degree of specialisation of the upper extremity in
the female than in the male, resulting in the greater “ carrying angle ” of
the female. The correlation (if it be one) of this inferior grade of specialisation in the female upper limb With a higher grade of specialisation in the
female pelvis is an interesting paradox.


The radius and ulna have been almost sufficiently discussed in connexion
The changes of torsion and angulation of the articular ends which take place between the 20-mm. and the 30-mm. stages are attributable in the case of the upper extremity to the pre- and postnatal alteration of position of the scapula, relative both to the axis of the humerus and to the curve of the chest wall; in the one case the change is an approach of the axillary border of the scapula to the humerus, and in the other it is a change due to the increase in length and curvature of the ribs, causing the scapula to migrate towards the vertebrae and the head of the humerus to rotate inwards to accommodate itself to the altered aspect of the glenoid. The alteration in the inclination of the distal articular surfaces to the axis of the shaft is productive of the specialisation of the elbow-joint for pronation and supination of the forearm bones. Lewis, in Keibel and Mallis T eastbook, p. 380, states that in an 11-mm. embryo, the forearm is midway between pronation and supination. This statement is incorrect, in principle and in detail, for, almost up to the 20-mm. stage, pronation and supination as movements or as postures are out of the question, owing to the form of the distal extremity of the humerus, the details of the skeleton showing that the forearm bones are parallel T and the hand apparently fully supine if the plane of the hand be projected upon the plane of the lower end of the humerus; the right-angled elbow, parallel forearm bones, and paddlepostured hand make an exact reproduction of the palaeo-reptilian fore-limb. The sex difference which is characteristic of the limb in the adult would seem to rest upon a less degree of specialisation of the upper extremity in the female than in the male, resulting in the greater “ carrying angle ” of the female. The correlation (if it be one) of this inferior grade of specialisation in the female upper limb With a higher grade of specialisation in the female pelvis is an interesting paradox.
with the distal extremity of the humerus; it only remains to add that, if
the inclination of forearm to arm be a true sex characteristic, the differential
torsion of the two extremities of the ulna and the relative aspects of the
articular surfaces of the radius should, if made capable of convenient
A Contribution to the Embryology of the Fore-Limb Skeleton 375


measurement, prove a valuable means for determination of sex in osteology
and anthropology. 6


The Uarpus and Hand.-—'1‘he presence of a centrale in Model II. and
The radius and ulna have been almost sufficiently discussed in connexion with the distal extremity of the humerus; it only remains to add that, if the inclination of forearm to arm be a true sex characteristic, the differential torsion of the two extremities of the ulna and the relative aspects of the articular surfaces of the radius should, if made capable of convenient measurement, prove a valuable means for determination of sex in osteology and anthropology.  
the mode of its inclusion are not in agreement with the observations of
Graefenberg. Graefenberg’s material seemingly did not include a stage as
early as that of Model I., in which no centrale is to be found, for he
states that it is among those carpal elements earliest differentiated, and,
further, that it is probably broken up by the appearance of the lunar,
and finally disappears, leaving no trace. As against these statements I
have to place the facts that the centrale is unrepresented in my 20-mm.
stage, yet in my 30-mm. stage it is visible on both Ventral and dorsal
aspects of the carpus, where it is entirely separated from all other elements
by a distinct perichondrium, and that in the depth of the massed elements
it is structurally continuous with the naviculare through a faintly staining
cartilaginous layer. (fig. 9). This further confirms Owen’s and MiVart’s
views on the fate of the centrale, whilst opposing those of Rosenberg
and Thilenius, and partially also those of Leboucq. The isolation of the
trapezium on the radial side of the carpus has been noted in description
of Model I.; its position confirms the observation of Hagen, one which
Graefenberg professes to be unable to understand, in that it is practically
confined to the ventral aspect of the wrist.


The question of the relation of intermedium and discus articularis
===The Carpus and Hand===
cannot be fully entered into here because of the limited amount of material
The presence of a centrale in Model II. and the mode of its inclusion are not in agreement with the observations of Graefenberg. Graefenberg’s material seemingly did not include a stage as early as that of Model I., in which no centrale is to be found, for he states that it is among those carpal elements earliest differentiated, and, further, that it is probably broken up by the appearance of the lunar, and finally disappears, leaving no trace. As against these statements I have to place the facts that the centrale is unrepresented in my 20-mm. stage, yet in my 30-mm. stage it is visible on both Ventral and dorsal aspects of the carpus, where it is entirely separated from all other elements by a distinct perichondrium, and that in the depth of the massed elements it is structurally continuous with the naviculare through a faintly staining cartilaginous layer. (fig. 9). This further confirms Owen’s and MiVart’s views on the fate of the centrale, whilst opposing those of Rosenberg and Thilenius, and partially also those of Leboucq. The isolation of the trapezium on the radial side of the carpus has been noted in description of Model I.; its position confirms the observation of Hagen, one which Graefenberg professes to be unable to understand, in that it is practically confined to the ventral aspect of the wrist.
under discussion, but the appearance of a separate cartilaginous nodule in
the 20-mm. stage, embedded in a mass of thickly crowded cells, and the
absence of such an element in the later stage, which shows chondrification
of the cell-mass in continuity, on the one side, with the ulnar styloid, and,


"on the other, with the inner edge of the extremity of the radius, both


seem to indicate early differentiation of an intermedium, followed by its
The question of the relation of intermedium and discus articularis cannot be fully entered into here because of the limited amount of material under discussion, but the appearance of a separate cartilaginous nodule in the 20-mm. stage, embedded in a mass of thickly crowded cells, and the absence of such an element in the later stage, which shows chondrification of the cell-mass in continuity, on the one side, with the ulnar styloid, and, on the other, with the inner edge of the extremity of the radius, both seem to indicate early differentiation of an intermedium, followed by its disappearance and replacement by the discus.
disappearance and replacement by the discus.


SUMMARY or CONCLUSIONS.
==Summary Or Conclusions==


Technical.
Technical.


1. The first and perhaps the most critical matter, in its bearing upon
1. The first and perhaps the most critical matter, in its bearing upon the technical results of this work, is the imperative necessity, in preparing a reconstruction of the cartilaginous skeleton, to adhere slavishly, in the drawings made, to the periphery of the fully differentiated cartilage and to exclude all the surrounding transitional perichondrial tissue.
the technical results of this work, is the imperative necessity, in preparing
a reconstruction of the cartilaginous skeleton, to adhere slavishly, in the
drawings made, to the periphery of the fully differentiated cartilage and to
exclude all the surrounding transitional perichondrial tissue.


2. The second conclusion of a technical kind follows from the first, and
2. The second conclusion of a technical kind follows from the first, and is, that reconstructions of the developing skeleton, at stages earlier than the 376 Mr N. C. Rutherford
is, that reconstructions of the developing skeleton, at stages earlier than the
376 Mr N. C. Rutherford


“optimum” of cartilaginous development, must necessarily be ambiguous
“optimum” of cartilaginous development, must necessarily be ambiguous since the zones of transition are much wider and more difficult of limitation, whilst the shape of the growing chondral nuclei signifies nothing of a more than ontogenetic importance. It is not desired to convey by this that the form of the condensed blastemal skeleton suffers under the same disability for comparative purposes, quite the contrary; the blastematous stage, also, has an “ optimum” development, only one which is more diflicult to assess than is that of the cartilage; it probably lies in or around the immediately prechondral period. It is further desirable to emphasise that nothing in these conclusions can apply to elements which manifest anything in the nature of direct ossification, that is to say, which, among vertebrates, may ossify otherwise than through the intermediation of cartilage; for example, a drawing and reconstruction of such an element as the chondral clavicle will convey nothing of value, because the chondrification of the clavicle never reaches an “ optimum ” in the accepted sense.
since the zones of transition are much wider and more difficult of limitation,
whilst the shape of the growing chondral nuclei signifies nothing of a more
than ontogenetic importance. It is not desired to convey by this that the
form of the condensed blastemal skeleton suffers under the same disability
for comparative purposes, quite the contrary; the blastematous stage, also,
has an “ optimum” development, only one which is more diflicult to assess
than is that of the cartilage; it probably lies in or around the immediately
prechondral period. It is further desirable to emphasise that nothing in
these conclusions can apply to elements which manifest anything in the
nature of direct ossification, that is to say, which, among vertebrates,
may ossify otherwise than through the intermediation of cartilage;
for example, a drawing and reconstruction of such an element as the
chondral clavicle will convey nothing of value, because the chondrification
of the clavicle never reaches an “ optimum ” in the accepted sense.


3. The blastema stage of the shoulder skeleton represents in its massive
3. The blastema stage of the shoulder skeleton represents in its massive cell agglomeration two arches, one mesial, consisting of the precursors of the supraspinous portion of the scapula and the cell-strand connecting this with the clavicle at the junction of its sternal and acromial segments, and one lateral, representing the acromion and acromial segment of the clavicle, both having comparable though simpler bony representatives in the Edentate Oholcvpus Hofimannii. In the absence of the clavicle of their progenitors the Cetacea show a conversion of the dorsal pillar of the medial arch into prescapula.
cell agglomeration two arches, one mesial, consisting of the precursors of
the supraspinous portion of the scapula and the cell-strand connecting this
with the clavicle at the junction of its sternal and acromial segments, and
one lateral, representing the acromion and acromial segment of the clavicle,
both having comparable though simpler bony representatives in the
Edentate Oholcvpus Hofimannii. In the absence of the clavicle of their
progenitors the Cetacea show a conversion of the dorsal pillar of the medial
arch into prescapula.


4. The supraspinous portion of the scapula may possibly be the original
4. The supraspinous portion of the scapula may possibly be the original scapula of phylogeny; it certainly is a separate morphological constituent of the scapula, as evidenced by the course of its development in man and by the various forms of its equivalent in the Cetaceans cited.
scapula of phylogeny; it certainly is a separate morphological constituent
of the scapula, as evidenced by the course of its development in man and by
the various forms of its equivalent in the Cetaceans cited.


5. The formation and precocious ossification of the spine of the scapula
5. The formation and precocious ossification of the spine of the scapula begins in cells which, appearing at the root of the prescapula, grow on to the dorsum along the coraco-scapular junction and under the trapeziusdeltoid intersection, cells which are therefore intimately related to the mesial arch, and may be, like this, representative of the reptilian clavicle. Spine and acromion are joined up through the intermediation of these cells, and the junctional proliferation may be so marked as to result, under ossification, in the production of a metacromion, as in certain rodents, and markedly in the elephant.
begins in cells which, appearing at the root of the prescapula, grow on to
the dorsum along the coraco-scapular junction and under the trapeziusdeltoid intersection, cells which are therefore intimately related to the
mesial arch, and may be, like this, representative of the reptilian clavicle.
Spine and acromion are joined up through the intermediation of these cells,
and the junctional proliferation may be so marked as to result, under
ossification, in the production of a metacromion, as in certain rodents, and
markedly in the elephant.


6. The spiral groove of the humerus is due to the impress of the
6. The spiral groove of the humerus is due to the impress of the musculo-spiral nerve and is not due to torsion, which, however, is not absent during the growth of the cartilage, but affects only the proximal end.
musculo-spiral nerve and is not due to torsion, which, however, is not
absent during the growth of the cartilage, but affects only the proximal


end.
7. The specialisation of the distal articular surfaces of the humerus takes place Within the stages examined, and its degree is different in the two sexes.
A Contribution to the Embryology of the Fore-Limb Skeleton 377


7. The specialisation of the distal articular surfaces of the humerus takes
8. The carpal centrale is most fully developed in cartilage about the “optimum” period for the other carpal cartilages. It fuses with the navicular.
place Within the stages examined, and its degree is different in the two
sexes.


8. The carpal centrale is most fully developed in cartilage about the
9. The intermedium is present in the 20-mm. stage, and disappears before the 30-mm. stage to make way for the chondrification of the articular disc from its ulnar and radial extremities.
“optimum” period for the other carpal cartilages. It fuses with the
navicular.


9. The intermedium is present in the 20-mm. stage, and disappears
==Acknowledgments==


before the 30-mm. stage to make way for the chondrification of the
I desire to record my thanks to Professor W. Wright for the kindly interest With Which he has followed the completion of this Work; to Professor A. C. Geddes, firstly, for the use of apparatus for reconstruction, Which was his private property, and, secondly, for the advice Which, when in any difficulty, I could always fall back upon with benefit.
articular disc from its ulnar and radial extremities.


ACKNOWLEDGMENTS.
The publication has been carried out with the help of a grant from the Research Fund of the London Hospital Medical College; the drawings are


I desire to record my thanks to Professor W. Wright for the kindly
by Mr W. Thornton Shiells; in the photography I have been much assisted by Mr T. Collyer Summers.
interest With Which he has followed the completion of this Work; to
Professor A. C. Geddes, firstly, for the use of apparatus for reconstruction,
Which was his privateproperty, and, secondly, for the advice Which, when
in any difficulty, I could always fall back upon with benefit.


The publication has been carried out with the help of a grant from the
==Bibliography of References==
Research Fund of the London Hospital Medical College; the drawings are


by Mr W. Thornton Shiells; in the photography I have been much assisted
Most of the papers referred to are quoted in the Bibliography on pp. 391-397, vol. i., of the Manual of Human Embryology, by Keibel and Mall. In addition are the following :—
by Mr T. Collyer Summers.


BIBLIOGRAPHY OF REFERENCES.
FAWCETT, E., “The Development and Ossification of the Human Clavicle,” Journ. of Anat. and Phys., vol. xlvii. p. 225.


Most of the papers referred to are quoted in the Bibliography on pp. 391-397,
GEDDES, A. (3., “‘ The Origin of the Vertebrate Limb,” Journ. of Anal. and Phys., vol. xlvi. p. 350.
vol. i., of the Manual of Human Embryology, by Keibel and Mall. In addition are
the following :—


FAWCETT, E., “The Development and Ossification of the Human Clavicle,”
{{Footer}}
Journ. of Anat. and Phys., vol. xlvii. p. 225.


GEDDES, A. (3., “‘ The Origin of the Vertebrate Limb,” Journ. of Anal. and Phys.,
[[Category:Historic Embryology]][[Category:1910's]][[Category:Limb]][[Category:Draft]]
vol. xlvi. p. 350.

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Rutherford NC. A contribution to the embryology of the fore-limb. (1914) J Anat Physiol. 48: 355-377.

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This 1914 historic paper describes upper limb development in the embryo. See links below for the modern notes.



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Musculoskeletal Links: Introduction | mesoderm | somitogenesis | limb | cartilage | bone | bone timeline | bone marrow | shoulder | pelvis | axial skeleton | skull | joint | skeletal muscle | muscle timeline | tendon | diaphragm | Lecture - Musculoskeletal | Lecture Movie | musculoskeletal abnormalities | limb abnormalities | developmental hip dysplasia | cartilage histology | bone histology | Skeletal Muscle Histology | Category:Musculoskeletal
Historic Embryology - Musculoskeletal  
1853 Bone | 1885 Sphenoid | 1902 - Pubo-femoral Region | Spinal Column and Back | Body Segmentation | Cranium | Body Wall, Ribs, and Sternum | Limbs | 1901 - Limbs | 1902 - Arm Development | 1906 Human Embryo Ossification | 1906 Lower limb Nerves and Muscle | 1907 - Muscular System | Skeleton and Limbs | 1908 Vertebra | 1908 Cervical Vertebra | 1909 Mandible | 1910 - Skeleton and Connective Tissues | Muscular System | Coelom and Diaphragm | 1913 Clavicle | 1920 Clavicle | 1921 - External body form | Connective tissues and skeletal | Muscular | Diaphragm | 1929 Rat Somite | 1932 Pelvis | 1940 Synovial Joints | 1943 Human Embryonic, Fetal and Circumnatal Skeleton | 1947 Joints | 1949 Cartilage and Bone | 1957 Chondrification Hands and Feet | 1968 Knee
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A Contribution to the Embryology of the Fore-Limb Skeleton

By N. C. Rutherford, M.B., F.R.C.S.

Introductory

THE concise account of the development of the human skeleton recently published in the Keibel and Mall Tecct-boo/c of Human Embryology forms the standpoint of present knowledge of and opinion on the subject. Regarded from this standpoint, certain observations of some importance resulting from a study of the development of the shoulder girdle and forelimb skeleton in man, recently undertaken by the writer, seem worthy of publication as supplementing the account of the cardinal features in the growth of these cartilages and giving an account of the early phenomena of the ossification of the scapula. In considering the observations made on the development of the skeletal arch which overhangs and strengthens the shoulder-joint, its origin from one of a smaller perimeter will be the chief subject of discussion. The embryonic material employed consists of human embryos and foetuses of from 10 to 30 mm. in greatest length, reconstructions of the fore-quarter skeletons being made in two cases, one a 20-millimetre and the other a 30-millimetre specimen. The specimens cited in comparison are in the Museum of the Royal College of Surgeons. As it is on the reconstructions that the initial Observations were made and round them that the whole work centres, a short description of them forms the first part of this paper.


Technical Note. — In making the drawings of the cartilaginous skeleton, care was taken to indicate exactly the margins of the fully differentiated cartilage as contrasted with the transitional perichondrial layers in all cases except that of the clavicle in which the easily followed enveloping layer was shown. VOL. XLVIII. (THIRD SER. VOL. IX.)—JULY 1914. 25 356 4 A Mr N. C. Rutherford

Descriptive

Model of the Fore-quarter Skeleton of a, 20 mm. Human Embryo (figs. 1 and 2).

This model includes :— Twelve vertebrae of which the upper two are cervical, nine complete and two incomplete ribs, one lateral half of the sternum, all the elements of the limb and girdle skeleton.

, The vertebrae are represented by their bodies, and continuous with these are the neural arches of the right side; cartilaginous continuity around the notochord exists between the bodies. They form a markedly arched series, the dorsal convexity being so great as to bring the two upper ones each rather ventral to the succeeding member of the series than on top of it; these two cervical vertebrae have procoelous bodies of approximately tetrahedral form, apex directed caudo-ventrally. The neural arches, imbricated above and in linear series below, show small lateral projections at their dorsal extremities representing demispines; the seventh cervical vertebra shows a separate chondral element, its costal process, which is in close articulation with the body.


Fig. 1. Wax-plate reconstruction from human embryo 20 mm. greatest length. Magnification in figure about x 8'5.


The disproportionate length of the ribs and the approximately horizontal ‘position each occupies give to . the whole thoracic skeleton an appearance of marked inspiration. In general the cross-section of each rib is circular, but in front there is dorso-ventral flattening, whilst behind the flattening is from above downwards; the anterior extremities of ribs I. to V. articulate with a delicate sternal bar of cartilage which merges above partly in the cellular nonchondral interclavicular mass; VI. and VII. meet and support each other caudal to the other extremity of this bar ; all turn slightly dorsally, and I. to V. then acutely caudally in contact with the sternal bar. Like VI. and VII., VIII. IX. X. and XI. bend forward and so aredisposed as in the adult.


The clavicle is represented in its inner four-‘fifths by a very stout bar prolonged as to its outerfifth in the form of a flattened plate by bevelling at the expense of its costal aspect. The curve of the lateral part of the adult bone is practically absent. The cellular, constitution can be well seen in fig. 6; it is made up of two ossific centres on the point of coalescence within a matrix of young cartilage cells, the whole being surrounded by a very dense cellular periosteum; this last is prolonged into (1) a cellular mass surrounding the tip of the acromion, (2) a similar mass at the opposite end, the inter-clavicle, and (3) a" tract or band connecting behind the coracoid with the pre-scapula in which there is an appearance of early chondrification. The wedge of cartilage described by Professor Fawcett and assumed by him to be associated with the formation of the deltoid tubercle is well shown in fig. 6. In this figure the deltoid is not associated with it.


fiG. 2. Wax-plate reconstruction from human embryo 20 mm. Schematic representation of scapula and limb skeleton. Magnification in figure x 7'14.


The scapula is as yet incompletely merged with the coracoid, as indicated by the Width of the scapular notch and by a line of division “across the glenoid cavity rather below its middle. The blade is irregularly diamond-shaped; its upper limit lies opposite the caudal extremity of the body of the sixth cervical vertebra, and its surfaces are parasagittal.


The coracoid is a bulbous mass of cartilage joined with the scapula by a narrow neck and having a short cornuate process projecting upwards above the greater tuberosity of the humerus and a long one directed caudoventrally in the neighbourhood of the lesser tuberosity, considerably below the clavicle.


The acromion is a delicate bar showing an approximately right angle bend just above its root and a gentle curve beyond that to its tip, which projects slightly beyond the lateral extremity of the clavicle. Its root is immediately behind the edge of the scapular part of the glenoid cavity.

fiG. 3. Wax-plate reconstruction from human embryo about 30 mm. greatest length. Magnification about x 8'5. Ossific plate shaded.


There is complete absence of the spine, but, on the other hand, there is present a distinct supraspinous element (which for reasons which will appear I will call the “ prescapula”), separated by a slight interval. near the middle of its length from the main part of the blade or “ postscapula ” and by a junctional zone dorsally to this. This prescapula is inclined at a slight angle to and occupies a more medial plane than the postscapula, as in fig. 5; a prominent ridge which lies on the superficial surface of the post-scapula, caudal to the interval between the two elements of the blade, indicates the future basis of support for the spine. By reason of this arrangement there exist two notches in this region, one which for my present purpose may be called coraco-prescapular, and becomes the future incisura scapularis, and the other which I will call acromio-postscapular, a temporary feature later filled up by the growth of the spine. Between these two notches is the narrow area of origin of the supraspinatus muscle which occludes on one aspect the interval between the two parts of the blade.


The roots of the acromion and coracoid, and most markedly that of the prescapula, are invested by a thick layer of cells which surrounds the origin of supraspinatus and forms the scapular extremity of the previously mentioned band or cellular condensation which reaches behind the main mass of the coracoid to be continuous" with the periosteum of the outer segment of the clavicle (fig. 6).


fiG. 4. Wax-plate reconstruction from human embryo about 30 mm. Schematic representation of scapula and limb skeleton. Magnification about x 6.


The humerus has a very remarkable shape. The shaft is bent outwards and forwards so as to form a salient angle opposite the deltoid insertion; its proximal half is arched outwards and its distal half backwards. Neither extremity in its relation to the axis of the shaft occupies a position corresponding to that of the adult bone; the proximal end is rotated somewhat outwards, and its articular surface is divided by a groove into two flattened condyles corresponding with the coracoid and scapular segments to which it is applied; the distal end occupies a plane such as might result from a great exaggeration of that angle between the axis of the trochlea and the long axis of the shaft which is characteristic of the adult. By reason of this the inner lip of the trochlea forms the distal extremity of the humerus, and the capitulum lies on the lateral aspect at a higher level. A delicate outgrowth from the perichondrium of the shaft near its lower end ventro-lateral to the median nerve indicates the position of the entepicondylic spine (fig. 7).


What has been said of the distal articular surfaces of the humerus conveys equally the relative position of the contiguous extremities of the radius and ulna. These two cartilages lie parallel, one above the other, but not quite in the same plane, owing to what may be ‘described as a very slight degree of pronation. There is present between their distal ends an independent cartilaginous nodule embedded in a thickly crowded mass of cells. This may represent the intermedium.



fiG. 5. Coronal section, human mbryo about 30 mm. Prescapa and postscapula, ossifying pine of scapula and trapezio-deltoid intersection.


Of the carpal cartilages those on the postaxial side are far in advance of those on the pre-axial side of the wrist; the same is true of the metacarpals and phalanges, the three digits of the ulnar side being almost equal in length and slightly longer than the index. End plates to the terminal phalanges are just recognisable by their dark staining and plexiform character. A Contribution to the Embryology of the Fore-Limb Skeleton 361

Model of Fore-quarter Skeleton of 30 mm. Human Fcetus (figs. 3 and 4;).

This reconstruction shows ten half-vertebrae, of which three are cervical, four complete, and three incomplete costal arches, the manubrium sterni, and representatives of three sternebrae and all the elements of the limbgirdle and free limb.

The position of the vertebrae has altered owing to the decrease of the spinal curve, and the demispines on the extremities of the neural arches are now more marked. The ribs are now much more slender, except dorsally, where they are very massive and show commencing angulation.


fiG. 6. —Horizontal section through shoulder of 20-mm. embryo.

sc., scapula; Acr., acromion; H., humerus; Co., coracoid; CL, clavicle; M., supraspinatus; and P., prescapulo-clavicular band shown attached dorsally where scapula is covered by thick cellular layer.


The manubrial cartilage is pierced by a small hole, and there is a median cleft in the third sternebra.

The clavicle has developed rapidly, and has now almost the adult form with two curvatures; the outer extremity is, however, not so flattened as in the adult.


The scapula reaches headwards to the level of the caudal border of the seventh cervical vertebra; its diamond shape is still preserved, but the length of that border which runs from the coracoid to the upper angle has increased disproportionately; it follows that T the “ prescapular ” bar is greatly increased‘ in size, the slit separating it from the postscapula has lengthened, and there is- quite a marked groove indicating the boundary between the two elements and extending from the slit to the dorsal border, which it notches. The growth of the prescapula’ has greatlyexceeded that of the postscapula in the 20-30 mm. period, and it now bears a greater proportion to the whole blade than does the resulting supraspinous part of the blade in the adult.

FIG. 7. Horisontal section, human embryo 20 mm., to show : H., humerus ; 1%., radius in cartilaginous continuity; Med., median nerve with entepicondylic process of perichondrium on its lateral "aspect (*).


The coracoid is little changed, being only rather smaller relatively. The glcnoid surface is now concave and undivided; it seems to have increased relatively in its lower blade part. The acromion has grown considerably and become flattened and spatula-like, so that the acromial angle of the. adult. is now recognisable. The tip of the process projects considerably ventral to the outer end of the clavicle. The right-angle bend near the root described in the previous stage is now a sharp projecting elbow or spur of cartilage connecting with a tract of young, actively growing cells which passes backwards over the dorsum scapulae, under cover of the small-celled fibrous intersection between trapezius and deltoid, nearly to the vertebral border. This tract represents the developing spine, and in it, especially . near. the L acromial elbow, ossification is well advanced (fig._.8). The ossifying region is shaded in the figures of the model, and it can be seen to extend into a projection at the scapular notch, over the edge of which it is continued on to the medial surface of the blade. The cells in which the ossification takes place are derived from the mass which in the 20-mm. stage clothed the roots of the postscapula, coracoid, and acromion.


fiG. 8.—Coronal section, human embryo 30 mm. Shows elbow of acromion and ossification of spine (*).


The humerus is constricted in the region of spreading ossification, and is gently curved convex backwards. The two curvatures seen in the earlier stage are much less prominent in this later one owing to the great increase in length of the humerus, but both are easily identifiable still.


The upper end is now only slightly out-turned as compared with that of the adult bone, and the lower end has assumed, in the inclination of its axis to that of the shaft, a position intermediate between that in the earlier model and that representing the average of the two sexes in adult bones.


The radius and ulna likewise show constrictions in the ossifying zones. They are now very decidedly crossed. The ulnar styloid seems to be prolonged into the chondrifying discus articularis, and the same is true of the ulnar side of the lower extremity of the radius: between the two prolongations is a dense, unchondrified cell-mass. The contrast_ between this condition and that described for the 20-mm. stage is remarkable.


fiG. 9. Corona1 section, human embryo 30 mm. 0., centrale continuous through faintly staining zone with N., navicular.

The caxr-pal elements, especially those of the distal row, are well forward in development, and there is visible, both on the palmar and dprsal aspects of the wrist, a distinct centrale; on that side it lies between navicular, lunar, and trapezoid, and on this between navicular, capitatum, and trapezoid; its surface isolation does not correspond with the conditions in the depth of the articulation, where it is continuous, through a faintly staining transitional zone, with the navicular (fig. 9). The navicular is in only narrow contact with the trapezium, which seems isolated at the radial end of-the distal row and is slightly smaller than the trapezoid still.


The metacarpals and phalanges of the free digits are so disposed as to suggest that the hand is grasping a globe of small diameter. The end plates of the terminal phalanges are very broad.


Comparative

In discussing the features of the models described, the opportunity of reference to other human embryos in the collection at the London Hospital will be made use of. These embryos comprise 8-mm., 10—mm., l5.5-mm.,

24°5-mm., and 25-mm. stages, the measurements being in all cases those of greatest length. i _

The Vertebrae

The position and the curious form of the cervical vertebrae in Model I. led me to seek in earlier stages for an explanation of the pointed caudal projection of their bodies. It is only in the cervical vertebrae that this condition is very ma_rked,.and at first it was thought to be purely a positional moulding. Naturally shape and position are related features in ontogeny, a fact which in this instance is confirmed by the further observation that a much less and rapidly diminishing degree of- the same moulding is visible in the upper thoracic bodies. Still, it seemed only reasonable to expect that the shape of the cervical and upper thoracic bodies in the adult, with their prominent ventro-caudal lips, would require for its production something more than a process of purely adaptive growth of the scleroblastema of what may be called the typical centrum. It remains to explain the two correlated features by means of some material organic addition to these vertebrae during their development; such an organic addition is provided for in the 10-mm. stage when there is present connecting the costal elements of all the upper vertebrae a hypochordal bar of condensed cellular tissue (fig. 10) into which the chondrification of the body can extend in a caudo-ventral direction. This extension will be facilitated by the positional relations of the upper vertebrae, which here form a more sharply curved arch than those lower in the series, where the hypochordal element is less easily identifiable. Lewis, in touching upon the hypochordal element, limits it to the upper three cervical vertebrae and connects it, not with the costal, but with the neural arches. Bardeen notes its presence as low as the thoracic region.



fiG. 10. Human embryo 10 mm. Trans. section costo-hypochordal part of vertebral blastema shown stretching between the ventro-lateral myotome buds in front of chords.




The Ribs

Apart from the excessive length of the ribs in relation to their average cross-section, the curve of the costal arches and the shape of the thoracic cavity resulting are noteworthy, since, in both models, the proportion between the depth and breadth of this is reversed as compared with the adult form; further, the cylindrical form of the earlier stage is seen to be transformed into a truncated cone in the later, the profile view of which shows it to be much blunter than after completion of its. full growth and expansion. In Model I. the ventral ends of the ribs are free, with the exception of the first, which is fused with the sternal bar, whilst the second, third, fourth, and fifth turn caudally alongside it, being accommodated in fossae on its lateral aspect; in Model II. these have fused with the side of the sternum. The cartilaginous sternal bar ends, in the 20-mm. stage, opposite thelfifth rib, and the ventral extremities of the lower ribs turn headwards, the sixth and seventh ending in a condensed blastema continuous with the cartilaginous sternum. It would thus appear that the thoracic skeleton is furthest advanced in development at its inlet, and that the fusion between rib and sternal cartilages is a secondary process, like the fusion of the sternebral halves, as seen occurring in the third body sternebra of the 30-mm. stage. The use of the term “sternebra” in blastemal and cartilaginous stages is of course unjustifiable, but it has been employed for convenience sake to designate those parts of the continuous bar or bars which correspond to the bony segments of later stages.


The Clavicle

The form of the clavicle in Model I. is very striking by reason of the absence of that curvature which characterises its outer segment in Model II. and in the adult. In the 10-mm. stage, which may be taken as the equivalent of that, '£.e. 106 mm., described by Lewis, the blastematous clavicle extends inwards only one-third of the distance to the ventral end of the first rib, which it reaches in the 15°5-mm. stage. Arrived at this stage in its growth, the clavicle is therefore represented only by that part which, if form be any criterion, is the equivalent, in the adult, of its inner two-thirds at most; at this stage it seems to halt until a short time before that represented in Model I. ; then begins a further and distinct stage in growth coincident with the onset of ossification, one in which the lateral third of the clavicle of the adult is evolved from the cellular mass at the distal end (fig. 11). In this way the clavicle achieves its full development, arriving at the condition seen in Model II. The striking difference in the two stages of the development of a bone whose two parts are just as strikingly different in the adult, separated as those stages are by a considerable period of time, seems to warrant that any theory of the growth of the clavicle should take full cognisance of the causal facts that in the first stage the growth is axipetal, in the second, axifugal. It may be contended that the axifugal growth of the outer segment here emphasised is undeserving of emphasis, since it is equalled by contemporary axipetal growth of the inner segment; but it must be remembered, on the contrary, that the proportionate increase of the two growing ends differs widely and remains in favour of the outer, otherwise no such change in shape as occurs between that in Model I. and that in Model II. would take place.


fiG. 11. Horizontal section, human embryo 155 mm.

01. clavicle continuous laterally with suprahumeral cell mass (S.H.M.) ; 15r., prescapula; Sc., postscapula; Acr., acromion; 0.H., omohyoid.


The Scapula

The most striking features of the growth of the scapula, as brought out by the two models, are the development of the supraspinous portion, of the blade and the late appearance and mode of origin of the spine. The partial separation of the growing cartilage which represents the supraspinous part of the blade, to which the name prescapula has been given, especially excites curiosity. This separation is first fully recognisable in the 15°5-mm. embryo (fig. 11), and reaches its greatest differentiation in that represented by Model II. ; it is the more remarkable in that the slit seen in the two models between pre- and postscapula is occupied only by cells of the limiting membranes or perichondria of the two parts (fig. 5), and is not a passage for vessels or nerve filaments. For this reason it is to be considered a truly morphological separation, and not merely a casual fenestration, such as is a noticeable feature of the cartilages of certain amphibian and reptilian shoulder girdles. It is further especially to be remarked that the prescapular segment is fully continuous with the rest of the blade laterally, where it bounds the scapular notch, and that, at its other extremity, it is marked off from the blade in both models by a distinct groove and projects somewhat from the vertebral border, where it forms a part of this; in the former situation also it has a decided ventral projection clothed by a distinct cell-mass, among the surface layers of which the fibres of origin of supraspinatus are interspersed. A comparable condition. is found in the scapula of the dolphin, Delphinus delphis (fig. 12 (III.)), a condition made the more noteworthy by the absence of anything (resembling a true acromion process. In the toothed whale, on the other hand, an acromion process is seemingly present, but the prescapular equivalent is absent to all appearances (fig. 12 (I.)), whilst in Mesoplodon Grayii a condition is present which can be regarded as an intermediate stage between the two; in it, to adopt the accepted terminology, the acromium is bent backwards into a prescapular position, without, however, becoming continuous with the blade at its vertebral extremity (fig. 12 (II.)). Here, seemingly, are three stages in the formation of a prescapular element out of what has been previously considered an acromion process—-an assumption which, in the absence of the clavicle and the scapular spine among Cetacea must, for the moment, remain a doubtful quantity. There is, then, in the development of the human scapula an element, the true morphological importance of which has hitherto been disregarded, and which I have called the prescapula, whilst in the scapula of the adult dolphin a similar element is separable which, in its turn, is to be compared with the so—called acromion of Mesoplodon Grayii and of the toothed whale. Turning to the development of the spine of the scapula, we find that appearances indicate an origin for it in a cellular proliferation connecting with the elbow or spur of the developing acromion process (as distinct from the adult acromial angle); this undergoes a precocious ossification (fig. 8) as it spreads dorsally under the trapezius-deltoid intersection from the region of the scapular notch. The nature of the cells is, from their appearance alone, not easy to discern, but such characteristics as they


fiG. 12.—I., Scapula of Physeter Macrocephalus ; II., Scapula. of Illesoplodon Grayii; IIl., Scapula of Delphinus delphis.

possess, coupled with their secondary continuity with the fully differentiated cartilage of the acromial elbow, places them as derivatives of cartilage cells. Perhaps the most striking fact brought out by the second model is the formation of a bony dorsal boundary to the scapular notch through the agency of cells which in the 30-mm. stage are continuous with those ossifying under the acromion, and which are only represented in the 20-mm. stage by the mass lying most thickly at the root of the prescapula. The position and relations of this cellular proliferation are very suggestive, especially in view of the ossific process which takes place in it so early after its assumption of rapid growth. firstly, it overlies the junctional zone between coracoid and scapula; secondly, it lies at the dorsal extremity of a band of thickly crowded cells which passes medial to the coracoid (figs. 6 and 11) to divide into three well-marked strands merging with the periosteal layer of the outer segment of the clavicle; thirdly, this connexion is identifiable in the 15°5-mm. embryo as a dense strand forming the mesial boundary of a cell-mass which includes more laterally the prechondral representatives of acromion and clavicle, the middle of which is less condensed than its mesial and lateral margins. The mesial margin is well seen in fig. 11, and can be traced dorsally to the nucleus of chondrification representing the prescapular element and ventrally to the clavicle, whilst the middle third of it gives origin to the omohyoid, just lateral to the subclavian vein. The ossification of the scapula commencing at a junctional zone is remarkable as a parallel phenomenon to that described by Professor Fawcett in the ossification of the clavicle ; closer examination may show even greater resemblance in the details of the process; whilst further, in view of the importance of junctional zones as centres of growth, brought out by the work of Professor Geddes on the Vertebrate Limb, an even more widely generalised significance may be attributable to this fact in the growth of the scapula. The cell strand connecting prescapula and clavicle is so far differentiated in fig. 6 that it represents the typical position of those ligamentous fibres which in many adults pass along the upper part of the conoid ligament into the transverse ligament; in this figure the omohyoid origin is not connected with these fibres, a factwhich is referable to the dorsal migration of the origin towards the scapula.


The explanation of the observed facts bases itself mainly upon the presence of the large cell-mass in the upper shoulder region in the 15.5-mm. stage. This mass is continuous with the acromion laterally, with the prescapula dorsally, and with the outer extremity of the chondrifying clavicular bar ventrally. It is in this mass that the specialisation of the clavicle-acromion arch so closely related to the evolution of a freely movable shoulder-joint must occur, and, since this specialisation is especially important in man, the steps of its development may be expected to abound in matter for comparison with the vertebrate girdles down even to those of thereptilia. Taking into consideration the variety of forms among the mammalia assumed by these portions of the skeleton, the cell-masses which are their precursors in ontogeny must be regarded as possessing a remarkable degree of lability, and, for this very reason, as being likely to preserve in the stages of their early development certain main features of their common and very early precursors in phylogeny. The earliest form of the human shoulder girdle, as figured by Lewis for a 10'5-mm. embryo, is a rectangular mass of crowded cells representing a scapula and situated high in the cervical region, to all appearance a plate-like headward prolongation of the axial condensation of the free limb.‘ In it, again, according to Lewis’s figure, there is a shallow furrow which may or may not be the first indication of the slit found in the cartilaginous scapula of later stages; if it be not, I am inclined strongly to the view that this rectangular mass of cells represents rather the prescapula of the cartilage stages than the postscapula, and from its caudo-lateral angle the postscapula may grow out; this View would be little more than speculation if it were not that the prescapula of a 15'5-mm. embryo shows a more advanced stage of differentiation than does the rest of the scapula. This is, however, a point on which the material at my disposal does not provide any further evidence of conclusive value, and which is of minor importance for the further development of the deductions made from the other facts observed in order to elucidate the connexion of prescapula and clavicle. This connexion has been fully described and figured, as has also the evolution of the so-called acromion in the Cetacea, through which it becomes converted in Delphvlmos delphis into a remarkable semblance of the human cartilaginous prescapula; and it only remains, in the first place, to emphasise that the connexion of the human prescapula with the clavicle is made at the mesial extremity of the lateral segment of the clavicle, and, in the second place, to postulate that the Cetacean so-called acromion connected with the clavicle of Cetacean progenitors, in order to reach the conclusion that the labile substance of the shoulder region can produce under evolution a mesial and a lateral arch ; that one prescapulo-palaeoclavicular — possibly identifiable in Cetacean ontogeny—this one acromio-neoclavicular in nature. In support of this conclusion and of the one postulate furthering it are a number of indisputable facts :—

1. That the ingrowth of the clavicle in stages from 10 mm. onwards occurs, not from the region of the tip of the acromion (sensu stricto as here applied), but from the ventral extremity of the strand of cells which forms the mesial limit of the suprahumeral arch mass, the outer periphery of which will later give rise to the outer segment of the clavicle ventrally and to the acromion dorsally. This is beautifully demonstrated in fig. 11, 15.5, which, it will be remembered, comes from a stage 155 mm., in which the clavicle has reached to the ventral extremity of the first rib.

2. That the variations in origin of the posterior belly of the omohyoid muscle almost never follow the lateral or acromio-clavicular, but nearly always the mesial or prescapulo-precoracoid arch.

3. That in the two-toed sloth, Uholwpus H0fi"ma'n/n/£7}, the prescapula and acromion are synostosed, and with the complete arch thus constituted from the periphery of the suprahumeral mass the clavicle articulates, which clavicle, to judge by its sole curvature, a ventral convexity, represents only the precoracoid portion of that bone (fig. 13). By reason of the primitive scale of general mammalian organisation found in the Edentata, and also by reason of the habits of the sloth, this fact supports both the conclusion I have come to and the postulate regarding the Cetacean clavicle necessary to its validity in the comparative sense.


fiG. 13.—Scapula. Clavicle of two-toed sloth, Cholaepus Hofimannii, showing acromio-prescapular arch.


To summarise, the shoulder arch in man shows in its development a fair epitome of the phylogenetic steps in its specialisation from a type which would be fairly represented by the shoulder girdle of the toothed whale, did this possess a clavicle, a type extant in both Ornithorhynchus and Echidna. With advancing specialisation the original arch becomes converted to other uses; the primitive acromion becomes the supraspinous plate, and a new acromion is evolved, whose earliest trace is possibly identifiable in Echidna and whose intermediate form is exemplified in the sloth, this new acromion having a wider sweep and necessitating an addition to the primitive clavicle. Meanwhile the intermediate portion of the original arch merges in, or specialises as the transverse and part of the conoid ligaments of man.


This theory of the development of two arches in the mammalian shoulder girdle deserves a reference to the conditions in lower vertebrates. In the reptiles the so-called clavicle often reaches far on to the dorsum of the scapula, whilst as yet no acromion can be said to exist, indeed the dorsal portion of the clavicle occupies a position on the reptilian scapula which is only comparable with that of the scapular spine in man, or in other mammals in which a truly homologous spine is developed. Such an extension of the clavicle may reasonably be supposed, I think, to follow the line of our prescapulo-precoracoid arch, and thus leads on to the hypothesis that that cellular covering of the root of the prescapula (fig. 6) which ossifies to form a bony spicule, the definitive dorsal edge of the scapular notch, and which further extends to the root of the acromion and under the trapeziusdeltoid intersection to form the spine of the scapula, ossifying as it goes, is the homologue of part’ of the original reptilian clavicle. This is only,‘ however, a hypothesis, but it has so many favourable features that it seems worthy of the more exhaustive examination of embryonic and comparative material necessary for its proof and acceptance as a well-grounded theory.


The secondary coalescence of spine and acromion would well account for the proliferation which forms a spur on the acromial elbow in Model II., and a similar but more marked outgrowth in this junctional zone doubtless results in the formation of a metacromion as found in certain rodents, and markedly in the elephant. For particularly directing my attention to this structure, I am indebted to Professor Wright.


The humerus in the forms in which it appears in Models I. and II. is a very interesting object. Its curvatures are striking, and the torsion and angulation of its upper and lower extremities are brought out in a way which previously figured reconstructions have failed to indicate. This is to be attributed to the method I have adopted of drawing only the limits of the cartilage and avoiding the perichondrium, at stages in development when the differentiation of that tissue has reached or slightly overstepped its “ optimum.” The seeming contrast between the two forms is dispelled on close examination of the second model, and the change is attributable only to the enormously increased length of the shaft and its relatively decreased girth in the region of the primary ossification. Distortions of the shafts of long bones have been noted in embryo by Holl, Schomberg, and others, and attributed to disproportionately rapid growth in length; these are especially marked in hardened specimens and are therefore probably artificial. Of such artificiality I see no trace in the developing humerus, either in Lewis’s figures or my own material, and I consider that both the described curvatures of the shaft are a phenomenon of correlated growth during development of humerus and musculo-spiral nerve in the first place, somewhat exaggerated by the shortness of the shaft and the form of the unspecialised articular ends, and, possibly, later, by the related deltoid insertion in the second place. That the spiral groove of the adult humerus is so much broader than the structures lying in it is merely an indication of the early date of its production, when the girth of the nerve relative to the length of the bone was much greater and separated the origin of the two humeral heads of the triceps at the time when they were acquiring a firm attachment to the ossifying tissue‘ of the shaft; for muscles never attach themselves to cartilage, but only to the perichondrial membrane, which is later incorporated with the periphery of the bone. The causation of the spiral groove of the humerus has no relation to the torsions about to be considered.


The changes of torsion and angulation of the articular ends which take place between the 20-mm. and the 30-mm. stages are attributable in the case of the upper extremity to the pre- and postnatal alteration of position of the scapula, relative both to the axis of the humerus and to the curve of the chest wall; in the one case the change is an approach of the axillary border of the scapula to the humerus, and in the other it is a change due to the increase in length and curvature of the ribs, causing the scapula to migrate towards the vertebrae and the head of the humerus to rotate inwards to accommodate itself to the altered aspect of the glenoid. The alteration in the inclination of the distal articular surfaces to the axis of the shaft is productive of the specialisation of the elbow-joint for pronation and supination of the forearm bones. Lewis, in Keibel and Mallis T eastbook, p. 380, states that in an 11-mm. embryo, the forearm is midway between pronation and supination. This statement is incorrect, in principle and in detail, for, almost up to the 20-mm. stage, pronation and supination as movements or as postures are out of the question, owing to the form of the distal extremity of the humerus, the details of the skeleton showing that the forearm bones are parallel T and the hand apparently fully supine if the plane of the hand be projected upon the plane of the lower end of the humerus; the right-angled elbow, parallel forearm bones, and paddlepostured hand make an exact reproduction of the palaeo-reptilian fore-limb. The sex difference which is characteristic of the limb in the adult would seem to rest upon a less degree of specialisation of the upper extremity in the female than in the male, resulting in the greater “ carrying angle ” of the female. The correlation (if it be one) of this inferior grade of specialisation in the female upper limb With a higher grade of specialisation in the female pelvis is an interesting paradox.


The radius and ulna have been almost sufficiently discussed in connexion with the distal extremity of the humerus; it only remains to add that, if the inclination of forearm to arm be a true sex characteristic, the differential torsion of the two extremities of the ulna and the relative aspects of the articular surfaces of the radius should, if made capable of convenient measurement, prove a valuable means for determination of sex in osteology and anthropology.

The Carpus and Hand

The presence of a centrale in Model II. and the mode of its inclusion are not in agreement with the observations of Graefenberg. Graefenberg’s material seemingly did not include a stage as early as that of Model I., in which no centrale is to be found, for he states that it is among those carpal elements earliest differentiated, and, further, that it is probably broken up by the appearance of the lunar, and finally disappears, leaving no trace. As against these statements I have to place the facts that the centrale is unrepresented in my 20-mm. stage, yet in my 30-mm. stage it is visible on both Ventral and dorsal aspects of the carpus, where it is entirely separated from all other elements by a distinct perichondrium, and that in the depth of the massed elements it is structurally continuous with the naviculare through a faintly staining cartilaginous layer. (fig. 9). This further confirms Owen’s and MiVart’s views on the fate of the centrale, whilst opposing those of Rosenberg and Thilenius, and partially also those of Leboucq. The isolation of the trapezium on the radial side of the carpus has been noted in description of Model I.; its position confirms the observation of Hagen, one which Graefenberg professes to be unable to understand, in that it is practically confined to the ventral aspect of the wrist.


The question of the relation of intermedium and discus articularis cannot be fully entered into here because of the limited amount of material under discussion, but the appearance of a separate cartilaginous nodule in the 20-mm. stage, embedded in a mass of thickly crowded cells, and the absence of such an element in the later stage, which shows chondrification of the cell-mass in continuity, on the one side, with the ulnar styloid, and, on the other, with the inner edge of the extremity of the radius, both seem to indicate early differentiation of an intermedium, followed by its disappearance and replacement by the discus.

Summary Or Conclusions

Technical.

1. The first and perhaps the most critical matter, in its bearing upon the technical results of this work, is the imperative necessity, in preparing a reconstruction of the cartilaginous skeleton, to adhere slavishly, in the drawings made, to the periphery of the fully differentiated cartilage and to exclude all the surrounding transitional perichondrial tissue.

2. The second conclusion of a technical kind follows from the first, and is, that reconstructions of the developing skeleton, at stages earlier than the 376 Mr N. C. Rutherford

“optimum” of cartilaginous development, must necessarily be ambiguous since the zones of transition are much wider and more difficult of limitation, whilst the shape of the growing chondral nuclei signifies nothing of a more than ontogenetic importance. It is not desired to convey by this that the form of the condensed blastemal skeleton suffers under the same disability for comparative purposes, quite the contrary; the blastematous stage, also, has an “ optimum” development, only one which is more diflicult to assess than is that of the cartilage; it probably lies in or around the immediately prechondral period. It is further desirable to emphasise that nothing in these conclusions can apply to elements which manifest anything in the nature of direct ossification, that is to say, which, among vertebrates, may ossify otherwise than through the intermediation of cartilage; for example, a drawing and reconstruction of such an element as the chondral clavicle will convey nothing of value, because the chondrification of the clavicle never reaches an “ optimum ” in the accepted sense.

3. The blastema stage of the shoulder skeleton represents in its massive cell agglomeration two arches, one mesial, consisting of the precursors of the supraspinous portion of the scapula and the cell-strand connecting this with the clavicle at the junction of its sternal and acromial segments, and one lateral, representing the acromion and acromial segment of the clavicle, both having comparable though simpler bony representatives in the Edentate Oholcvpus Hofimannii. In the absence of the clavicle of their progenitors the Cetacea show a conversion of the dorsal pillar of the medial arch into prescapula.

4. The supraspinous portion of the scapula may possibly be the original scapula of phylogeny; it certainly is a separate morphological constituent of the scapula, as evidenced by the course of its development in man and by the various forms of its equivalent in the Cetaceans cited.

5. The formation and precocious ossification of the spine of the scapula begins in cells which, appearing at the root of the prescapula, grow on to the dorsum along the coraco-scapular junction and under the trapeziusdeltoid intersection, cells which are therefore intimately related to the mesial arch, and may be, like this, representative of the reptilian clavicle. Spine and acromion are joined up through the intermediation of these cells, and the junctional proliferation may be so marked as to result, under ossification, in the production of a metacromion, as in certain rodents, and markedly in the elephant.

6. The spiral groove of the humerus is due to the impress of the musculo-spiral nerve and is not due to torsion, which, however, is not absent during the growth of the cartilage, but affects only the proximal end.

7. The specialisation of the distal articular surfaces of the humerus takes place Within the stages examined, and its degree is different in the two sexes.

8. The carpal centrale is most fully developed in cartilage about the “optimum” period for the other carpal cartilages. It fuses with the navicular.

9. The intermedium is present in the 20-mm. stage, and disappears before the 30-mm. stage to make way for the chondrification of the articular disc from its ulnar and radial extremities.

Acknowledgments

I desire to record my thanks to Professor W. Wright for the kindly interest With Which he has followed the completion of this Work; to Professor A. C. Geddes, firstly, for the use of apparatus for reconstruction, Which was his private property, and, secondly, for the advice Which, when in any difficulty, I could always fall back upon with benefit.

The publication has been carried out with the help of a grant from the Research Fund of the London Hospital Medical College; the drawings are

by Mr W. Thornton Shiells; in the photography I have been much assisted by Mr T. Collyer Summers.

Bibliography of References

Most of the papers referred to are quoted in the Bibliography on pp. 391-397, vol. i., of the Manual of Human Embryology, by Keibel and Mall. In addition are the following :—

FAWCETT, E., “The Development and Ossification of the Human Clavicle,” Journ. of Anat. and Phys., vol. xlvii. p. 225.

GEDDES, A. (3., “‘ The Origin of the Vertebrate Limb,” Journ. of Anal. and Phys., vol. xlvi. p. 350.


Cite this page: Hill, M.A. (2024, March 29) Embryology Paper - A contribution to the embryology of the fore-limb. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_A_contribution_to_the_embryology_of_the_fore-limb

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