Paper - The development of the arm in man (1902)
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- 1 The Development of the Arm in Man
- 1.1 Introduction
- 1.2 Part 1 Relation of the Myotomes to the Arm Bud
- 1.3 Embryo CLXIV
- 1.4 Embryo XII
- 1.5 Embryo LXXVI
- 1.6 Embryo LXXX
- 1.7 Embryo II
- 1.8 Summary
- 1.9 Part 2 The Differentiation of the Mesenchyma of the Arm Bud into musculae and skeletal elements, and the growth of the nerves
- 1.10 Embryo CLXIII
- 1.11 Embryo CIX
- 1.12 Embryo XLIII
- 1.13 Embryo XXII
- 1.14 Summary
- 1.15 References
- 1.16 Plates
The Development of the Arm in Man
Warren Harmon Lewis, M. D.
Instructor in Anatomy, The Anatomical Laboratory, Johns Hopkins University.
With 3 Plates and 14 Text-Figures.
The wandering of the trapezius and the latissimus dorsi and also of muscles in the ahdominal wall was noted by Dr. Mall several years ago. At his suggestion I undertook, in the spring of 1897, a more careful study of these and other changes in the development of the arm region in man. Similar studies were undertaken later by Dr. Bardeen on the leg and body wall. We have embodied many of the important points obtained from our studies in a joint article  which appeared in the first number of this journal, and of which this present article may be considered a continuation.
In the present paper I purpose to consider the origin of the tissue which fills the arm bud, the entrance of nerves into this tissue and its differentiation into skeleton, ligaments, muscle and tendon, and finally the growth and wandering of these structures until practically the adult conditions are present.
I wish here to express my most sincere thanks to Dr. Mall for his constant interest and many suggestions, and also for the use of the valuable embryological material in this laboratory.
The embryos studied, with the exception of the one belonging to Dr. Buxton, of Cornell University, are in the collection belonging to Dr. Mall. Most of those considered in this paper are tabulated on page 2, Vol. I, of this journal.
From the serial sections of embryos CLXIII, CIX, XLIII and XXII I have made reconstructions of the arm region after the Born method. The arm region in Plates III to IX in the paper by Bardeen and Lewis are drawn from these models, and are to be consulted in connection with the descriptions given in this article. Dr. Mall's embryos are stained in alum caraiine or alum cochineal.
Part 1 Relation of the Myotomes to the Arm Bud
Considerable study and perhaps even more theorizing has been done on the relation of the myotomes to the musculature of the limbs. The present state of our knowledge upon this subject is far from satisfactory, especially in the higher vertebrates. The great difficulty or impossibility in many cases of distinguishing between the cells at the ventral edge of the myotomes and those in the neighboring portion of the limb bud renders the problem very difficult. Experimental work, such as has been done by Byrnes, may lead to a clear understanding of the relations in the lower vertebrates. The majority of workers appear to have been able to trace myotomic processes into the limbs. Mollier â– * has shown in Selachians that myotome buds enter into the fin anlage or pectoral plate. From these buds are developed the muscles. From the mesoderm between the buds are developed the fin rays. Braus " also shows myotome buds going into the pelvic fins of Selachians. Dohrn * finds two buds from each myotome, an anterior and a posterior, entering the fin anlage, these he believes form the fin muscles. Balfour^ holds that the limb muscles in Elasmobranchii come from muscle plate buds. Harrison * has shown that in teleosts the pectoral fins are derived wholly from the somatopleure and that the myotomes take no part in the formation of these fins. Boyer^ believes elements from the peripheral layer of certain myotomes are contributed to the pectoral plate which comes from the somatopleure. Corning" believed in 1894 that the pectoral fins in teleosts received muscle-plate buds, but he has since come to the conclusion " that these fins in teleosts do not receive such buds, and agrees with Harrison that the myotomes take no part in the formation of the pectoral fims. Kaestner " was not able to show in Anura that the myotomes take any part in the formation of the limbs, though he believes they do at a very early period. Field " believes that the elements which form the muscle of the extremities in Amblystoma are separated at a very early age from the ventral part of the myotome. Byrnes " work, both her embryological and experimental studies, shows that " the myotome processes, as such, take no part in the formation of the limbs . . . The limbs are of somatopleuric origin, i. e., the muscle, cartilage, and connective tissue." Goette " believes that the limb muscles in Bombinator develop from the outer layer of the muscle plate. Van Bemmelen" believes that in the lizard the limb muscles are derived from the myotome buds. Mollier" finds cells from myotome buds go into the arm anlage in Lacerta niuralis. According to Patterson," the limbs of the chick are derived wholly from the somatopleure. He does not find muscle buds or homologous structures entering into the limbs. In a recent paper by Maj," the conclusion is reached that the myotomes do enter the limbs in the chick. He pictures the ventral end of the myotome entering the limb in company with the nerve and splitting into dorsal and ventral lamellae. Fischel '" believes that in birds and mammals myotome cells mix in the limb bud and give rise to the muscles. There is a diffuse entrance of cells from the myotomes but not of myotome buds. In a section of a human embryo of the fourth week he pictures these myotome cells as forming a peripheral layer around the arm bud and even extending into the somatopleure. The rest of the bud comes from the somatopleure. Kollmann '^ pictures in a very diagrammatic manner the downgrowth of the outer lamella of the muscle plate into the arm bud where it lies between the ectoderm and the mesenchymal core.
Mollier, Zur Entwickelune: der Selachierextremitaten, Anat. Anz., Vol. VII, 1893, p. .3.51. Die paarigen Extremitaten der Wirbelthiere, Anal Hefte, Bd. Ill, 1893.
5 Braus, Beitrage zur Entwi-ckeluno; der Muskulatur und des peripheren Nervensystem der Selachier, Morph. Jahr., Bd. XXVII, 1899, p. .501.
6 Dohrn, Studien zur Urgeschichte des Wirbelthier Korpers, VI, etc., Mittheil. aus der Zool. Station zu Neapel, Bd. V, 1884.
1 Balfour, Comp. Emb., 3nd. Ed., 1885.
8 Harrison, Die Entwickelung d. unpaaren und paaren Flosseu der Teleostier, Archiv f. Mikr. Anat., Bd. XLVI, Ileft 3, 1895.
9 Boyer, The mesoderm in Teleosts, etc., Bull. Museum Comp. Zool., Harvard Univ., Vol. XXIII, 1893.
10 Corning, Ueber die Ventralen Urwirbelknospen in der Brustflosse der Teleostier, Morph. Jahr., Bd. XXII, Heft 1, 1894.,
11 Corning, Ueber die Entwickelung der Zungen Musculatur bei Reptilien, Anat. Anz. (Gesellschaft) 1895.
12 aestner, Extremitaten- und Bauehmusculatur bei Auuren, Arcbiv f. Anat. und Phys. (Anat. Abtheil.), Hefte .5 und 6, 1893.
13 Field, Die Vornieren Kapsel, ventrale Musculatur und Extremitiitenanlagen bei den Amphibien, Anat. Anz., Bd. IX, No. 33, 1894.
14 Byrnes, Op. cit.
13 Goette, Die Entwickelungsgeschichte der Unke., 187.5.
16 Van Bemmelen, Ueber die Herkunf t der Zungen- und Extremitiitenmusculatur bei Eidechsen, Anat. Anz., Bd. IV, 1889.
17 Mollier, Die paarigen Extremitaten der Wirbelthiere. Anat. Hefte, Bd. Ill, Heft VIII; Bd. V, Heft XVI.
18 Patterson, On the fate of the muscle plate and the development of the spinal nerves in birds and mammals. Quart. Jour. Micr. Sci., Vol. XXVIII, 1887.
"Maj, Contribute alio studio dello sviluppo della musculatura negli arti. Osservazioni sur polio (Gallus domesticus), Dal Bollettino della Soc. Med.-Chir. di Pavia, 1901.
In the lower vertebrates it would appear therefore that the limb muscles may arise either from distinct buds of the myotome or they may arise independently of the myotomes from the somatopleure. In the higher vertebrates no distinct myotome buds have been traced into the limbs. Myotome cells are supposed by most observers to enter the limbs and take part in the formation of the muscles.
The question as to whether in man the muscles of the arm are derived from cells of the myotomes which have migrated into the arm bud at a very early period, I have not been able to determine satisfactorily. Neither am I convinced by the work of Pischel or Kollmann that the myotomes take such a part in the formation of the arm. Their pictures are quite unlike any of the conditions found in the human embryos which I have studied.
Early Stages of the Arm Bud
In Embryo CLXIV, 3.5 mm. in length, there are thirteen myotomes. No signs of an arm bud are present. The myotomes are sharply limited and do not give off any cells into the region where the arm bud is soon to sprout. Cells appear to be migrating from the myotome towards the chorda. The somatopleure, hov/ever, shows a proliferation of the cells lining the ccelom. This is very close to the place where the arm bud is soon to appear and lateral to the Wolffian duct and tubules. (See Fig. 1.)
5io Fischel, Zur Entwickelung der ventralen Rump- und Extremitiiteumusculatur der Vogel und Saugethiere, Morph. Jahr., Bd. XXIII, 1895.
21 Kollmann, Die Rumpfsegmente menschl. Embryonen von 13 bis 35 Urwirbel, Archiv f. Anat. und Pliys. (Anat. Abtbiel.), 1891.
Fig. 1. Cross section through the eighth myotome of embryo CLXIV. X 100 diameters.
Embryo XII, 2.1 mm. in length, has fourteen myotomes and is slightly older than CLXIV. The first definite signs of an arm bud are here noticed by a slight swelling ventrolateral to the myotomes in the lower cervical region. Its position is seen in Fig. 2. The origin of the cells which cause this swelling I am not able to determine, though there are suspicious looking processes from the myotomes. No spinal nerves are present.
Embryo LXXVI is 4.5 mm. in length and about three weeks old.
Between embryos XII and LXXVI there is quite a gap. There are 35 myotomes. The arm bud is quite large and filled with uniformly and closely packed cells whose nuclei take a deep stain with the alum carmine. A few thin-walled blood-vessels are scattered here and there. The base of the arm bud lies opposite the fifth cervical to the first thoracic intervertebral disks. The cells of the median lamella of the myotomes have been converted into muscle fibers. The myotomes are fairly well defined and do not show buds, or, so far as I can determine, migration of their cells into the arm bud. The general trend of the growing ventral end of the myotome is not out towards the arm bud, biit ventrally towards the ccelom. It will be seen in Fig. 3 that a considerable portion of the root of the arm lies close to the dorsal end of the ccelom and that a proliferation of cells from its lining might easily contribute to the arm tissue. The spinal nerves are not formed though a few anterior root fibers appear to pass directly lateral from the anterior horn. Most of them are lost in the surrounding mesenchyma, a few, however, appear to reach the group of muscle fibers on the median surface of the myotomes. This is an exceedingly important stage. The arm bud is filled with a peculiar closely packed mesenchyma which, so far as I am able to judge, is the same sort of tissue from which at a later stage the skeletal and muscular tissues differentiate. This tissue fills the arm before the nerves are developed, and if there are cells from the myotomes present they have migrated there without the nerve supply.
- Dr. Mall considers embryo CLXIV slightly older than embryo XII. The greater length of CLXIV he accounts for by a straightening of the body of the embryo through mechanical injury to the ovum. See Mall, On the development of the human diaphragm, The Johns Hop. Hosp. Bui., Vol. XII, 1901, p. 160.
Fig. 2. Cross section through the eighth cervical myotome of embryo Embryo XII. X 100 diameters.
Fig. 3. Cross section through the eighth cervical myotome of embryo LXXVI. X 50 diameters.
In Embryo LXXX, 5 mm. in length, the arm bud has increased considerably in size. The cells which fill it resemble those in LXXVI, but are more closely packed together and stain deeper. There is no differentiation of this mesenchyma. Thin-walled blood-vessels are numerous, the border vein (Eandvene of Hochstetter) is present. Numerous mitotic figures indicate that there is a rapid proliferation of the mesenchymal cells. The myotomes are fairly well defined, though in places the ventral end is not always sharp and the possibility of wandering of cells from it into the arm bud cannot be denied. The almost constant presence of several blood-vessels at the ventral end of the myotome would interfere somewhat with that process. The spinal nerves have grown out some distance from the cord, they however pass by the median side of the myotomes without sending branches into them. The distal ends of the nerves reach beyoud the myotomes. The lower four cervical and first dorsal end at the root of the arm. As will be seen in Fig. 4, this end of the nerve spreads out somewhat and is surrounded here as well as along its course by loose mesenchyma which is quite different from that in the arm bud, but like that which lies between the myotome and the aorta, and through which the nerve has pushed, probably carrying some of this tissue with it and before it. The first beginnings of the cervical and brachial plexuses are present in the form of anastomoses of the brush-like ends of the first cervical to the third thoracic. It is an interesting fact that at this stage the upper thoracic myotomes extend to a considerable distance ventral of the ventral union of the arm bud with the body wall. The tip of one of these thoracic myotomes is seen in Fig. 4. In the cervical region, on the contrary, the myotomes are much shorter and do not extend so far ventrally.
Fig. 4. Cross section through the eighth cervical myotome and nerve of embryo LXXX. X 50 diameters.
Fig. 5. Cross section through the eighth cervical myotome of embryo II. X 50 diameters.
In the Buxton embryo about the same conditions exist as in LXXX. Embryo Buxton is 5 mm. in length and about 25 days old. It was stained in haematoxylin and eosin, thus bringing out the muscle plates even better than with the alum carmine in which Dr. Mall's embryos were stained.
Embryo II is 7 mm. in length, and about four weeks old. It shows some advances over LXXX. The arm bud is filled with the closely packed mesenchyma similar to that seen in LXXVI and LXXX, with this important difference however that in the center of the mass the cells are somewhat more closely packed than at the periphery, and represent the first beginnings of differentiation in the arm. This probably represents the humerus. It will be seen from Fig. 5 that the peculiar tissue in the arm bud has spread some distance into the membrana reuniens. Here, as in the previous stages it is impossible to determine whether cells may not go from the myotomes into the arm bud. The nerves, as in LXXX, pass along the median side of the myotome without sending branches into the myotome or, so far as I can determine, taking a portion of the myotome along into the arm bud. They extend farther into the arm than in the preceding stage. The beginning of the cervical and brachial plexus is even more marked, and is formed by anastomoses of the brush-like ends of the first cervical to the second thoracic. The root of the arm lies at the level of sixth cervical to the second thoracic intervertebral discs.
The tissue from which the muscles, ligaments, tendons, and cartilages of the arm develop is present at a very early stage in the arm bud, probably by the beginning of the third week. No distinct myotome buds take part in the formation of this tissue. That cells from either or both myotomes and somatopleure enter into this early arm mesenchyma cannot be determined from the material at my disposal. If cells do migrate from the myotomes, they apparently do so independently of the nerves which are not present until the tissue is formed and fills the arm bud. The first beginnings of differentiation of this peculiar tissue which fills the arm bud occur durine; the fourth week.
Part 2 The Differentiation of the Mesenchyma of the Arm Bud into musculae and skeletal elements, and the growth of the nerves
The first indication of a differentiation of the mesenchyma of the arm bud occurs as we have seen in an embryo of about four weeks. In our next stage, embryo CLXIII, quite marked changes have taken place.
Embryo CLXIII is 9 mm, in length, and about four and one-half weeks old.
In order to gain a clear conception of the form and various relations of the structures in this embryo, I found it necessary to construct a model, and in order to do so it was necessary to draw sharp lines about the various structures when in reality there were no sharp limits. One mass often shading off into another, while the central portion of each was very distinct. Thus, in most places the skeletal core of the arm shades off into the surrounding premuscle tissue, or as in the region of the hand plate into the primitive condensed mesenchyma, filling the distal end of the arm bud. The same was often true of the various premuscle masses. The main portion of these are quite distinct, but they often shade off into each other and into the surrounding mesenchyma. We find in this embryo in the arm region that the premuscle masses most closely associated with the trunk are the farthest advanced, those connecting the arm and trunk next, and the least developed is the general arm pre-muscle sheath, especially its distal portion.
Fig. 6. Skeleton and nerves of the arm region in embryo CLXIII. X 40 diameters.
- I have given the name premuscle to various classes of condensed mesenchyma from which at a later period I believe muscle develops by histogenetic changes of the cells.
The Skeletal System
There is no cartilage at this stage. The skeleton is composed of condensed or closely packed mesenchyma which takes a deeper stain than the surrounding tissue.
The vertebral column consists in the arm region of the intervertebral discs, and their nenral processes which lie in the posterior third of each segment. Between the discs is a loose mesenchyma, the cells of which, as well as those in the disc, have a concentric an-angement about the chorda.
The ribs spring from the adjacent portions of the disc and neural process. A line of separation is visible. They take a ventrolateral direction into the body wall. The sixth and seventh cervical intervertebral discs have short rib-like processes.,
In the arm the exact limits of the skeletal strnctures cannot be determined as this central core which is easily recognized, shades off into the surrounding mesenchyma, which develops into muscle. The scapula is a quadrilateral mass at the level of the fourth and fifth cervical discs. There are no indications of coracoid, acromion or spinous processes. The scapula is continuous with the humerus, which is a cylindrical mass occupying the center of the proximal portion of the arm bud. Practically all of it lies at a level anterior to the first rib. At the level of the first rib the humerus is continuous with tlie ulna and radius. There is a slight flexion of the forearm. They are short and thick. The ulna is the larger and is more directly a continuation of the humerus. Partially surrormding the ulna and radius is a plexus of blood-vessels which helps to outline them. The continuation of this plexus is seen in Fig. 8. Both ulna and radius are continuous, with the very ill-defined mass of condensed tissue which lies in the center of the distal end of the arm bud. This rather thin plate composed of cells more closely packed together than those of the surrounding tissue, shows no signs of division into the various elements of the hand. I name it the hand plate.
The Muscular System
The muscle plates are fused into a continuous column. Indications of segmentation remain. This column lies close and lateral to the neural processes. In the cervical region it ends abruptly at the brachial plexus. In the costal region, however, it extends ventrally into the body wall, between, and partially surrounding the ribs. It ends ventrally beyond the tips of the ribs. The muscle plate system is easily distingnished from the surrounding tissues by its fibrillation.
Lateral to the muscle-plate system are ill-defined masses of condensed tissue without fibrillation, but from which muscles differentiate.
Lateral to the anterior six ribs lies the lateral premuscle mass. It occupies most of the space between the costal portion of the muscle-plate system and the integument. It shades off into the surrounding loose mesenchyma everywhere, but at the anterior end, at about the level of the first intercostal space, it splits into four divisions which pass anteriorlv.
Fig. 7. Outline of the arm region of embryo CLXIII from Plate III. Bardeen and Lewis, Vol. I, No. 1, this Journal. X 15 diameters.
The first or dorsal division lies lateral to the muscle-plate column, and extends to the level of the fifth cervical disc.
The second, third and fourth divisions correspond so closely with the position in which I find certain muscles in the next stage, and as they also have the same nerve supply as the muscles into which I believe they develop, that I have called them in order: The (2) levator scapulae and serratus anterior, the (3) latissimus dorsi and teres major, and the (4) pectoral premuscle masses.
The second division, the levator scapulce and serratus anterior premuscle mass, ventral to the first and opposite the ventral portion of the muscle-plate column is fairly well defined. It extends into the upper cervical region. It lies in a more median plane than the scapula, and at this stage is in no way attached to it.
The third division, the laUssimus dorsi and teres major premuscle mass, passes anteriorly along the dorsal side of the brachial plexus and becomes continuous with the arm premuscle sheath at the proximal portion of the humerus. The humeral end is thicker and broader, and continuous also with the arm premuscle sheath about the scapula.
Fig. 8. Ventral view of the arm region of embryo CLXIII. X 40 diameters.
The fourth division, the pectoral premuscle mass, passes ventral to the brachial plexus and joins the arm premuscle sheath near the proximal end of the humerus. This pectoral premuscle mass is continuous medially with an irregular mass of condensed tissue which extends to the base of the tongue. The cephalic portion of it is supplied by two nerves, one a branch of the first and second cervical, and the other a branch of the third cervical nerve. These two branches form a loop on the siu'face of the mass. They correspond to the ramus descendens n. hypoglossus and ramus communicans hypoglossus uniting to form the ansa hypoglossus. Hence I have called this the infra-hjoid premuscle mass. I have not been able to determine the fate of the condensed tissue on the median side of the pectoral premuscle mass, and caudal to the infrahyoid mass. The phrenic nerve ends very close to it, and very likely this is diaphragm premuscle mass.
The rhomboid premuscle mass lies lateral to the second division of the lateral premuscle mass and is an ill-defined plate of condensed tissue. It lies at the level of the fifth cervical vertebra and receives a branch from the fifth cervical nerve, arising in connection with a nerve to the levator scapulae mass.
The caudal end of the trapezius premuscle mass is seen in Fig. 7, lateral to the levator scapulse mass. The main portion of the trapezius premuscle mass lies opposite the cephalic four cervical vertebrae. It is supplied by the spinal accessory and communicating branches from the first four cervical nerves.
Arm pre muscle sheath
The skeletal core of the arm is surrounded by a mass of tissue which shows no signs as yet of splitting into separate masses. Along the median side of the humerus this sheath is interrupted by the entrance of the brachial plexus and nerves. In places the sheath is separated from the skeletal core by blood-vessels, but in most places no sharp line of separation can be seen. Toward the distal end of the arm the sheath merges into the more primitive mesenchymal tissue which fills most of the distal end of the arm. In Fig. 8 the ,distal limit of the premuscle sheath is indicated, a portion of the primitive arm mesenchyma having been removed to show the limit of the sheath, the hand plate, the border vein and the venous plexus between the hand plate and the mesenchyma.
The muscle plate column is supplied by branches of the dorsal rami from all the nerves in this region. They enter the median side of the muscle-plates branch Avithin them, one branch passing through to the subcutaneous tissue.
Branches from the anterior rami of the III, IV, V, VI and VII cervical nerves supply the levator scapulfe and serratus anterior premuscle mass. The rhomboid premuscle mass is supplied by a branch which comes off with the one from the V cervical.
The phrenic nerve arises from the median side of the trunk formed by the IV and V cervical nerves. It does not reach quite to the level of the first rib. See Fig. 6.
The brachial plexus is formed from the ventral divisions of the IV, V, VI, VII, VIII cervical and I thoracic nerves. The main portion of the plexus forms a continuous sheet of nerve tissue in which only indications of the three cords can be distinguished. The plexus passes laterally into the arm without any caudal inclination. On reaching the arm it splits into a dorsal and a ventral division. The dorsal division corresponds to the continuation of the posterior cord. It passes around the dorsal side of the humerus, decreasing rapidly in size and ends in the premuscle sheath near the distal end of the humerus. Most of it represents the musculo-spiral nerve. A small branch, which is probably the circumflex, is given off near its beginning. Fibers from all the spinal nerves forming the plexus can be traced into this dorsal division. The ventral division is partially divided into two parts, which probably represent the outer and inner cords. From the outer arises the suprascapular nerve, having fibers from the IV, V, and VI cervical. It passes ventral to the scapulo-humeral junction into the arm premuscle sheath. The rest of this outer cord splits into the musculo-cutaneous and the outer head of the median. The musculo-cutaneous passes into the premuscle sheath on the ventral side of the humerus, and the median into the sheath distal to this, reaching as far as the distal end of the humerus. The inner cord terminates in the ulnar nerve, which runs into the premuscle sheath along the median side of the humerus as far as the beginning of the ulna. Branches going into the pectoral premuscle mass leave the median side of the plexus, one mostly from the outer and the other two from the inner cord. They correspond to the external and internal anterior thoracics. In Fig. 6 the lengths of the various nerves are indicated.
Embryo CIX measures V. B. 10.5 mm. and X. B. 11 mm. in lengtli and is about five weeks old. There is a marked advance over the preceding stage. Cartilage has made its appearance both in the vertebrae and in portions of the arm skeleton. There is considerable difference in the character of the cartilage of the vertebra from that in the arm. The latter seems more advanced and lias more the appearance of true hyaline cartilage. It is possible that the cartilage appears first in the arm, though I have not been able to examine intervening stages to determine this with certainty. Other portions of the arm skeleton are in the precartilage and condensed tissue stages. Both cartilage and precartilage are surrounded in most places by a distinct perichondrium. This takes a very deep stain with the alum carmine. This perichondrium shades off into the condensed tissue of the carpus, which is like that composing the skeletal core in the preceding stage. This again shades into the even less differentiated tissue of the digits, which is at a.bont the same stage of development as the hand plate of the preceding stage, and it in turn shades off into the surrounding mesenchyma.
The muscles in the arm region show very different degrees of development. Those derived from the muscle plate system are in advance of most of the others. The trapezius, levator scapulae and serratus magnus are about as far advanced as those from the muscle plate system, they show distinct muscle fibers and are for the most part quite sharply limited from the surrounding loose mesenchyma. In position they correspond with their premuscle masses of the preceding stage. The pectoral muscle is next in advance and the latissimus dorsi next. These two muscles grow from the humeral region towards their future attachments on the body wall. It is this portion which lies farthest from the humerus which seems to show the most advance in fibrillation and the sharpest limitation from the surrounding mesenchyma. At the humeral end these muscles gradually shade into a condensed mesenchyma, which fuses with neighboring muscle and skeletal elements. Both muscles correspond in position to their premuscle masses of the preceding stage. As in the preceding stage, embryo CLXIII, the trapezius and serratus premuscle masses were in advance of the pectoral and latissimus; in embryo CIX we find the same relation still continues.
The remaining muscles of the arm apparently develop in situ from the premuscle sheath and undergo practically no migrations. They do not appear to be as far advanced as any of the above mentioned muscles. Of these muscles developing from, the arm premuscle sheath, the more proximal ones are more developed than the ones more distal. In the scapulo-humeral region most of the muscles show partial fibrillation, while those in the palm of the hand are in about the same condition as the proximal portion of the premuscle sheath in the preceding stage.
The fibrillation, position and nerve supply have made it possible to determine the presence of most of the muscles of the arm.
The Skeletal, System
The Vertebral Column
The intervertebral discs are composed of condensed mesenchyma, the cells having a concentric arrangement about the chorda. The vertebral bodies between the discs are each composed of two masses of cartilage, one on either side of the chorda. Tliey are surrounded by a perichondrium. Along the ventral surface of the vertebral coluuni is a layer of dense mesenchyma, which probably represents both perichondrium and the anterior common ligament. The neural processes, composed of condensed mesenchyma, are clearly defined. They are continuous with the discs and form a wide, shallow groove for the spinal cord. The transverse processes arise by two roots, one from the base of the neural process and the other from the disc. They are of condensed mesenchyma.
The Ribs. - The ribs are more sharply defined than in CLXIII. They are of condensed tissue except for a small area near the head, which is of precartilage. They extend farther into the body Avail than in the preceding stage.
Fig. 9. Skeleton of the arm region of embryo CIX, lateral view. X 12 diameters.
The Arm Skeleton
The Scapula is composed of precartilage and has greatly altered in shape. It lies in the region of the lower four cervical and first one or two thoracic vertebrae. From the anterior border, which corresponds to the spine, springs the large curved acromion process. On the median surface at the junction of the humerus with the scapula arises the large hooked coracoid process. Eunning across the median surface of the scapula to the vertebral border is a slight ridge which separates the supraspinatus from the subscapularis muscles and corresponds to the future anterior border. The condensed tissue is thickened on the medial surface into a perichondrium, while on the lateral surface the precartilage shades off into the surrounding mesenchyma.
A rather poorly defined mass of condensed tissue continues from the tip of the acromion toward the tip of the first rib, extending for about one-third this distance. This mass represents the clavicle. From it a mass of ill-def]ned tissue extends to the coracoid process and represents the coraco-clavicular ligament.
The Humerus is directly continuous with the scapula and root of the coracoid process. No signs of joint surfaces or cavity are present. Both ends of the shaft are enlarged and Ihe distal end shows both external and internal condyles. The core of the shaft is of hyaline cartilage; this is surrounded by very thick perichondrium, which shades ofE into the condensed tissue of each end in which is enclosed an area of precartilage. The distal end seems more advanced than the proximal.
The Radius and Ulna are continuous with the distal end of the humerus, no indications of joint surfaces or cavities being present.
Fig. 10. Outline of the arm region of embryo CIX, lateral view from Plate IV. Bardeen and Lewis, Vol. I, No. 1, this Journal. X 12 Diameters.
There is more flexion at the elbow than in CLXIII. The forearm occupies a position about half way between pronation and supination. The core of each shaft is composed of hyaline cartilage. This is surrounded by a very thick perichondrium, which continues into the condensed tissue at either end of the bone, in which precartilage is enclosed. The hand-plate is continuous with the distal ends of the radius and ulna. It is composed of condensed mesenchyma. There are several centers of increased condensation which I believe must correspond to the carpal bones, namely, the scaphoid, lunar, pyramidal, trapezium, trapezoid, OS magnum and unciform. The scaphoid is in line with the radius and the lunar with the ulna, while the pyramidal is at the ulnar side of the carpus, and as the metacarpal V continues from it more than the uniform the whole hand has a peculiar bend toward the ulnar side. From the carpus five masses of condensed tissue project. They shade off into the surrounding mcsenchyma which fills the distal end of the arm. The condition of these finger masses corresponds to the condition of the hand-plate in CLXIII. There is not the sliglitest indication of segmentation into metacarpals and phalanges. The radial of the five projections probably consists of both trapezium and metacarpal I, which have not yet shown signs of separate centers of condensation.
The Muscular System
The muscle plate system has become differentiated into several muscles, namely, the deep dorsal muscles, the intercostals, the abdominal muscles and the deep ventral neck muscles.
The infrahyoid muscles correspond in position and nerve supply with the infrahyoid premuscle mass of the preceding stage. They extend nearly to the region where the median end of the clavicle will eventually extend.
The trapezius muscle has extended posteriorly to the level of the fifth cervical vertebra. Its posterior end lies near to the lateral surface of the body and is connected to the tips of the neural processes as far posteriorly as the second thoracic vertebra by a considerable interval of fascia. As the muscle passes anteriorly it lies deeper and deeper from the surface, being separated from it by the platysma and facial muscles. Its ventral border is free from attachment to the scapula and clavicle. At the level of the second cervical vertebra it is joined by the stemomastoid muscle, which has ascended from the more ventral neck region. The nerve supply is as in the adult.
The rhomboid mass lies in the region of the Y and A^I cervical vertebrae. It connects with the fascia passing to the dorsal tips of the neural processes but has no scapular attachment. A branch of the fifth cervical nerve supplies it.
The levator scapula; and serratus anterior muscles form a continuous fibrillated mass, extending from the first cervical vertebra to the ninth rib. It occupies much the same position that its premuscle mass did in embryo CLXIII except that the posterior end now extends to the ninth rib. Digitations go to all the cervical transverse processes and to each of the anterior nine ribs. The anterior and posterior digitations are very slender and contain but few fibers. The thickest part of the- muscle lies in the scapular region. There is no scapular attachment. The ventral edge of the muscle lies at about the same level as the dorsal edge of the scapula but in a more median plane. Branches from the second to the seventh cervical nerves supply the muscle. The first three penetrate directly into the muscle. The last three form a trunk which runs along the lateral surface of the muscle as far as the fourth rib.
The pedoralis major and minor "^ are united into a common muscle mass, which is well differentiated from the surrounding tissue. It forms a thick oval mass, which extends from the level of the second rib to the proximal portion of the humerus. The greater part of the muscle thus lies anterior to the first rib. As the mass bends towards the humerus it is attached also to the clavicle. So probably both sterno-costal and clavicular portions are present. The median side of the mass bulges towards the coracoid process and represents the minor. Most of the mass shows distinct fibrillation, but toward the humerus this passes into the condensed tissue which is not sharply outlined from the surrounding structures. The position of the pectoral muscle corresponds to the position of the pectoral premuscle mass in embryo CLXIII. Branches from the median side of the brachial plexus supply the pectoral. Two from the external cord contain fibers from the fifth, sixth and seventh cervical nerves. Two come from the inner cord. Within the muscle complicated anastomoses occur from which fibers spread out in all directions.
The muscles thus far considered were fairly definite, and, as we have seen, come from quite definite premuscle masses. The remaining muscles of the arm are in process of differentiation from the arm premuscle sheath. The exact limits of the individual muscles are almost impossible to determine.
The deltoid muscle extends from the acromion and clavicle and fascia over the infraspinatus to the humerus. It is very closely connected with the infraspinatus and only by the difference in the nerve supply can the two be separated. The position of the teres minor is also only indicated by its nerve and not by any line of separation between it and the infraspinatus or deltoid. The origin of part of the deltoid from the acromion and clavicle helps to distinguish some of its fibers, but a short distance from this origin no line of separation can be made between it and the infra- and supraspinatus muscles. Condensed tissue connects it with the triceps and pectoral muscles. The circumflex nerve supplies this muscle and also sends a branch to fibers which are closely associated with the infraspinatus and probably constitute the teres minor muscle.
That portion of the infraspinatus which lies on the lateral surface of the scapula is fairly distinct except where the deltoid and teres minor muscles join it. The portion of tlie supraspinatus on the anterior onefourth of the median surface of the scapula is distinct, but after it passes the acromion it is inseparably' connected with the infraspinatus and deltoid and pectoral muscles. These muscles shade off into the 23roximal end of the humerus. The main portion of each of these muscles contains muscle fibers. The suprascapular nerve supplies the supra- and infraspinatus muscles.
23 Lewis, Observations on the pectoralis major muscle in man, Johns Hopkins TTosp. Bui., Vol. XII, 1901.
The subscapularis muscle arises from the posterior one-half of the median surface of the scapula and passes beneath the coracoid process to the humerus. The circumflex nerve separates a portion of it from the teres major muscle, but the scapular portions of the two are closely imited, as is also the long head of the triceps. A branch from the circumflex and another from the posterior cord of the brachial plexus supply the subscapularis.
The teres major and latissimus dorsi muscles are closely associated at "their humeral end. The latissimus dorsi' lies in the lateral thoracic region, extending posteriorly as far as the fourth rib. It has no attachments to the ribs or vertebral column. The two muscles are inserted together into the proximal portion of the humerus. The teres major arises from the axillary border of the scapula near its posterior angle. The common portion of the latissimus and teres passes close to the posterior cord of the brachial plexus, from which a large branch is given off that runs into the latissimus and has a brush-like ending near the posterior limit of the muscle. A smaller branch of the posterior cord is given off to the teres major.
The triceps muscle extends along the posterior and lateral surfaces of the humerus, extending from the scapula to the ulna. Indications of the three heads are present. The portion of the muscle lying near the insertion of the latissimus dorsi and the infraspinatus muscles is not sharply defined from them. The musculo-spiral nerve passes through the muscle and gives branches to it.
The biceps and coracohracJnaUs muscles lie along the median side of the humerus, extending from the coracoid process to the radius. The two heads of the biceps are quite closely united nearly to their origins, Avhich are but a short distance apart. The portion of the coracoid process from which the long head arises must ultimately become a portion of the head of scapula. The attachment of the coracobrachialis to the humerus is by condensed tissue, as is the distal end of the biceps to the radius. The distal end of the biceps blends with the brachialis and the flexor mass. The musculo-cutaneous pierces this group and gives off branches to it.
The brachialis muscle is closely attached to the distal one-half of the hmnerns over the anterior and median surfaces. It is also closely attached to the overlying biceps muscle and it is impossible to determine just the line between the two or between it and the brachioradialis muscle. It is also impossible to determine the exact line between the muscle and the underlying perichondrium. It is closely associated with the triceps on one side and the deltoid on the other. The main portion of the muscle is fibrillated and is inserted into the ulna by condensed tissue, which is closely associated with the, flexor mass of the forearm. The musculo-cutaneous nerve gives off a large branch which has a brush-like endins; within the muscle.
Fig. 11. Outline of the arm region of embryo CIX, median view, from Plate V. Bardeen and Lewis, Vol. I, No. 1, this Journal. X 15 diameters.
The flexor muscle mass of the forearm forms a thick layer over the median surface of the ulna, radius, carpus and proximal end of the metacarpus. It is with considerable difficulty that I have separated this mass into two layers. The superficial layer is smaller in extent and lies in the proximal region of the forearm. It is connected with the radial portion of the forearm by a condensed tissue mass and distally fuses with the deep layer to become continuous with the condensed tissue of the digits. The median nerve passes through the proximal portion and then comes to lie between the two layers. From its position and relation to the median nerve I believe this to be the layer from which the flexor carpi radialis, flexor sublimis digitorum, pronator teres and palniaris long-us muscles differentiate. Branches from the median nerve supply this layer. Both layers arise partly from the inner condyle of the humerus, and are continuous more or less with the muscles of the upper arm. The deep layer is closely attached to the perichondrium of the forearm and hand. It is wider in extent than the superficial and shows indications of separations into muscles. Tlie portion for the flexor carpi nlnaris shows most advance. The extension into the hand probably constitutes the portion from which the interossei and lumbrical muscles and flexor tendons develop. It is continuous with the condensed tissue of the digits. The portion on the forearm forms the flexor profundus digitorum, flexor pollicis longus, flexor carpi ulnaris and pronator quadratus muscles. Both the ulnar and median nerves supply the deep layer.
The extensor mass of the forearm is farther advanced than the flexor. It can be differentiated into three groups of muscles which accord well with the adult groups. The first group, the largest and most superficial, extends from the lateral condyle to the proximal ends of the digits, where it blends with the condensed mesenchyma. It is a thin layer and spreads out over the ulnar two-thirds of the forearm and is quite closely applied to the perichondrium and cpndensed mesenchyma of the skeletal structures beneath. A portion of it overlaps the second and third groups. It is the still undifferentiated extensor communis digitorum, extensor carpi ulnaris, and extensor minimi digiti. It is supplied by branches of the posterior interosseus nerve.
The second group occupies the proximal portion of the radial side of the forearm. It arises in connection with the first group from the external condyle and adjoining portion of the humerus. The muscle mass passes distally along the radius and soon divides into two parts between which the radial nerve passes. The radial part fuses with the condensed tissue of the distal end of the radius. It is the brachioradialis muscle. The second part passes beneath the third group and fuses with the condensed mesenchyma at the proximal ends of the second and third digits. It is the extensor carpi radialis longior et hrevior muscle. Branches of the musculospiral nerve supply this second group.
The third group arises beneath the first from the ulna and radius. Its fibers pass toward the radial side of the forearm, passing from beneath the first group and over the second group, and finally end in the condensed tissue of the first and second digits. The portion to the second digit is closely fused with the portion of the first group which goes to this digit. This group is quite closely applied to the underlying skeletal condensed tissue. The third group represents the abductor pollicis longus, extensor pollicis brevis, extensor pollicis longus and extensor indicis proprius. Branches of the musculospiral nerve supply this group.
The supinator I believe must arise in connection with the third group, judging from its position and the direction of its fibers.
The muscle fibers of the extensor groups do not extend as far distally as do those of the flexor mass.
The enormous size of the lower cervical nerves attracts the attention at once. In the plates and figures they are given in their true proportion to the other structures. The main portion of the brachial plexus has but a very slight posterior inclination.
A branch from the V cervical supplies the rhomboid muscle mass.
The V, VI, VII and VIII cervical and I thoraeic nerves unite to form the brachial plexus. The IV cervical does not connect with the plexus. The main portion of the plexus forms a continuous sheet in which indications of the three cords can be seen. The V and VI unite before joining the others and from this union is given off the -suprascapular. It leaves the trunk at right angles and has the appearance of having its proximal end dragged distally to\\'ard the arm by the main portion of the plexus. The VIII and I thoracic unite before joining the plexus. The continuous sheet formed by these five nerves soon splits into a lateral (dorsal) and median (ventral) division. The lateral corresponds to the posterior cord and from it arise the circumflex, subscapular and musculospiral nerves. These nerves take the normal course found in adult and supply the same muscles as in adult. Cutaneous branches are also given ofl^. The median sheet of the plexus quickly divides into several bundles. The anterior one corresponds to the distal end of the external cord. From it are given off the musculo-cutaneous, two branches to the pectoral mass, and one head of the median nerve. The posterior division corresponds to the distal end of the inner cord. From it arise branches to the pectoral mass, the inner head of the median, the ulnar and internal cutaneous nerves. The distal end of the median splits into a peculiar fan-like arrangement of its branches. Both median and ulnar give branches to the deep flexor mass and anastomose within the mass.
I have attempted to trace the origin of the fibers in the main nerves of the arm. The results are given in the following table:
Suprascapular V, VI ?
Subscapularis V, VI, VII
Long thoracic VII, VIII I
Anterior thoracics V, VI, VII, VIII I
Musculo-cutaneous V, VI, VII ?
Median V, VI, VII, VIII I
Circumflex V, VI, VII
Musculospiral V, VI, VII, VIII I
Ulnar VI?, VII, VIII I
Embryo XLIII measures 16 mm. V. B. and 11 mm. jST. B. It is about six weeks old. Many changes have taken place during the sixth Aveck. The entire arm has migrated posteriorly, dragging muscles and nerves with it. The brachial plexus has a decided posterior inclination. The skeletal system is much farther advanced and consists for the most part of cartilage; its individual elements are assuming more the adult form. The clavicle now unites the arm and thoracic skeletons.
The muscular tissues have become more clearly differentiated and except in the hand are easily distinguished. Muscles, such as the trapezius, serratus, and pectoral, have spread out into sheets and acquired more their permanent attachments, in the case of the trapezius, latissimus and pectorals by migTation or extension of their fibers.
In the hand, however, we find the interossei still in an undifferentiated condition like that of the deep flexor layer in embryo CIX or the serratus and infrahyoids in embryo CLXIIL'
The Skeletal System
The vertebral column. The intervertebral discs are of still more compact tissue than in embryo CIX, but they occupy only about one-fourth height of the segment, while in CIX they occupied nearly one-half the anterior-posterior length of the segment. The body of each vertebra contains a large mass of cartilage, which is continuous with the cartilage in the transverse and neural processes. Indications of the hypochordal brace of Froriep are present in connection with the ventral side of the first three discs. The anterior one is the largest, the others decreasing rapidly in size.
The ribs are composed of long, slender cartilages, surrounded by a thick perichondrium. This is continuous with the condensed tissue of the tips of the ribs. The tips of the first seven ribs are connected by a narrow strip of condensed tissue which appears to be formed by the turning anteriorly of their tips until they touch the rib above and fuse with it. Thus is formed the' anlage of one-half the sternum on either side some little distance from the median line. There is at present no sign of union of the two halves of the sternal anlagen. The first rib is fused with the median end of the clavicle. The ribs show a marked increase in their lateral convexity, as in embryo CIX there was scarcely any. There are no joint cavities between the ribs and vertebrte.
The scapula is composed largely of cartilage. It has migrated posteriorly so that less than one-half of it lies above the level of the first rib. The whole scapula is larger than in embryo CIX. There is a thick layer of perichondriuui around the cartilage and a considerable mass of condensed tissue along the vertebral border, and at the posterior angle, the cartilage reaches to the level of the third rib and the condensed tissue nearly to the fifth. The anterior border is somewhat irregular and thickened and gives origin in part to the supraspinatus muscle. The lateral lip of this border probably represents the spine and the median lip the anterior border. Projecting from the lateral side of the head and continuous with the lateral lip of the anterior border is the acromion process. It is large, curved and mostly of condensed tissue and contains a slender core of cartilage continuous with the cartilage of the body. The coracoid process arises from the median side of the head, is larger than the acromion, and contains a much larger cartilao-inous core, which is continuous with the cartilage of the body. The acromio-clavicular ligament is strongly developed.
Fig. 12. Cartilaginous slceleton of tlie arm of embryo XLIII, lateral view. X 20 diameters.
The clavicle consists of a thick mass of condensed tissue, extending from the acromion to the tip of the first rib, where it continues with the half sternal anlage. There is no line of separation at either end. There is a small core of a peculiar precartilaginous tissue.
The humerus is larger, longer and more slender in proportion to its length than in the preceding stage. The two ends are enlarged. The main portion is of cartilage snrronnded by a thick perichondrihm which is continuous with that of the head of the scapnla, forming the Ijeginning of the capsular ligament. There is also a strip of perichondrium between scapula and humerus in which there are no signs of a joint cavity. At the proximal end the perichondrium shows thickenings for the tuberosities, while at the distal end the condyles are for the most part of cartilage continuous with that of the main portion. Considerable masses of condensed tissue, however, help to increase the size of the condyles. A portion of the head of the humerus rests against the base of the eoracoid process, indicating that a portion of this is to be incorporated with the head of the scapula.
The ulna and radius are of cartilage surrounded by a thick perichondrium. This is continuous with that of the distal end of the humerus, forming the beginning of the capsule. The perichondrium of the proximal end of the radius is continuous with that of tlie adjoining surface of the ulna. The cartilages of the humerus, radius and ulna are separated from each other by condensed tissue in which no signs of cavities are present. The olecranon is quite well developed and consists mostly of cartilage. The coronoid process is mostly of condensed tissue. The great sigmoid fossa is rather shallow. The bicipital tuberosity is of condensed tissue. The distal ends of these bones are enlarged and separated from each other by condensed tissue continuous with the perichondrium of each.
The carpus consists of a condensed tissue matrix in which lie imbedded the various cartilages. The distal row is complete, the trapezium, trapezoid, os magnum and unciform. The latter has spread in between the fifth metacarpal and the cuneiform (pyramidal). In the proximal row the cuneiform and scaphoid are of cartilage and the hmar and pisiform of condensed tissue.
The metacarpus shows five slender cartilages surrounded by very thick condensed tissue layer or perichondrium. The first metacarpal cartilage is only about one-half the length of the others.
The ulnar four plialanges of the first row are present as short slender cartilages deeply imbedded in condensed tissue. In the first digit condensed tissue takes the place of the cartilage. At the tip of each digit is a mass of condensed tissue.
There are no joint cavities between the cartilages of the hand, each one is separated from its neighbor by an area of condensed tissue.
Hagen has reconstnicted the cartilaginous skeletal system of a hnman embryo of abont this age. A comparison of the drawings from the reconstructions shows that there is considerable variation in the carpal region. In none of my stages does the metacarpal come irt contact with the radius, either before or after the cartilages of thecarpus and metacarpus appear, and there is a considerable area of dense mesenchyma between metacarpus and radius. I am inclined to believe what he calls metacarpal I, may be trapezium and his so-called firstphalanx the metacarpal.
The Muscular System
Plates I and II, Figs. A and B. The trapezius muscle has both clavicular and acromial attachments. The muscle has extended posteriorly so that the muscle fibers run from theocciput to the level of the fifth rib. They are connected by a considerable interval of fascia with the dorsal ends of the cervical and all the thoracic neural processes.
The levator scapulce and serratus anterior muscles are greatly altered iit shape. The latter forms a broad, thin sheet between the dorsal border of the scapula and the first nine ribs, being attached by a digitation tO' each rib. The scapular attachment is into the condensed tissue along its dorsal border.
The pectoral mass is now spread out into a large, thin sheet, which has split into the major and minor muscles. The clavicular and sternocostal portions of the pedoralis major are separated by a considerable interval. The clavicular fibers arise from the median one-third of the clavicle and pass to the humerus. They overlap the humeral ends of the sterno-costal fibers which arise from the first six ribs and the sternal anlage.
The pedoralis minor is a distinct muscle arising from the second, third and fourth ribs and passing to the coracoid process.
The subelavius muscle is quite Avell developed and runs from the first ril) to the clavicle, having a course nearly at right angles to the latter.
The latissimus dorsi has spread out into a broad, thin sheet of muscle fibers, which are connected by fascia with the lower thoracic and lumbar neirral processes. Its humeral end is closely miited with the teres major.
The teres major muscle has about the relations found in the adult. It and the latissimus dorsi are inserted together into the humerus.
Tlie deltoid muscle is very much like the adult in its attachments and shape.
Hagen, Die Bildung des Knorpelskeletes beim mensclalicben Embryo, Arch, fiir Anat. u. Pbys., 1900.
The infraspinatus nniscle arises from the anterior portion of the lateral sin-face of the scapula and can bo easily traced to its insertion into the great tuberosity of the humerus. The teres minor cannot be separated from it.
The supraspinal us muscle arises from the anterior thickened border of the scapula and passes to the great tuberosity of the humerus.
The suhscapularis muscle occupies the central portion of the median surface of the scapula. It is separated from the teres major. It passes beneath coracoid process to the lesser tuberosity of the humerus.
The triceps muscle is easily traced from its origin by the three heads to its insertion into the olecranon process. The three heads are quite easily distinguished. The long head is smaller in proportion than in the adult.
The biceps muscle is more elongated and shows more of a separation of its two heads than in embryo CIX. The long head still arises from the base of the coracoid process. The two heads join about the middle of the humerus and pass to a thickening of condensed tissue on the radius. The short head arises in common with the coracobrachialis muscle from the tip of the coracoid process. This latter muscle is inserted into the middle of the median surface of the humerus. It is closely connected with the biceps for most of its length.
The hracJiiaUs muscle is spread out more over the distal portion of the humerus and its muscle fibers extend farther toward the insertion into the coronoid process of the ulna than in the preceding stage.
The flexor mass of the forearm and hand show a most marked advance over the preceding stage. The various muscles of the superficial layer which arise from the internal condyle are easily recognized. They are more or less fused at their origin and for some little distance from it.
The pahnaris longus muscle, the most superficial one, is thin and wide, ends in the condensed tissue of the palmar fascia.
The pronator teres muscle passes to the middle of the shaft of the radius.
The flexor carpi radialis muscle lies mostly on the radial side of the forearm, towards the distal end of which it bends under the deep flexor and ends in a condensed tissue tendon which fuses with the condensed tissue near the proximal end of the second metacarpal. This portion of the muscle is not yet clearly differentiated from the condensed tissue on the palmar surface of the caqms.
The flexor digitonim suhlimis muscle arises beneath the palmaris longus in connection with it from the internal condyle, and also from the shaft of tlie ulna, for a little distance distal of the coronoid ]~)rocess.
It is very broad and spreads out over the middle of the forearm and carpus, where it divides into fonr broad, thin tendons which fnse with the condensed tissue surrounding the distal end of the four ulnar metacarpals and first row of phalanges. The muscle fibers continue distal as far as the middle of the carpus, where the muscle becomes wider and thicker. The tendons do not show the split which is later to appear and enclose the deep flexor tendon. The strongest part of the tendons lie on the ulnar side of digits.
The deep layer of the preceding stage has undergone marked changes.
The flexor carpi ulnaris muscle is quite distinct. It arises partly from the internal condyle superficial to the sublimis and closely connected with it and the palmaris longus and partly from the ulna. The muscle at its origin is broad and thin but narrows into a condensed tissue tendon which is inserted into the os pisiform.
The flexor digitorum profundus and the flexor polUcis longus muscles arise from the surfaces of the radius and ulna and the internal condyle. They are closely imited and pass to the carpal region where division takes place into five well-formed oval tendons, which pass beneath the tendons of the sublimis, and fuse with the condensed tissue about the ends of the digits.
The pronator quadraius muscle is a small, oval mass connecting the distal ends of the ulna and radius.
The lumhride muscles are fonned. They arise from the profundus near the angles formed by the iive tendons. They are short and contain distinct muscle fibers which end in tendons that fuse with the condensed tissue on the radial side of the ulnar four digits.
The intrinsic muscles of the hand, the interossei, and muscles of the thumb and little finger, are represented by a late premuscle tissue in which a few muscle fibers are beginning to appear. These masses are more or less continuous with each other and lie on the palmar surface of the carpus and metacarpus and partially in between the latter. The distal ends of these masses fuse with the less differentiated condensed tissue about the digits.
The extensor muscles of the forearm show considerable advance over the preceding stage, but the development does not seem to have been as rapid as in the case of the flexor muscles.
Of the first group, the extensor communis digitorum and the extensor minimi digiti are united into a broad, thin sheet which divides in the metacarpal region into four broad, thin tendons that end in the condensed tissue of the four ulnar digits. The extensor carpi ulnaris closely associated with this muscle at its origin from the external condyle arises also partly from the ulna and is inserted into the condensed tissue at the proximal end of the fifth metacarpal. It is quite separate from the common extensor for the greater part of its length.
Of the second group, the hracMoradinlis is quite distinct from the extensor- carpi radialis longior et hrevior for most of its length, but at their origin, however, the two are closely connected. Both muscles are broader and larger than in the preceding stage. The extensor passes beneath the third gTOup and ends in the condensed tissue near the proximal ends of the second and third metacarpals.
The third group, which arises beneath the first from both radius and ulna, has split more or less into four parts. The proximal one, which is the most completely separated, is the supinator and passes from the ulna and external condyle to the radius. It is united with rest of this group along their ulnar origins, forming thus a continuous sheet for a short distance. The next two pass over the extensor carpi radii tendon, and fuse with the condensed tissue of the first digit. They are the abductor pollicis longits, extensor poUicis brevis and the extensor poUicis longus muscles. The fourth division is broad and thin and soon joins the deep surface of the tendon of the extensor communis and goes with it to be inserted into the condensed tissue of the second digit.
By the migration of the arm posteriorly the brachial plexus has been pulled caudally and given a decided posterior inclination. It has also divided into the various cords more than in the preceding stage.
The distribution of the muscle and cutaneous nerves is much as in. the adult and as in the next stage.
Embryo XXII measures 20 mm. V. B. and 18 mm. X. B. It is about seven weeks old. The entire arm has a more posterior position. The lower angle of the scapula is at the level of the sixth rib, its anterior limit is about at the seventh cervical vertebra. The entire arm as well as its various parts have increased in size. The muscles are sharper and better developed than the preceding stage. Every muscle that the adult arm presents can now be recognized and each one now contains muscle fibers. The tendons are better formed and can be traced farther towards their final insertions. The ligaments and fasciae are also more distinct. The process of ligament and tendon formation from the condensed mesenchyma is still in progress at the distal ends of the digits. The skeletal elements are for the most part fairly well formed in cartilage except the distal row of phalanges.
The Skeletal System
The vertebral column
The intervertebral discs are reduced in thickness, while the bodies of the vertebra have increased and occnpy about four-fifths of each segment. The neural and transverse processes are larger and for the most part of cartilage. At the tip of the neural processes, which reach about one-half way around the spinal cord, is a small mass of condensed tissue at what juay be considered the growing point. These processes arise entirely from the body and not from the disc. So the body has probably grown at the expense of the disc. The perichondrium, wliich surrounds the body and its processes, is thickened along the ventral side of the bodies into the anterior common ligament.
The ribs are of cartilage surrounded by thick perichondrium, wliicli is continuous with the condensed tissue anlage of the one-half the sternum. The distance between the two halves of the sternum is not as great as in the preceding stage and at the anterior end they ai'e just beginning to come in contact with each other. There are no joint cavities between the ribs and vertebrae.
The clavicle is composed of cartilage somewhat different in appear ance from that in the other bones. It is continuous with the acromion and sternum by an area of condensed tissue. It is surrounded by a typical perichondrium. There are distinct coraco-clavicular, costoclavicular, and interclavicular ligaments.
The cartilaginous scapula is very much larger than in the precedingstage and contains no large areas of condensed tissue. It has moved posteriorly and lies in the region from the last cervical to the fifth thoracic vertebrae. Its dorsal border also extends farther dorsal than in any of the preceding stages. The acromion and coracoid processes are large and of cartilage with only the ordinary thickness of perichondrium which is continuous with that surrounding the rest of the scapula. The spine has not yet appeared but the thickened anterior border from which the supraspinatus muscle arises probably represents by its lateral lip the spine and by its median lip the future anterior border. The acromion arise partially from the lateral side of the anterior border. The head seems to have enlarged at the expense of part of the base of the coracoid process as the long head of the biceps now arises from the junction of the coracoid and the head, and the head of the humerus does not rest against such a large proportional area of the coracoid. There is a distinct suprascapular and a coraco-acromial ligament. At the posterior angle of the scapula there is small mass of condensed tissue which gives attachment to a portion of the serratus, latissimus, and teres major muscles.
The humerus is much hirger than in embryo XLIII, and has much the adult shape, though of course it is thicker in proportion to its length. It is composed of cartilage. There is a capsular and a coraco-humeral ligament. No joint cavity exists between the scapula and humerus. The tuberosities and condyles are fairly well formed in cartilage and â€¢condensed tissue. The bicipital groove is present.
The ulna and radius are larger and longer than in the preceding stage 3ind are well formed in cartilage. The olecranon, coranoid and styloid processes are partially formed in cartilage and condensed tissue. The perichondrium about the ulna and radius is quite thick. The capsular .and orbicular ligaments are present. No joint cavities exist and the cartilages are separated by condensed tissue continuous with the periâ€¢ciiondrium.
Fig. 13. Cartilaginous skeleton of the arm of embrj-o XXII, lateral view. X 12 diameters.
All the bones of the carpus are represented by cartilage, and in about their relative positions. The amount of condensed tissue matrix is much less than in the preceding stage. The condensed tissue matrix is continuous with the ulna and radius and the five metacarpals without joint cavities. Indications of ligaments of the wrist are present.
The five metacarpals are present in cartilage surrounded by thick perichondrium. The first is the shortest.
The first two rows of phalanges are present in all the digits. They are of cartilage surrounded by a very thick perichondrium, which is continuous with the condensed tissue between them and the metacarpals and between the phalanges them.selves. It is also continuous with the enlarged condensed tissue tip of each digit. There are thickenings for the various ligaments connecting the metacarpals and phalanges and the phalanges with each other.
The Muscular System
(Plate II, Fig. C.) The trapezius muscle fibers extend from the occiput to the level of the sixth rib. There is a considerable interval of fascia connecting them to the neural processes of the lower cervical and the thoracic vertebrae. There is a tendonous attachment to the clavicle and acromion and into fascia or condensed tissne on the surface of the infraspinatus between the trapezius and the deltoid.
The rliomhoid muscle lies in the region of the seventh cervical to the fourth thoracic vertebrae. It is inserted into the condensed tissue along the dorsal border of the scapula.
The latissimus dorsi muscle fibers extend from the humerus to the level of the ninth rib. There is a considerable interval of fascia between them and the neural processes of the lower thoracic and the first two or three lumbar vertebrae. This dorsal fascia is not very well marked. The latissimus also has fibers attached to the condensed tissue at the inferior angle of the scapula.
The serratus anterior muscle is separate from the levator scapulae except near its attachment to the scapula. It is a broad, thin sheet, having digitations to the first eight ribs.
The pedoralis major muscle is well developed. The separation between the clavicular and the sterno-costal portions is less marked than in the preceding stage.' The muscle is attached as low as the sixth rib.
The pedoralis minor muscle is quite distinct from the major, as a considerable layer of loose mesenchymal tissue lies between them. It arises from the second, third and fourth ribs and passes to the coracoid process.
The siibclavius muscle is inserted into the clavicle at an angle of 45°. As the scapula and clavicle sink down towards the level of the first rib the angle at which this muscle is inserted into the clavicle decreases.
The teres major muscle arises from the lower angle of the scapula and passes to the humerus. It is interesting to note that at this stage tendon of the latissimus dorsi twists around the lower l^order of the teres to be inserted with it into the humerus.
The deltoid muscle is large and well developed.
The suprasfinatus muscle arises from the thickened anterior border of the scapula. It cannot be said to take origin more from the lateral surface than from the median surface of the scapula.
The infraspinatus muscle occupies the middle of the lateral surface of the scapula and passes beneath the deltoid to the great tuberosity of the humerus.
The suhscapularis muscle arises from most of the median surface of the scapula. Its tendon of insertion is broad and thin and closely applied to the capsular ligament.
The three heads of the triceps muscle are easily distinguished. The long and external heads are of about the same size. The anconeus muscle is continuous with the triceps but arises from the external condyle and passes to the side of the olecranon and adjoining surface of the shaft of the ulna.
The long head of the biceps muscle arises from the junction of the coracoid process and the head of the scapula and passes through the bicipital groove. The two heads are inserted together into the condensed tissue swelling on the radius.
The corncobracJtviUs muscle and short head of the biceps are intimately connected for most of the length of the former.
The brachialis muscle has spread out over more of the distal surface of the humerus than in the preceding stage.
The flexor muscles of the forearm are easier to distinguish than in the preceding stage.
The tendon of the palinaris longus is narrower in proportion than in embryo XLIII.
The tendon of the flexor carpi raclialis muscle can be traced farther towards its insertion into the base of the second metacarpal than in embryo XLIII.
The muscle fibers of the flexor sublimis digitorum still run to the carpus before the ^\ide tendon begins. This tendon soon splits into four tendons which go to the four ulnar digits. These tendons are better formed than in the preceding stage and split to surround the tendons of the deep flexor. Their ends fuse with the thick perichondrium about the phalanges.
The flexor carpi uhiaris muscle shows distinctly its two heads of origin. It has a well-formed tendon of insertion.
The deep flexor muscles can be separated into the flexor polUcis longus and the flexor profundus digitormn muscles. The muscle fibers of the profundus continue into the carpal region and end in a broad tendon which divides at the base of the metacarpus into four well-formed tendons. These fuse with the condensed tissue at the tips of the digits. There is a slight split in each of these tendons near its end. The tendon of the flexor longus pollieis behaves similarly.
The pronator quadratns muscle is oval in cross section, and connects the distal ends of the radius and ulna.
The lumbricales are quite well developed and their fairly well-formed tendons end in the perichondrium on the radial side of the digit.
The interossei mnscles and the small mnscles of the thumb and little finger are now fairly well developed. Muscle fibers are present.
The extensor muscles of the forearm show considerable advance over the preceding stage. The tendons of the extensor communis digitoriim are longer and narrower. The muscle fibers continue to the base of the metacarpus, where the splitting into the four tendons takes place. The tendons are inserted into the condensed tissue tips of the digits. The edge of the tendons near their insertions are more or less continuous with the perichondrium about the digit.
The tendon of the extensor carpi ulnaris is beginning to. form. One branch of it seems to join the communis tendon. This may be the tendon of the extensor minimi digiti.
Fig. 14. Lateral view of the arm of embryo XXII. from Plate VIII.
The extensor carpi radialis longior et hrevior are not to be separated.
The supinator muscle is well developed and has the posterior interosseus nerve passing through it.
The abductor pollicis longus and extensor pollicis brevis muscles are only to be separated where the muscle fibres pass into tendons, which fuse with the perichondrium of the first digit. The separation occurs at the lower end of the radius. These two muscles are fairly distinct from the supinator and the extensor pollicis longus and extensor indicis projiriiis muscles. The last two muscles are inseparable for part of their course and shortly after dividing each forms a round tendon. The extensor pollicis longus then spreads out into the sheath about the first digit. The extensor indicis muscle joins the nlnar side of the tendon of the commimis to the second digit.
The drachial plexus has a decided posterior inclination and seems to have been pulled down against the first rib. The three cords are so close together that it was impossible to separate them satisfactorily though indications of the cords are present. There is nothing especially peculiar about the distribution of the nerves from the plexus either motor or sensory, which is not present in the adult.
The first indications of the arm bud appear during the third week as a slight swelling in the lower cervical region on the anterior portion of the Wolffian ridge. This gradually enlarges and by the time the embryo is 4.5 mm. in length and three weeks old the arm is of considerable size. The base now lies opposite the lower four cervical and first thoracic vertebrae. The arm bud is at first filled with a homogeneous and closely packed mesenchyma. No nerves or myotome buds have entered the arm, yet it contains the tissue from which the muscular and skeletal elements develop.
During the fourth week before the nerves enter differentiation begins by an increased condensation for the skeletal core. The nerves, however, have reached the base of the arm and have united by their expanded ends into the first beginnings of the cervico-brachial plexus. During the fifth week the nerves from this plexus push into the pre-muscle sheath which surrounds the skeletal core.
By the end of the fifth week the skeletal core can be differentiated into many of the skeletal elements, three of Avhich contain cartilage, namely, the humerus, ulna and radius. The premuscle sheath also has become more or less differentiated into muscles or groups of muscles, between which, however, no sharp lines can, as a rule, be drawn. Toward the distal end the differentiation is less complete, and in the hand premuscle tissue still represents the intrinsic muscles. The nerves have grown into the hand and spread out in a veiy peculiar manner. Most of the branches of the brachial plexus found in the adult are now present.
By the end of the sixth week most of the muscles of the arm are easily recognized. The intrinsic muscles of the hand are just beginning to show fibrillation and are still mostly of premuscle tissue. The tendons and ligaments are also becoming more sharply differentiated. Most of the skeletal elements consist of cartilage and the surrounding thick perichondrium. The clavicle, some of the carpals and the second row of phalanges are of condensed tissue, while the distal row of phalanges are not differentiated as yet. The nerves, both sensory and motor, are distributed much as in the adult.
By the end of the seventh week all the skeletal elements are of cartilage except the distal row of phalanges from the second to fifth digits, which are of condensed tissue. All the muscles are to be recognized and are composed of muscle fibers. The tendons and ligaments, except in the distal part of the digits, are well formed. The digits present a very interesting picture of the differentiation of the cartilage, perichondrium, ligaments, and tendons from the condensed tissue tip of each.
During the process of differentiation other important changes are taking place, namely, the migration caudally of the whole arm, the migTation or extension of certain muscles from the arm caudally along the body wall and the migration of other muscles from more anterior regions to the arm, shoulder girdle and thorax.
We may consider the position of the scapula and the inclination of the brachial plexus as indicators of the migration of the arm. We find, in an embryo of four and one-half weeks, that the scapula lies in the region of the fourth and fifth cervical vertebrae. The brachial plexus and the nerves forming it run to the arm without any caudal inclination. The nerves which leave the plexus do bend posteriorly in the arm. At five weeks the scapula has greatly enlarged and extends from the fourth cervical to the first dorsal vertebrae. Its center has evidently shifted posteriorly. The brachial plexus and the anterior nerves which go to it have a slight caudal inclination. By the end of the sixth week the greater portion of the scapula lies below the level of the first rib, its posterior angle, including the condensed tissue, having extended to the level of the fifth rib. The brachial plexus has been pulled along with the shifting of the arm and has a decided posterior inclination. By the end of the seventh week very little of the scapula lies above the level of the first rib, and its lower angle reaches to the fifth intercostal space. The brachial plexus has a very marked caudal inclination and appears to be bent over the first rib. Before the adult conditions are attained the sca]nila must migrate some distance posteriorly. Part of this movement will take place with the sinking posteriorly of the ventral portion of the thoracic wall, for in these stages the ventral ends of the ribs are as far anterior as the vertebra? from Avhicli they arise.
The migration of the pectoralis major and minor and the latissimus dorsi muscles from the arm posteriorly to the thoracic wall is very evident from the stages we have studied. At a very early stage these masses receive their nerves and later drag them posteriorly. By the seventh week the pectoral mnscles have reached their adnlt positions so far as the thoracic attachments are concerned. The latissimns dorsi, even Ly the end of this week, only extends to the ninth rib.
Another very important group of muscles migrate from the head and anterior cervical region to the arm and thorax. In an embryo, four and one-half weeks old, the posterior end of the trapezius })remuscle mass lies at the level of the fourth cervical vertebra, at five weeks the muscle fibers extend to the level of the fifth cervical vertebra, and at six weeks to the fifth thoracic vertebra. At this age also the muscle has acquired its attachment to the scapula and clavicle. At seven weeks the muscle extends to the level of the sixth thoracic vertebra. The spinal accessory nerve is connected to the premuscle mass as early as the middle of the fifth week, and as the muscle extends posteriorly the nerve is carried along with it.
The sterno-mastoid muscle originates high up in the neck with the trapezius. It extends posteriorly and ventrally, reaching the clavicle and sternum during the sixth week.
The infrahyoid muscles also migrate from the anterior neck region, carrying their nerves down with them.
The rhomboid premuscle mass at 4.5 weeks lies at the level of the fifth cervical vertebra and gets its nerve supply at this time from the fifth cervical nerve. At five weeks it has extended to the sixth cervical vertebra, and at seven weeks it is for the most part in the thoracic region and has acquired its scapidar attachment.
The serratus anterior premuscle mass at four and one-half weeks already extends into the upper thoracic region and has its cervical nerve supply. It has probably already migrated from the cervical region. At five weeks it has reached its posterior attachment on the thorax, but is not as yet attached to the scapula. This occurs during the sixth week. The serratus anterior muscle is thus one of the first of these migrating muscles to attain its permanent attachments. It is also evident that the various serrations of this muscle are of secondary origin.
Currently in Draft section only.
- Mall FP. Development of the ventral abdominal walls in man. (1898) Jour. Morph. 14: 347-366.Mall, Development of the ventral abdominal walls in man. Jour, of Morph., Vol. XIV, 1898
- Bardeen CR. and Lewis WH. The development of the limbs, body-wall and back. (1901) Amer. J Anat. 1: 1-36.
- Byrnes, Experimental studies on the development of the limb muscles in Amphibia, Jour, of Morph., Vol. XIV, 1898.
Plate I, Fig. A. Lateral view of the arm region of embryoXLIII. X 20 diameters.
Plate II, Fig. B. Median riew of left arm of embryo XLIII. X 20 diameters.
Plate III, Fig. C. Median view of right arm of embryo XXII. X 20 diameters.
Cite this page: Hill, M.A. (2020, October 27) Embryology Paper - The development of the arm in man (1902). Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_development_of_the_arm_in_man_(1902)
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