Paper - The development of muscle in the human foetus

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Hewer EE. The development of muscle in the human foetus. (1927) J Anat. 62(1): 72-8. PMID 17104172

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This historic 1927 paper by Hewer describes fetal skeletal muscle development.


Also by this author - Hewer EE. The development of nerve endings in the human foetus. (1935) J Anat. 69(3):369-79. PMID 17104543


Modern Notes: skeletal muscle

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The Development of Muscle in the Human Foetus

By Evelyn E. Hewer

Lecturer in Histology and Assistant Lecturer in Physiology at the London (Royal Free Hospital) School of Medicine for Women


The histogenesis of muscle in the human has not, as far as the author is aware, been hitherto described in detail, although the process has been followed in considerable detail in certain other mammals. Thus McGill (1) gives a full account of the development of smooth muscle in the pig, the process being similar to that described below. The histogenesis of striped muscle has been described by many workers, including Godlewski (2) (puppy, mouse, rat, guinea-pig), Bardeen (3) (pig), MacCa1lum (4) (pig, man), Schaffer(5) (various vertebrates); from these writers it is by no means clear whether the original myoblasts fuse to give rise to a syncytium, or whether each muscle cell arises from one myoblast that elongates with division of the nucleus (6). The development of cardiac muscle has been described by Retzer(7) (pig) and by MacCallum (8) (pig) and also by Tandler(11).


The present account is based on an investigation of human material only; it is incomplete in that the earliest embryo available was one of 10 mm., and also in that variations in the cardiac muscle of the different parts of the heart and the tracing out of the auricular-ventricular bundle (see Retzer(7) for pig) has not yet been done; it is hoped to make these points the subject of a later communication. The following is a description of the general appearances characteristic of various stages of development in the human: the interpretation of these appearances is not attempted.


The determination of the age of an early embryo is very difficult, the length of the embryo probably giving the best means of comparison: the ages given below have been determined during a systematic and comparative investigation of the general development of these embryos that Professor Lucas Keene and the writer are now engaged upon. The ages of older foetuses have been determined from the history, ossifications, and general post-mortem findings.

(A) STRIPED MUSCLE

The voluntary muscle is developed from mesoderm which is early set aside for this purpose (9). In two human embryos of 10 mm. and 12 mm. respectively no differentiation of cells for this formation could be detected: in an embryo of 25 mm., however, among the branching general mesoderm cells could be seen quite clearly some elongated cells with long nuclei. These cells are found in the regions later occupied by the back muscles of the lumbar region, and represent the beginning of differentiation of mesoderm cells into striped muscle cells. Even at this early stage the cells differ in size; this can best be seen in cross sections of the cells, the centre being occupied by either nucleus or non-staining protoplasm. The nuclei of these cells then begin to ‘divide, and at six weeks many cells show two nuclei and sometimes as many as four or five. The cells stand out from among the general connective tissue cells by virtue of their large ,amount of granular and strongly eosinophil cytoplasm.



fig. 1. Human embryo, aged about 7 Weeks. Beginning of differentiation of striped muscle cells. Some cells already contain two nuclei and at this stage are nearly spherical.



can be seen in some cells.

section.

At eight weeks (30-40 mm.) there is marked differentiation actually Within these cells. The multinucleated cells have become larger, and the row of nuclei in the centre of the cell is embedded in a zone that does not stain but contains highly-refracting granules: outside this zone is the eosinophil cytoplasm that is now showing Well-marked fibrillation in parts of the cells and also some cross striation. The cytoplasm which is being differentiated into contractile substance gives a curious staining reaction with Mallory’s connective tissue stain: the nuclei are usually stained purple-red With an orange nucleolus, and the developing contracting substance either blue or orange or often mixed blue and orange. This possibly indicates a chemical modification, as fully differentiated muscle gives a uniform orange staining. The cells at this stage are said to be rich in glycogen.


fig. 2. Human embryo, aged about 8 Weeks. Striped muscle cells further difierentiated. Cross striations Note central row of nuclei. The cells are in the region corresponding to fig. 1. a, cell in cross section; b, cell in longitudinal


As growth proceeds the fibrillation and cross striation gradually become more marked, and involve the whole fibre with the exception of the central row of nuclei with the surrounding undifferentiated protoplasm. At twenty-two weeks the nuclei are taking up their permanent position. In a preparation from a foetus of this age some of the muscle fibres present an appearance very similar to that seen when fully developed, with nuclei beneath the sarcolemma, the cross sections of the fibres being however considerably smaller than they are at birth. Among these fibres, however, there are still to be found others of the embryonic type, with central nuclei surrounded by unstained undifferentiated protoplasm, showing fibrillation in the periphery of the cell only, very similar to the type of cell forming the Purkinje tissue of the heart. This embryonic type of fibre was not found among the striped muscle cells after the 26th week of foetal life.



fig. 3. Human embryo, aged about 22 weeks. Note nuclei of muscle cells either in the centre or at the periphery. The cells are in the region corresponding to fig. 1. a, cell in oblique section; b, cell in transverse section, with central nucleus; 0, cell in transverse section, with peripheral nucleus.


At full time the striped muscle resembles exactly that of full development, except that the fibres are actually smaller. The variation in size of individual fibres as seen in cross section in the fully developed condition is present from the very beginning, as will be seen from the diagrams.


The developing muscle is richly supplied with blood vessels as early as six weeks. The ingrowth of nerve fibres has not as yet been studied in detail, but takes place at a very early stage of development. A delicate membrane is said to appear about the 8th week, but a real sarcolemma is difficult to demonstrate. By a modified silver nitrate method, whereby the sarcolemma can be demonstrated in fully developed muscle, this structure has been distinguished in muscle from a foetus of 24: Weeks. . MacCallum (4) notes the appearance of a single row of fibrils round the periphery of the cell in embryos of '7 5 mm. and 102 mm., and the nuclei nearly all peripheral in embryos of 170 mm. At an early stage of development there is said to be a degeneration of some of the developing fibres, and a formation of new ones by longitudinal splitting of the remainder; this process was not observed in the preparations available.


fig. 4. Human embryo, aged about 7 weeks. Small intestine in cross section, showing unstriped muscle in transverse and in longitudinal section (compare fig. 5).


fig. 5. Full-time human foetus. Unstriped muscle of small intestine. The growth of the cells is shown by the relative diminution in the number of nuclei.


I The foregoing is an account of the development of the muscle cells in the lumbar region of the back: the muscle cells are formed in a similar Way in other regions of the body.

(B) UNSTRIPED MUSCLE

Unlike striped muscle, which arises from easily distinguishable cells that are early marked out for this purpose, unstriped muscle may arise from mesoderm cells in very various situations, and possibly also from ectoderm. These cells, which usually have an irregular and branching form and a round nucleus, elongate, and the nucleus becomes drawn out although remaining rounded at the poles. In an embryo of 10 mm. these were distinguished as long cells that were arranging themselves quite definitely round the lumen of the developing gut and of the larger blood vessels: the latter are extremely thin Walled, and it is difficult to be certain whether these cells are actually developing muscle cells or only undifferentiated cells of the surrounding mesoderm. In a 12 mm. embryo these long cells with elongated nuclei can be found in almost all the situations Where unstriped muscle will ultimately appear, being seen at this stage most clearly in the walls of the large blood vessels, of the alimentary tract, of the uterus and of the ureters. At six weeks these cells are lying parallel with one another, so forming definite sheets of muscular tissue in the walls of the various tubes. As development proceeds the cells acquire rather indefinite longitudinal striations and elongate to such extent that the number of nuclei seen in a given area of a section are less numerous (see diagrams).

The development of the unstriped muscle coats does not occur simultaneously in all the organs. Thus, at eight weeks, the longitudinal and oblique muscle fibres of the bladder Wall are easily distinguishable but not the circular ones: in the gut the longitudinal muscle coat is more advanced in its stage of development than the circular coat in both small and large intestine, Whereas in the oesophagus and in the stomach the muscle coats appear to develop at corresponding rates: the muscularis mucosae does not appear as a distinguishable layer until about 12 Weeks. Again, at eight Weeks the unstriped muscle of the trachea is Well developed, but there is none in the bronchioles until about 11 weeks.

At full time the unstriped muscle resembles in appearance that of an adult, except that the cells are less elongated, and the nuclei more rounded, than they appear later.

(C) CARDIAC MUSCLE

Although the heart itself is early differentiated yet the adult type of cardiac muscle is not developed for some time. In an embryo of 10 mm. the heart tissue was found to consist of an open branching network of minute fibres, with many large round nuclei frequently showing mitosis. No striation could be detected in the fibres, and the appearance was that of a syncytium rather than that of definite cells. The same arrangement can be made out in slightly older embryos, and the appearance is that given by Tandler(11) for Keibel’s Normentafel N o. 27; at about eight weeks (or between 30 and 40 mm.) definite cross striations can be made out in some of the fibres. The nuclei are now spherical or ovoid, and lie in the faintly staining protoplasm in which are running many fibres. These fibres tend to run in groups parallel with one another, the individuals running first with one group and then breaking away to join an adjacent group. The nuclei in some cases appear somewhat elongated as if pressed among the fibres, but more frequently they lie in more open spaces between the groups. As differentiation proceeds the fibres become more strongly eosinophil. At first sight one might think that the fibres really represent cell boundaries, but acareful examination of the relation between the nuclei and the fibres as seen in transverse and longitudinal section shows that some at least of the fibres are of far greater length than would correspond to the cells. (Mallory’s connective tissue stain after formalin fixation brings out these features more clearly than any other method tried.)


By 11 weeks development of a few transverse “cell boundaries” can be seen. The fibres, in which striation is more clearly seen than at ten weeks but is still far from universal, run parallel with each other, and arrange themselves loosely in groups, any one fibre attaching itself to several groups in succession. The nucleus is often surrounded by faintly staining undifferentiated protoplasm which appears continuous with that between the fibres. The whole tissue is very richly supplied with capillary vessels.


As development proceeds the cross striated fibres become more general, but the nuclei still retain the surrounding zone of undifferentiated protoplasm. The fibres gradually become more closely packed together, and the nuclei become rather more drawn out and elongated. At 16 weeks the cross striations are further apart than they are a few weeks later, and are not yet present in all the fibres.

By 20 weeks the continuity of the fibres for comparatively long distances can be clearly seen, but the transverse cell boundaries are still rare; the cross striation of the fibres has now become universal.

The individual fibres gradually increase in thickness, and the nuclei tend to become more elongated, and thus the fully developed type is finally reached. The nucleus often retains a small surrounding zone of undifferentiated protoplasm, and a general appearance of .“ cells ” may be given by the way in which the fibres arrange themselves in groups, and by the so-called cross “ cell boundaries ”; according to Krause(10) these latter are to be regarded as of the nature of discs interpolated on the course of a bundle of fibres. The yellow pigment frequently associated with the nucleus in later life has not been seen in foetal material.

Conclusions

In the human foetus it was found that of the three types of muscle the unstriped is the first to develop, being clearly defined in an embryo of 10 mm., and is also the one that shows the least subsequent differentiation. The striped muscle begins to differentiate at about 25 mm., but the development is slow and the adult type is not found until about 22 weeks. The cardiac muscle is differentiated probably before 10 mm., but striations were not clearly seen until between 30 and 40 mm. (eight weeks).


This special piece of work was undertaken during the course of an inVestigation on the human foetus that is being carried out jointly with Professor M. F. Lucas Keene, and for which we beg to acknowledge a grant from the Thomas Smythe Hughes Medical Research Fund of the University of London. I also have to thank the Medical Research Council for a grant.

References

(1) MCGILL (1907). Intern. Monatschr. Anat. u. Morph. Bd. XXIV, p. 209.

(2) Gonmnwsxr (1902). Arch. f. milcr. Anat. Bd. LX, p. 111.

(3) BARDEEN (1900). Johns Hopkins Hosp. Rep. IX, p. 367.

(4) MACCALLUM (1898). Johns Hopkins Hosp. Bull.‘ p. 208.

(5) SCHAFFER (1893). S. Ber. cl. Acad. d. Wiss. Wien. 3. Abt. Bd. CII, p. 7.

(6) KEIBEL and MALL (1912). Manual of human embryology, pp. 534-569.

(7) RETZER (1908). Anat. Record, vol. II, p. 149.

(8) MAOCALLUM (1897). Anat. Anzeig. Jena, Bd. XIII, p. 609.

(9) SCHAFER (1912). Microscopic Anatomy, p. 192.

(10) KRAUSE (1913). Normal Histology, Part II, p. 110.

(ll) TANDLER (1912) in Keibel and Mall. Human Embryology, pp. 543, 554.



Cite this page: Hill, M.A. (2024, March 19) Embryology Paper - The development of muscle in the human foetus. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_The_development_of_muscle_in_the_human_foetus

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