Paper - Comparative studies upon the origin and development of the brachial plexus

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Miller RA. and Detwiler SR. Comparative studies upon the origin and development of the brachial plexus. (1936) Anat. Rec. 65(3): 273- .

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This historic 1936 paper by Miller and Detwiler is a description of the brachial plexus.


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Comparative Studies upon the Origin and Development of the Brachial Plexus

Ruth A. Miller And S. R. Detwiler

Department of Anatomy, College of Physicians and Surgeons, Columbia University

ELEVEN FIGURES

Introduction

The effect of the mesodermal somites upon the development and segmentation of components of the nervous system has been studied by several investigators. Lehmann (’27), working upon Pleurodeles embryos shortly after closure of the neural folds, removed certain somites from one side of the body and also grafted portions of spinal cord lateral to the host’s somites. He concluded that the somites are- responsible for the development of spinal ganglia and the location of sensory and motor roots; ganglionic segmentation is effected by the mesial surface of the somites. Detwiler (’32, ’34), Who performed similar experiments upon Amblystoma embryos at very early stages, obtained irregular spinal ganglia in the complete absence of somites. He also found that ganglia with dorsal roots developed lateral to the host’s somites when the cord was grafted to this position. He concluded that the crest cells have a certain self-dificrentiating capacity and can develop independently of developing muscle and cartilage. His findings verify those of Lehmann in showing that segmenta.tion in the nervous system is dependent.upon the mesodermal somites. l

Closely associated with the question of mesodermal and nervous segmentation is the problem of the relation between the brachial somites, the respective segmental nerves, and the extremity supplied by these nerves. In repeated experiments (’28, and earlier) involving transplantation of the limb bud to various positions upon the body of the host embryo, Detwiler found that the spinal nerves normally supplying the limb tended to innervate it when the latter was grafted several segments from the normal site. The limb exhibited coordinated function as long as it retained connection with one of the original brachial nerves. A series of recent experiments (’34) has further emphasized the close relationship between somites and segmental nerves and the limb. 1) Removal of brachial somites results either in partial loss or in atypical arrangement of the li.mb nerves. In the latter case, the nerves reach the limb, which exhibits normal function. 2) Increasing the number of mesodermal segments by intercalation of extra somites in the brachial region increases the number of segmental nerves to the limb. 3) An increase in the size of the limb bud by the fusion of two rudiments also brings about an increase in the number of nerves supplying the enlarged rudiment. In cases where the rudiments fail to fuse, the extra bud is innervated either in part from the normal plexus or from an entirely new one (Detwiler and McKennon, ’30).

These results raise the question as to the relation between the metameric position of the limb bud and its segmental nerve supply. Harrison (’07) observed that plexuses with identical distribution may have different segmental origins. He ex— plained this as due to variations in the position and extent of the limb rudiment at the time of initial nerve connection. The number of nerves entering into a plexus is influenced by the position of the limb bud; the intrinsic pa-ttern of the plexus is determined by structures within the developing limb. These observations are easily demonstrated in elasmobranch fishes, where the pectoral fin musculature is formed by buds arising from the myotomes, with a spinal nerve to correspond with each bud. Later concentration of the folds results in a fin with a ‘nerve supply greater than the extent of the base seems to Warrant. However, the musculature of the forelimbs of higher ve_rtebrates does not arise from myotomic buds, but is derived from somatopleural mesoderm, as was first demonstrated by Harrison (1895) for the teleost and by Lewis. (’10) and others onrem for the amphibian. Nevertheless in these classes also it is to be inferred that the position and extent of the limb rudiment before concentration are responsible for differences in the number of nerves entering into the formation of various adult plexuses... This has been proven experimentally by Detwiler in the Amphibia (’34).

Investigation of this problem in the higher vertebrates was the object of the present research. Its purpose was to ascertain, in as many different species as possible, the corre spondence between the metameric location of the forelimb rudiment at the time of its greatest extent and the number of segmental nerves which contribute to the brachial plexus.

Materials and Methods

A representative species from each of the great vertebrate classes was chosen for investigation. Among these were includedrtwo divisions of Pisces and four orders of Mammalia. Sixty-five embryos representing eleven different species were studied. The work involved, 1) a study of the position of the forelimb rudiment with respect to the body segments at the so-called"bud stage’ of development, and 2) dissection of the brachial plexus in the adult animal to determine the number of spinal nerves entering into its formation. The bud stage of development proved to be a difficult period to standardize among the different species. In some types the limb rudiment is a fold, in some it is a hemispherical swelling, and in others a gradual ridge. As far as possible the stage was selected in which the ‘bud’ appeared at itslgreatest metameric extent. At this period of development the spinal nerves had not yet begun their growth into the extremity, as was ascertained by serial sections of the brachial region. Sections also proved of aid in determining the metameric position and cranio-caudad extent of the limb rudiment. The following classification gives the relative age and length of ‘the embryos studied.

I. Pisces

A. Elasmobranehii Squalus ac.-mthias (rlogfish), embryo at 15 mm., structure of the adult plexus obtained from descriptions by Miiller (’11).

B. Teleostomi Esox masquinongy (rnuskellunge), embryos at 4 mm., or 8 days, structure of the adult plexus determined by dissection

II. Amphibia Amblystoma punetatum (spotted salamander), embryo at 8 mm., or 12 days, structure of the adult plexus determined by dissection. III. Reptilia

Sceloporus undulatus (fence lizard), embryos at 4 mm., or 2 days, structure of the adult plexus determined by dissection. (No sections were made of this species.) ‘

IV. Aves Gallus domesticus (chick), embryo at 7 mm., or 3 days, structure of the adult plexus obtained from descriptions by Fiirbringer (1879). V. Mammalia

A. Rodentia

1. Mus musculus (house mouse), embryo at 4 mm, or 9 days, structure of the adult plexus determined by dissection. 2. Mus norvcgicus (Norway rat), embryo at 5 mm., or 11 days, adult plexu determined by dissection. 3. Lepus cuniculus (rabbit), embryo at 5 mm., or 11 days, adult plexus determined by dissection.

B. Carnivora. Felis domestiea (eat), embryo at 8 mm., or 12 days, structure of the adult plexus obtained from descriptions in Reighard and Jennings’ Anatomy. (At this age the limb bud showed signs of concentration; earlier embryos were not obtained.)

0. Ungulata Sns scrofa (pig), embryo at 6 mm., or 17 days, structure of the adult plexus obtained from descriptions by Chauveau (1893).

D. Primates Homo sapiens (human), embryo at 7 mm., or 40 days 4!, structure of the adult plexus determined by dissection.

The various developmental stages were checked with descriptions of similar embryos by other investigators. Among these were Scammon (’11) for the dogfish, Harrison (’18, and earlier) for the salamander, Peter (’04-.) for the lizard, Patten’s embryologies of the chick and pig, Minot and Taylor ’05) for the rabbit, and Arey’s embryology of the human. The rnuskellunge, salamander, mouse, rat and rabbit embryos were developed under observation in the laboratory. The dis sections of the brachial plexus also were compared with those onrom of other Workers upon the same or related species. Among these were Herrick’s (1899) description of the teleost plexus, Detwiler’s (’20) of the salamander, Fiirbringer’s (1876) of the lizard, and Krause’s (1884) of the rabbit. Gray’s Anatomy was used as the authority on the structure of the human plexus.

The authors here wish to express appreciation to Mr. Louis L. Mowbray of the New York Aquarium for the supply of muskellunge eggs; to Dr. G. K. Noble of the American Museum of Natural History for the embryo and adult lizard; to Dr. C. M. Gross of this department for mice and rats in all stages, and serial sections of the same; to the Physiology Department of the College of Physicians and Surgeons for their cooperation in obtaining cat embryos; and to Dr. W. M. Copenhaver of this

department for the use of a human embryo from his eollecti on.

RESULTS

For an accurate statement of results a certain amount of explanation and qualification is necessary.

1. The limb rudiment was not at identically the same degree of development in each of the species studied. With the exception of the eat, all were in stages prior to entry of the spinal nerve into the rudiment, and before the latter had become concentrated at the base.

2. The exact length of the base of the bud proved diflicult to determine, even with the aid of serial sections. The rise of the swelling was so gradual that a definite cranial or caudal line of demarcation between the pectoral Wall and limb rudiment Was not always perceptible. The base of the bud extended at least two or three spinal segments cranially and caudally beyond the visible point of greatest Width. This criterion of measurement proved of use in all the types studied with the exception of those in which the rudiment assumed the form of a fold; in these cases the fold disappeared posteriorly with the developing somites and could not be definitely limited. 278 RUTH A. MILLER AND s. 3. DETWILER

3. The greatest difliculty was encountered in determining the metameric location of the limb bud. According to the review by Fiirbringer (1897), the location of the first spinal somite varies with each species, depending upon the number of post-vagal segments. This implies that the spinal and cranial neuromeres are serially continuous. The continuity is more easily demonstrated in the lower than in the higher vertebrates, Where the ‘occipital’ segments are reduced or incorporated with others. However, the disappearance of these segments, especially in the mammals, serves-to emphasize the distinction between head and body somites and to facilitate the isolation of the latter. According to the views of Kingsley, Coghill and Neal, it is to be assumed also that the segments of the hind-brain are homologous with those of the trunk, as the result of primary mesodermic segmentation. The correlation between the number of the somites and the spinal nerves, which was proved by the amphibian experiments mentioned above, shows a subservience of neural to mesodermic segmentation. This correlation may well be applied to the remnants of the cranial somites and their nerves.

The information upon which the enumeration of the trunk somites was based, was obtained from the reults of researches by other workers. The following list, giving the relative position of the first spinal segment in the forms studied, is a compilation of the work of various investigators.

1. Dogfish—-somlte 1 at the second neural segment caudal to that of the vague (Neal, Miiller, Norris and Hughes).

2. Muskellunge—somite 1 at the second neural segment caudal to that of the vague (Harrison, Fiirbringer, Herrick).

3. Salamander——somite 1 at the first neural segment caudal to that of the vague

(A (coghiu).

4. Lizard—somite 1 at the fourth neural segment caudal to that of the vagus ‘ (van Wijhe, van Bemmelen). 5. Chick—-somite 1 at the fourth neural segment caudal to that of the vague (van Wijhe, Fiirbringer).

6. Mammal—somite 1 at the fourth neural segment caudal to that of the vague ' (Fiirbringer, Bardeen and Lewis).

The serial numbers of the spinal nerves entering into the adult plexuses can be determined without difliculty. In the fish some doubt may arise over the formation of the cervical plexus or ‘hypobranohial nerve’ and its relation to the branchial plexus. The structures of the plexuses, which are given below, are interpretations of descriptions by Norris and Hughes

ABBREVIATIONS

Abd., nerves to abductor muscles L. than, long thoracic nerve

Add., nerves to adduetor muscles M., median nerve

A. thorn, anterior thoracic nerve Musc., musculocutaneous nerve Ax., axillary nerve ' Peet., nerves to peetorales

Car. 1. and b., nerves to coracobrachiales Prcor., nerve to procoraeoideus

longus and brevis R., radial nerve

Corhy., nerve to coracohyoideus S. ant, nerve to serratus anterior Dep., nerve to depressor muscles S. p1-of., nerve to serratus profundus D. seap., dorsal scapular nerve So., somite

Dors., nerve to dorsalis scapulae Stcor., nerve to sternoeoracoideus Dors.rm., dorsal rami Sscap., supraseapular nerve Hypobi-., hypobranchial nerve Subcl., subelavian nerve

Inf. t}.-or., inferior thoracic nerve Subs., subscapular nerves

L. dor., nerve to latissimus dorsi Supcon, nerve to supracoracoideus Lev., nerve to levator muscles Thord., thoracodorsal nerve

L. scap., nerve to levator scapulae U., ulnar nerve

fl ‘ n\\ 4 5

.4 1 "‘ N ‘.1 I 6 I f-__ { .’.\ A30.

ADD. A B

Fig.1 A, embryo of Squalus acanthias (X 6). B, plexus of S. acanthias. 280 RUTH A. MILLER AND s. R. nnrwrnnn

(’20) of the elasmobranch; and by Vogt and Young (1894), Fiirbringer (1897), and Herrick (1899) of the teleost.

The following results were obtained for the two phases of the present work.

I. Elasmobranch (fig. 1)

A. The fin rudiment is a narrow fold, which arises immediately behind the gill region. It extends caudally above the yolk stalk and is lost with the developing somites. Its anterior origin may be fixed at somite 3; it extends posteriorly to the vicinity of somite 13.

B. The brachial plexus is composed of nerves from the third to thirteenth spinal segments. The hypobranchial nerve, which is formed of the occipitals and first two spinals, sends a small branch to the plexus.

II. Teleost (fig. 2)

A. The fin fold is a ridge-like swelling just caudal to the gill region above the heart. ‘It is placed opposite somites 1 to 3 or 4 ; the swelling is most pronounced at 2 and 3.

B. The adult plexus comprises spinal nerves 1 to 3. Nerve 3 sends no directbranch to the trunks of the other two components, but communicates with them through the terminations within the fin muscles. The hypobranchial nerve, which is composed of a hypoglossal root and contributions from the first two spinals, has no communication with the muscles supplied by the plexus.

III. Amphibian (fie. 3)

A. In the urodele the forelimb rudiment is a globular swelling in the region of the pronephros, opposite somites 3 to 5 (in Harrison’s stage 36). It is a welldefined rounded mass, easily distinguished from the body wall.

B. The first spinal root of the adult arises immediately posterior to the vagus complex; occipital nerves are lacking. The first two nerve roots contribute to the hypoglossal (hypobranchial) nerve. The brachial IJDRS.RM.


Fig. 3 A, embryo of Amblystoma punctatum (X 11). B, plexus of A. punc tatum. plexus is formed of nerves from the third, fourth,iand fifth spinal segment. IV. Reptile (fig. 4) A - .

A. The forelimb bud is an ovoid prominence dorsal to the heart. Its rise is so gradual that the cranial and caudal limits are not clearly defined. The point of greatest Width, however, is opposite the seventh, eighth and ninth somites, so that the bud may be said to arise between the sixth and tenth.


Fig.4 A, embryo of Sceloporus undulatus (X 12.5). ‘B, plexus of S. undulatus.

Fig.5 A, embryo or Gallua domesticus ()<12.5). B, plexus of G. domesticus.


B. The brachial plexus is composed of the sixth to the tenth spinal nerves inclusive. The cervical plexus, of nerves 2 to 5, is separate from the occipital roots and the first two spinals, which form the hypoglossal

nerve.


Fig.6 A, embryo of Mus musculue (X 14). B, plexus of M. musculus.


Fig. 7 A, embryo of’ Mus norvegicus (X 11). B, plexus of M. norvegieus.

V. Bird (fig. 5)—Gal1us domesticus

A. The pectoral limb rudiment is a gradually rising prominence situated posterior to the heart. As in the reptile, the extent of the bud is not definitely delimited. The structure is located in the region between somites 13 and 18 and attains its greatest width opposite 14, 15 and 16.


Fig. 8 A, embryo of Lepus euniculus (X 12.5). B, plexus of L. eunieulus.


Fig.9 A, embryo of Felis domestica (X 9). B, plexus of F. domestica. ORIGIN AND DEVELOPMENT 019 BRACHIAL PLEXUS 285

B. The upper spinal nerve roots are arranged similarly to those of the reptile, with a distinct cervical plexus. The brachial plexus is formed of nerves 13 to 17.


Fig. 10 A, embryo of Sue: serofa (X 11). B, plexus of S. scrofa.


VI. Mammal (figs. 6 to 11)

A. The forelimb bud is situated at approximately the same level in the various orders of mammals. It arises in the region caudal to the heart and above the liver, opposite somites 4 to 10. The rudiment is formed similarly to that of the reptile and bird, without clearly defined boundaries.

B. The first three or four spinal nerve roots enter into the formation of the cervical plexus, conforming to the general plan for the higher vertebrates, which is followed by the reptile and bird. In the mammal the occipital segments are incorporated into the cranial series and oifer no complications to the dissection of the adult form. The brachial plexus is composed of nerves arising from the fourth to the ninth spinal roots. Some species vary slightly from this arrangement. The following list gives the ‘normal’ number of nerves for the forms studied. Individual variations within the species are extremely common.

Mouse 4 to 9 (fig. 6 B) Rat 5 to 9 (fig. 7 B) Rabbit (4) 5 to 9 (fig. 8B) Cat 6 to 9 (fig. 9 B) Pig (4) 5 to 10 (fig. 10 B)

Human (4) 5 to 9 (fig. 11 13)

Discussion

The results of the anatomical investigations listed above confirm those of Lehmann and Detwiler which were obtained experimentally in Amphibia. The conclusions emphasize the fact that nervous segmentation depends primarily upon the segmentation of the mesodermal somites. There is a close correlation between the body segments and the nerves of each segment, regardless oftheir destination. There exists also anintimate rcla-tionship between the somites, the corresponding nerves, and the extremity which is supplied by these nerves. This was proved experimentally in the amphibian embryo by Detwiler. The present research deals with the problem of the relation between the position of the limb rudiment and its segmental nerve contribution from the standpoint of comparative anatomy. The results show that the nerves which make up the brachial plexus correspond segmentally to the somites beneath which the embryonic forelimb bud lies.


Several interesting inquiries are suggested by the observations just described. Chief among these is the question of the origin of the forelimb musculature of the higher vertebrates. In the lower forms, where the muscles of the fin folds arise from myotomic buds, a segmental nerve accompanies each bud; in consequence, the number of nerves in the adult plexus corresponds with the number of somites contributing buds to the fin. The limb musculature of the higher vertebrates, however, has been proved in a. number of forms to arise in situ from the somatopleural mesoderm, whereas the myotomic processes contribute to the muscles of the body wall. No attempt will be made here to enumerate the results obtained by the many workers in this field. Byrnes (1898) and Lewis (’02) have given able summaries of the earlier re— searches. Opinion is unanimous that in the elasmobranch the musculature of the pectoral fin originates from myotomic buds, as was demonstrated by Balfour, Mollier, and Braus. Harrison proved conclusively that the pectoral fin musculature of teleosts arises from somatopleure and not from myotomes. In the‘Amphibia, Byrnos (1898), and later Lewis (’10), Harrison (’15), and Detwiler (’18) established the fact that the muscles of the anterior extremity are formed from somatopleure. Corning was finally convinced that the forelimb musculature of reptiles arises from unsegmented mesoderm, but other investigators, notably Mollier, van Bemmelem, Sewertzoff (’07), and Goodrich (’30) observed muscle buds growing into the limb rudiment from the myotomes. In the bird, Paterson found proof that the musculature of the fore« limb is formed from somatopleural mesoderm; Fischel believed that, although the rudiment does not receive definite myotomic buds, cells from the myotomes are found in the limb region. In regard to. the Mammalia, opinion is generally against the presumption of a direct myotomic origin for the muscles of the anterior extremity. The work of Bardeen and Lewis, and the embryologies of Keibel and Mall and Arey show that the forelimb musculature arises from unsegmcnted mesoderm and that the myotomes contribute 011ly to the trunk muscles. Other workers, however (Kollman, 1891; Ingalls, ’07 ; and Zechel, ’24), have observed myotomic proliferations into the forelimb bud of the human embryo.


The results of the above observations show a definite correlation, throughout the higher vertebrates, between the metamerie position of the limb bud and the segmental nerves supplying the extremity This relation, however, cannot be regarded as proof of the myotomic origin of the limb musculature. Experimental evidence points strongly to the contrary. Detwiler (’34), working upon the amphibian embryo, produced functional limbs in the complete absence of brachial somites. Function was made possible by the innervation of the extremity through spinal nerves, ' which reached their destination without the guidance of the metameric structures. Lack of somites caused irregularities in the number of nerves and in their segmental pattern, but did not affect their growth to the limb. These experiments demonstrate that the development and innervation of limb musculature can take place independently of the myotomes. _


Another interesting consideration, which should be included in the present discussion, is that of muscle-nerve relationship. The seeming ‘attraction’ of muscles for certain nerves is a subject which has been discussed from time to time. Numerous experiments have been performed to ascertain the reason for specific nerves supplying certain structures, especially the extremities. Harrison ( ’07), by means of experiments involving limb transplantations in amphibian embryos, showed that the growing limb exerts a certain influence upon the number of spinal nerves supplying it and upon the direction of nerve growth within the limb. In a series of transplantation experiments Detwiler (’20, ’22) emphasized the influence of the limb upon the source of its nerve supply and demonstrated the tendency of brachial nerves toreach the extremity when the latter is moved short distances from its normal position. Numerous theories have been advanced to account for the phenomena of the growth of nerves and their ultimate connection. These have invoked the influence of electrical, chemical, and mechanical forces (Detwiler, ’34, ’36).


The problem of nerve—muscle connection may be considered as taking placeunder the influence of different forces, 1) those which are responsible for the direction of growth. of the nerves and 2) those which are more specifically concerned with the final connection of the nerves with their muscles. '

1. The influence of mechanical forces in guiding the nerves was first stressed by His in his Outgrowth Theory. It Was further emphasizedexperimentally by Harrison. Weiss ( ’34), who grew embryonic nerve tissue in vitro, was able" to make the growth of the nerve fibers conform to various structural organizations created in the plasma medium. He interprets his results as showing that the course of nerve growth is dependent upon the mechanical organization of "the environment. In experiments upon the embryo the mechanical theory offers an explanation for the atypical growth of nerves to grafted structures (e.g., limbs, optic cups, nasal placodes). Under the influence of the proliferating center, structural pathways are established in the embryonic ground substance which serve as mechanical guides for the growing nerves.

2. The final connection of a nerve with its muscle may involve a more specific force than the one concerned in directing the growth of the nerve toward the periphery. Proliferating muscle fibers exert a certain influence upon the nerves growing toward the muscle primordium until connections are made. When a muscle has received its nerve supply, its susceptibility for further innerv'ation,presumabl.y ceases. The forces involved in the phenomenon of ultimate nerve—muscle connec— tions have not yet been satisfactorily determined.

After nerve connection with the limb rudiment has been made, the type of plexus which is formed depends upon the segregation of the limb musculature. Harrison (’07) observed that the developing structures follow Nussbaum’s law, which states that the direction of nerve branching within a muscle is an index of the direction in which the muscle has grown. Harrison’s experiments were conducted upon amphibian embryos at stages when the nerves had already reached the periphery. His findings were verified by Detwiler (’20) who Worked upon stages prior to nerve outgrowth. Rogers (’33) implanted a supernumerary brachial region of the spinal cord between the normal cord and the forelimb rudiment. Regardless of the number of segmental nerves entering the limb from the grafted cord, the pattern within the limb was a normal one, if the limb developed normally.

Comparative anatomical studies by Miller ( ’34) show that the arrangement of the peripheral portion of the brachial plexus is determined by the size, position, and relativeiimportance of the muscles which are supplied by it.‘

Conclusions

Comparative embryological and anatomical studies have been made upon eleven different species, representing five classes of vertebrates. The segmental position and extent of the forelimb rudiment of the embryo in the ‘bud stage’ (before penetration of the nerves) were ascertained by gross observation and by study of microscopic sections. In adult forms of the species, the segmental levels and the number of nerves entering into’ the brachial plexus were determined by dissection. In all cases studied the pleurisegmental origin and number of nerves contributing ‘to the adult plexus corresponds to the location and cranio—caudal length of the embryonic limb bud.

‘The results of these earlier studies are further emphasized by the plexuses which are illustrated in the present study. These show a series of nerve patterns increasing in complexity as the limb, which they supply, becomes more complicated in structure and function.


Literature Cited

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Cite this page: Hill, M.A. (2024, March 19) Embryology Paper - Comparative studies upon the origin and development of the brachial plexus. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_Comparative_studies_upon_the_origin_and_development_of_the_brachial_plexus

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