Human Embryology and Morphology 27

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Keith, A. Human Embryology And Morphology (1921) Longmans, Green & Co.:New York.

Human Embryology and Morphology: 1 Early Ovum and Embryo | 2 Connection between Foetus and Uterus | 3 Primitive Streak Notochord and Somites | 4 Age Changes | 5 Spinal Column and Back | 6 Body Segmentation | 7 Spinal Cord | 8 Mid- and Hind-Brains | 9 Fore-Brain | 10 Fore-Brain Cerebral Vesicles | 11 Cranium | 12 Face | 13 Teeth and Mastication | 14 Nasal and Olfactory | 15 Sense OF Sight | 16 Hearing | 17 Pharynx and Neck | 18 Tongue, Thyroid and Pharynx | 19 Organs of Digestion | 20 Circulatory System | 21 Circulatory System (continued) | 22 Respiratory System | 23 Urogenital System | 24 Urogenital System (Continued) | 25 Body Wall and Pelvic Floor | 26 Limb Buds | 27 Limbs | 28 Skin and Appendages | Figures

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Chapter XXVII. Morphology Of The Limbs

In the previous chapter the chief events connected with the development of the limb buds in the human embryo have been noted and incidentally certain points relating to the morphology — primitive structure — of the limbs have been alluded to. In the present chapter we propose to deal with the more important problems relating to the pectoral and pelvic girdles, to the bones of the hand and foot, to the origin of joints and to the significance of certain muscular modifications.

Congenital Elevation of the Shoulder

We have already seen that the arm of the human embryo is cervical in position — in this respect resembling the pectoral fins of fishes. It descends during the 2nd month, reaching its final position over the ribs in the 3rd month. Its descent is not only accompanied by an elongation of the brachial nerves, but also by a downward migration of certain muscles — originally placed in the neck — trapezius, serratus magnus, latissimus dorsi and pectoral muscles. The descent may be arrested. The condition, which is not rare in children, is often accompanied by irregularities in the formation of the cervical vertebrae — for the elongation of the cervical region to form a neck is related to the descent of the shoulder, of the heart, and of the diaphragm — and with the appearance of a skeletal element of the shoulder girdle which is present in certain fishes (dipnoi and selachians). This omovertebral element is represented in Fig. 463 — from the classical case of Willet and Walsham (1880). In fishes this bone joins the supra-scapula to the occiput ; when it appears in man it is usually fixed to, or articulates with, the spinous processes of the lower cervical vertebrae. Man's upright posture has thrown the duty of constantly supporting the shoulder on the trapezius. Under certain circumstances it gives way, the shoulders then drooping. Symptoms may then arise from pressure of the nerves against the 1st rib — or a cervical rib.^

Pelvic and Shoulder Girdles

In the basal part of each limb bud a cartilaginous arch is developed. It consists of a dorsal and ventral part, the joint cavity for the articulation of the limb being situated at the junction of the two parts. Fishes retain this simple primitive form of girdle.

File:Keith1921 fig463.jpg

Fig. 463. The Omo-vertebral Bone in a Case of Congenital Elevation of the Shoulder.

^ The condition is often spoken of as SprengeVs shoulder. See H. A. T. Fairbank, Brit. Med. Journ. 1911, ii. p. 1533. For recent literature see D. M. Greig, Edin. Med. Journ. 1910, vol. 5, p. 236 ; 1911, vol. 6, p. 242.

The pelvic girdle has undergone less modification from the primitive type than the shoulder girdle. The primitive type of pelvic girdle, such as is seen in the crocodile or lizard, and of which the mammalian type is a derivative, is shown diagrammatically in Fig. 464. For comparison the human girdle in the 7th week foetus is shown in Fig. 465.

Fig. 464. Diagram of the Pelvic Girdle of a Lizard.

The dorsal element consists of the ilium ; it is attached by ligaments to the costal process of one or more sacral vertebrae. In the ventral portion of the mesenchymal arch are developed two cartilaginous elements the pubes and ischium, both of which take part in the formation of the acetabulum (Fig. 464). Both reach the ventral median line in which a median bar of cartilage is developed (see Fig. 442).

In man the following changes may be noted : (1) The costal processes of the sacral vertebrae (2| usually) have fused together to form the lateral sacral mass ; with these the ilium articulates (Fig. 451) ; (2) the vertebral border (crest) has become enormously elongated and gives attachment to abdominal muscles, cutting ofi the fibres of insertion of the external oblique which form the chief part of Poupart's ligament ; (3) the ischium does not reach the ventral line. In most birds, neither ischium nor pubis reaches the ventral line. The pubes fail to meet in cases of ectopia vesicae, just as the sternum is cleft in cases of ectopia cordis. The symphysis pubis is formed in the ventral line during the 3rd month. The cotyloid bone — OS acetabuli — is formed in the Y-shaped cartilage between the three elements. It ossifies in the ISth year. Professor Howes has pointed out that it is this ossification which forms the pubic part of the acetabulum, and that it is really part of the pubes.

1 Prof. T. W. Todd, Anat. Anz. 1912, vol. 41, p. 385.

The median pelvic bar corresponds to the sternum, and like it is of bilateral origin. In reptiles (Fig. 442) it is divided into anterior, middle and posterior parts. The anterior parts form the cartilaginous epiphysis of the pubic crest, which represent the marsupial bones, and correspond to the supra-sternal ossifications ; the middle parts become the cartilaginous surfaces of the symphysis ; the posterior parts (the hypoischium of reptiles) form the epiphyses on the pubic arch and ischial tuberosity (Parsons).

Congenital Dislocation of the Hip Joint

Under this title two quite different groups of cases are included : (1) cases in which there has been an arrest of development of the parts entering into the formation of the hip joint ; (2) cases which are produced during the act of birth. It is only the first group which is referred to here. In the 8th week — when the foetus is about 20 mm. in length, the three cartilaginous elements — ilium, ischium and pubis — meet in a Y-shaped acetabular suture, the pubic element being later in chondrifying than the other two. In the 9th week the hip joint is formed by (1) the appearance of a synovial cavity, (2) cartilaginous outgrowths from all three elements, but especially from the iliac — ^to form the acetabular cup ; (3) the separation of the head from the shaft of the femur by the formation of the neck (see p. 429). The joint is completely formed early in the 3rd month. The synovial lining of the joint arises from an ingrowth of peripheral cells into the blastemal tissue between the acetabulum and head of the femur (Jenkins ^). The outgrowth of the acetabular brim may be arrested at the reptilian stage reached in the 2nd month ; congenital dislocation of the femoral head, which is fully formed, results. In the cases of cleft palate and imperforate anus (and tMs is a similar case) human development is arrested at a reptilian stage. The condition has an obscure relation to the development of the female sexual characters ; 90 % of cases occur in female infants.

Fig. 465. The Pelvic Girdle of a Human Foetus at the 7th week. (After KoUmann.)

^Prof. T. W. Todd, Amer. Journ. Physic. Anthrop. 1920, vol. 3, p. 285 (age changes in pubic bone).

" G. T. Jenkins, Brit. Med. Journ. 1906, vol. 2, p. 1702.

Shoulder Girdle

The duckbill (ornithorhynchus) shows the most generalized type of mammalian shoulder girdle ; it resembles closely the primitive reptilian type ; from such a form the various types of mammalian shoulder girdle were probably evolved.

The dorsal part of the arch consists of (1) scapula, (2) supra-seapula (Fig. 466). The supra-scapula is represented in man by the cartilage along the vertebral border ; it ossifies in the early years of manhood. The supra-spinous part of the scapula appears first in higher mammals ; it is produced late in the development of the scapula (in the 3rd month of foetal life) by the upgrowth of the supra-spinous blade of the scapula ; it is not represented in the pelvic girdle. The dorsal segment of the pelvic girdle becomes fixed to the costal processes ; the corresponding part of the scapula remains free.

Fig. 466. The Shoulder Girdle of Ornithorhynchus.

In the typical reptilian shoulder girdle, as in the pelvic (Fig. 464), two elements are formed in the ventral part of the arch — a posterior part — the coraeoid, corresponding to the ischium, and an anterior — the precoracoid, corresponding to the pubes.^ Both elements reach the ventral median line in which the sternum is developed (p. 419). In ornithorhynchus the coraeoid element is represented by two bones — the coraeoid and epicoracoid — the second of which is formed from the anterior end of the sternal bar and therefore corresponds to the suprasternal ossification of man.

^ I have repeated the statement made in former editions, but the reader will perceive if the mirror-image correspondence is true (p. 430), that the ischium on the distal side of the pelvic girdle corresponds with the coraeoid on the proximal side of the shoulder girdle — as stated above — but the representative of the pubis should be on the distal — not on the proximal side of the shoulder girdle as the clavicle is placed. I am convinced that there is no pubic representative in the shoulder. Developmental phenomena show that the clavicle is a new formation. Dr. D. M. S. Watson (reference p. 425) has shown that in the evolutionary history of the shoulder girdle the precoracoid is the first element to reach the mid ventral or sternal line and that later it is supplante d by the coraeoid element. He regards the epicoracoid of ornithorhynchus as corresponding to the precoracoids of amphibia.

The dorsal extremity of the coracoid helps to form the glenoid cavity ; its ventral articulates with the presternum. In man and all higher mammals, in which mobility of the fore limb is of advantage for speed and free movement, the coracoid element is much reduced. It forms merely a process on the scapula, which it joins in man about the 15th year. It still enters into the formation of the glenoid cavity, the articular part (supra-glenoid) having a separate centre of ossification which appears in the 12th year. It is possible that the costo-coracoid ligament may be derived from the ventral part of the coracoid element — the part which articulates with the sternum in the duckbill. The precoracoid in the shoulder girdle of a lizard corresponds to the pubic element in the pelvis. The precoracoid, which, like all the primitive elements of the pelvic and shoulder girdle, is formed in cartilage, has been partly or entirely replaced in all mammals by the development over it of the clavicle, a dermal or membrane-formed bone, the first of all the bones to ossify. There is thus no true representative of the clavicle in the pelvis. The interclavicle so strongly developed in the ornithorhynchus and in the " merry-thought " of the fowl is also a dermal bone. It is represented in man by the interclavicular ligament.

Fig. 467. The Parts in the Shoulder Girdle of a Human Foetus which correspond with those of Ornithorhynchus.

In order to give greater mobility and speed to some four-footed mammals, the clavicle has been reduced to a ligamentous band, except at its extremities (rabbit, dog, etc.). In climbing animals, and those in which the power of grasping or embracing is highly developed, the clavicles are fully developed.


At the beginning of the 7th week the clavicle is represented by a cellular or blastemal bar passing from the neighbourhood of the acromial process of the scapula to end ventrally in the anterior end of the sternal blastema. Professor Fawcett found that during the 7th week, when the embryo is 15 mm. long, two centres of chondrification appear in the clavicular blastema, quite close to each other, one corresponding to the termination of fibres of the sternomastoid, the other to the ending of fibres of the trapezius. Before proper cartilage has had time to form centres of ossification appear in the adjacent margins of the two precartilaginous masses, the two ossific centres uniting in a few days. From this double centre ossification spreads during the 8th week towards the sternum and towards the acromion, ossification being preceded by a true formation of cartilage.

^ For development of clavicle : Prof. E. Fawcett, Journ. Anat. 1913, vol. 47, p. 225 ; Pr. N. C. Rutherford, ibid. 1914, 48, p. 355 ; for sexual characters Prof. F. G. Parsons, ibid. 1917, vol. 51, p. 71.

There is a malformation of the clavicle which throws light on its double nature. In the remarkable disorder of growth known by the cumbersome name of cleido-eranial dysostosis ^ the clavicle is made up of two parts — an outer and inner, united by a fibrous band which may form only a short ligament, or may even represent the middle two-thirds of the bone. In such cases all the bones of the skeleton which are formed in membrane — especially those of the cranial vault — are imperfectly ossified. The condition in this disease suggests that the clavicle is a compound bone made up of outer and inner elements, and that arrest has occurred before the two elements have become joined. In cleido-eranial dysostosis some condition occurs which arrests the union of the two ossific centres ; as ossification in cartilage proceeds normally in such cases we may presume that in spite of the appearance of cartilage in the clavicle, it was originally a membrane bone.

Fig. 468. The Carpal Bones of a Tortoise.

The acromion process is ossified from several centres which appear in the years of adolescence ; the epiphysis so formed may be united to the spine by fibrous tissue only. This occurs in over 8 % of subjects (Symington), and may be mistaken for a fracture of the process. The coracoclavicular ligaments may be derived from the precoracoid element.

Hand and Foot

The hand and foot of man, as is the case in all primates, retain the primitive arrangement of elements much more closely than do most other mammalian orders. The primitive type of hand or foot, out of which the various forms found in mammals have been modified, are seen in such reptiles as the lizard or tortoise (Fig. 468). In the hand of man the same bones are to be seen as in the tortoise, and in the same order of arrangement, with some exceptions. The elements in the foot of a typical lizard resemble closely the arrangement seen in its hand ; the same elements are present even in the highly modified human foot. The hand and foot bones have undergone great specialization in most mammals. In the evolution of the horse, for instance, one lateral digit after another has become vestigial, leaving the central digit enormously enlarged and specialized to form the lower part of the extremities. In ruminants the 3rd and 4th digits have become predominant ; the rest of the digits have become reduced until only traces of them are left ; in rodents the hallux is vestigial. The hallux and pollex are the mammalian digits most liable to undergo retrogression. In man, on the other hand, the hallux and pollex find their greatest development.

1 D. Fitzwilliams, Lancet, 1910, vol. 2, p. 1466.

Fig. 469. The Os Trigonum and other Bones of the Tarsus.

Comparison of the Tarsus and Carpus.^ — Both are the derivatives of such a typical form as is shown in Fig. 468. In the typical tarsus or carpus there occur the following bones :

1. Badiale or Tibiale forms the scaphoid in the hand and astragalus in the foot.

2. Intermedium forms the semilunar in the hand ; in the foot it is much reduced and usually unites with the astragalus to form the external tubercle of that bone. It may remain separate and form the os trigonum (Fig. 469).

3. Ulnare becomes the cuneiform in the hand, the os calcis in the foot. During the cellular and early cartilaginous stages in the development of the human tarsus, the os calcis is in contact with the fibula. In the hand the ulnare and intermedium are bound by fibrous bands to the ulna (Fig. 468) ; these bands assist to form the triangular fibro-cartilage ; in the ankle the corresponding bands form the middle and posterior fasciculi of the external lateral ligament.

4. Carpale or Tarsale I. becomes the trapezium in the hand, the internal cuneiform in the foot. In the prehensile foot of apes, the hallucial articular surface is directed inwards for the movable big toe. This is also the case during the foetal development of the human foot (Leboucq). At no period of development is the hallux of man directed inwards and separated from the other toes. In man the great toe resumes a primitive position, and its metatarsal lies in line with the metatarsal series.

1 See note on p. 444 and Fig. 453. Papers on carpal and tarsal bones : see R. B. S . Sewell, Journ. Anat. and Phynol, 1906, vol. 40, p. 152 (Astragalus) ; T. MannersSmith, Journ. Anat. and Physiol. 1907, vol. 41, p. 255 (Navicular of Foot) ; H. M. Johnston, Journ. Ayiaf. and Physiol. 1907, vol. 41, p. 59 (Scaphoid of Hand).

5. Carpale or Tarsale II. forms the trapezoid in the hand, the middle cuneiform in the foot.

6. Carpale or Tarsale III. forms the os magnum in the hand, the external cuneiform in the foot.

7. Carpale or Tarsale IV. and V. have united in both hand and foot to form the unciform and cuboid. This union occurs in all mammals. The unciform process has a separate centre of chondrification (Lewis). In the cat and carnivores the scaphoid and semilunar unite together, a union which may occur in man. In the foot an intimate union persists at the junction of the os calcis, cuboid and scaphoid until late in the 3rd month ; in the cartilage of union a separate tarsal element may develop.^

The Os Centrale is situated between the first and second rows of the carpal or tarsal bones (Fig. 468). In the foot it forms the scaphoid — a bone which plays an important part in the formation of the plantar arch — but is yet remarkably late in beginning to ossify, viz. about the 3rd year. It appears at the end of the 6th week as a separate cartilage element of the human carpus, but at the end of the 2nd month it has joined the dorsal and distal aspect of the scaphoid of the hand. It may be occasionally detected as a tubercle on the dorsal aspect of the scaphoid, or even as a separate bone. It is a separate bone in the carpus of all primates except the gorilla, chimpanzee and man. There are two centralia in lower vertebrate forms. The styloid process at the base of the 3rd metacarpal bone may occur as a separate ossification {os styloideum).

The Pisiform (ulnare laterale of Forsyth Major) is of doubtful nature. It is possible that in a very early stage of the evolution of mammals there were more than five digits — one behind the little finger — post minimi digiti ; and another on the radial side of the hand — a prehallux. Supernumerary digits, when they appear, are commonly situated on the radial side of the thumb or ulnar side of the little finger, but they may represent merely a fission of the normal pollex or little finger. The pisiform has been regarded as the vestige of a post-minimal digit ; the sesamoid on the trapezium, in which a slip of the extensor ossis metacarpi pollicis ends, as a remnant of a prehallux. It is possible also to regard the pisiform as a sesamoid developed in the tendon of the flexor carpi ulnaris — for that muscle is originally a flexor of the metacarpus and ends on the 5th metacarpal — the pisimetacarpal ligament representing the terminal part of the tendon. The pisiform, however, is developed with the rest of the carpal bones and before the tendon of the flexor carpi ulnaris. In mammals generally, but not in man, the pisiform articulates with the ulna as well as the cuneiform, and its synovial facet opens into the wrist joint. It may be represented in the foot by the heel epiphysis of the os calcis. The gastrocnemius, which represents the flexor carpi ulnaris in the leg, is also primitively a flexor of the metatarsus ; the long plantar ligament, from which it is separated by the growth of the heel, represents the continuation of its tendon.

^ For extra carpal and tarsal bones see Pfitzner, Morphol. Arbeiten, 1896, vol. 6, p. 245.

Fig. 470. The Foetal and Adult (in dotted outline) Forms of the Astragalus contrasted.

Eversion o! the Foot and Development of the Arch

The human foot has been highly modified for upright progression. The chief modifications are : (1) Gradual eversion of the foot, so that the sole can be applied to the ground. Even at birth — and for some time after — and always up to and before the 7th month of foetal life, the soles of the feet are inverted, so that when the foetal limbs are in their natural position they are directed towards the belly of the child. In club foot the natural process of eversion does not take place. The ape's foot is kept normally in the inverted position, an adaptation for prehension. The following factors assist in producing eversion :

(a) The neck of the astragalus (Fig. 470), which in the foetal foot is long and directed downwards and inwards at an angle to the axis of its body, becomes relatively shorter and directed more in line with the axis of the articular surface of its body (Fig. 470). Further, the lateral border of the tibial articular surface of the astragalus is prominent in the foetus ; the mesial border is much the lower ; a growth upwards of the mesial border causes the astragalus and foot to rotate outwards (Lazarus).

(b) The bones on the inner side of the foot, particularly the scaphoid and internal cuneiform, grow more rapidly than those on the outer side of the foot — especially after birth. This tends to evert the foot and also to produce the longitudinal arch.

(c) A special evertor of the foot is produced — the peroneus tertius — a muscle peculiar to man. It is developed from the outer and lower fibular fibres of the extensor longus digitorum and represents part of the tendon of that muscle to the 5th toe. The peroneus brevis and longus may also assist, especially the latter, which in apes is a grasping muscle, acting as a flexor of the metatarsal bone of the hallux.

(2) The tarsal bones of the human foot — -especially the astragalus and OS calcis — are of great size when compared with the tarsal bones of other primates ; while the digital or phalangeal elements, except, in the case of the great toe, which is relatively of great size, have undergone retrogression. This is especially the case in the human little toe ; some of its muscles are not infrequently fibrous, and the terminal phalanx may not be separated from the middle phalanx. The terminal phalanx is the last to be differentiated in development of the fingers and toes (in 3rd month).

(3) The plantar arches, both longitudinal and transverse, are produced. The arch of the foot is a human character. At birth the child is flatfooted when the weight of the body rests on its feet ; the head of the astragalus touches the ground. When the muscles are removed by dissection the foot of the newly born child shows a well-developed arch (RusseU Howard). The arch becomes stable as the child learns to walk. The chief factor in its production is the growth of the tarsal bones — especially of the scaphoid and internal cuneiform — and 1st metatarsal and the co-ordinated action of the muscles. Hence in rickets, where the normal tarsal growth is disturbed, the occurrence of flat foot. Amongst the structures which help to maintain the arch are : (a) The growth of the os calcis to form a prominent heel separates the tendon of the plantaris from its prolongation in the sole — the middle part of the plantar fascia, which assists in maintaining the arch. In lower primates the two parts are continuous, the tendon of the plantaris plying across the os calcis in a cartilage-lined groove.

(6) The internal lateral ligament of the ankle (anterior part) and the inferior calcaneo-scaphoid ligaments undergo great development in man.

(c) The flexor brevis digitorum which in lower primates arises principally from the long flexor tendons in the sole, has its origin completely transferred to the os calcis in man. It can thus act more powerfully in maintaining the arch. The flexor accessorius, a detached part of the flexor longus hallucis, is specially well developed and helps to maintain the arch of the foot.

(d) The tibialis posticus, originally a flexor of the metatarsus, correspond ing to the flexor carpi radialis in the hand, obtains a secondary attachment to the scaphoid. The tibialis anticus, which answers to the extensor ossis metacarpi poUicis, becomes permanently inserted into the internal cuneiform and metatarsal. Both of these muscles, thus modified, help to maintain the arch of the foot. So does the tarsal part of the tendon of the tibialis posticus.

(e) The long plantar ligament, originally a part of the tendon of insertion of the gastrocnemius — also assists to maintain the arch.

(4) The development of the great toe and the peculiar arrangement of its muscles must also be regarded as adaptations in the foot to upright posture and progression.

Certain Features of the Musculature of Human Limbs

Muscles of the Pollex and Hallux

The extensor ossis metacarpi poUicis corresponds to the tibialis anticus. The thumb muscle has commonly a carpal insertion as well as metacarpal. The extensor brevis or primi internodii pollicis is constant in man only ; it is a segment of the extensor ossis metacarpi pollicis. The extensor brevis hallucis is not represented in the thumb.

Muscles of the Second Digit

In the lower primates each finger has two extensors — a deep and superficial. The deep in the second digit becomes the extensor indicis ; in the little finger it forms the extensor minimi digiti. The deep extensor muscles have disappeared in man from the 3rd and 4th digits, but occasionally reappear. In the leg the deep extensors have migrated to the foot, and form the extensor brevis digitorum. That for the little toe, however, has not descended ; it is always vestigial, if present. It runs beneath or with the peroneus brevis, and is known as the peroneus quartus or peroneus quinti digiti. If the mirror-image theory is true it represents the extensor brevis pollicis.

Flexors and Extensors of the Metacarpus

These have retained their primitive insertions in the hand ; their modifications in the foot have been already mentioned. Both at the knee and elbow joint the origins of these muscles have undergone much shifting and migration.

Migration of Muscular Attachments

Many of the human muscles acquire during development attachments to segments at a distance from those from which they are developed. The serratus magnus arises from 5th, 6th, 7th cervical segments ; its attachment has extended backwards from the 1st rib until, in man, it reaches the 8th rib ; the trapezius, originally situated in the neck, migrates backwards, and in the 7th week obtains an insertion to the shoulder-girdle, and before the end of the 3rd month its origin has reached as far backwards as the 12th dorsal spine along the median dorsal line. The latissimus dor si migrates to the median dorsal line over the spinal musculature and reaches the spine and crest of the ilium. The diaphragm, which arises in the neck (4th and 5th segments) comes to be attached in the floor of the thorax. The facial musculature takes its origin in the hyoid arch. The sub vertebral (hypaxial) musculature is a migrated part of the transversalis sheet. The omo-hyoid is attached at first to the sternum ; it migrates along the clavicle and reaches (often it fails to reach) the upper border of the scapula. The migration of the subclavius has been in an opposite direction ; originally it reached to the humerus. The case of the extensor brevis digitorum of the foot has just been mentioned. The flexor accessorius is a part of the flexor longus hallucis which has migrated to the sole of the foot. The opponens of the thumb and of the little finger is a separated part of the short flexor muscles of these digits. These are only a few of the more striking examples of the migration of the attachment of muscles, but the mechanism which brings about migration and the biotactic influence which is at work are unknown.

1 J. P. McMurrich, Amer. Journ. Anat. 1906, vol. 6, p. 407 (Plantar Musculature) ; J. P. McMurrich, Amer. Journ. Anat. 1904, vol. 4, p. 33 (Musculature of Thigh).

Vestigial and Abnormal Muscles of the Limbs and Trwik.— (1) The muscles of the human ear and scalp may be described as vestigial when compared to the development in other mammals. Although their action on the ear and scalp is feeble, yet they serve as most important bases into which certain psychological states are reflected.

(2) The levator claviculae (omo-trachelian) is a muscle which passes from the upper transverse cervical processes to the outer end of the clavicle or acromion process. It is well developed in climbing primates. It is not a common muscle in man. It can be recognized during life in the posterior triangle of the neck.

Fig. 471. Latissimo-condyloideus Muscle.

(3) The latissimo-condyloideus (dorsal epitrochlearis), a climbing muscle, is always represented in man, commonly by a fibrous bundle between the tendon of the latissimus dorsi and the long head of the triceps (Fig. 471). The bundle may be occasionally muscular. In apes it passes from the latissimus dorsi at the axilla to the inner aspect of the elbow and arm, which it retracts in climbing. It belongs to the same sheet as the coracobrachialis. The ligament of Struthers — a strip of fibrous tissue over the internal intermuscular septum, above the internal condyle — represents part of the tendon of this muscle. The muscular slips occasionally found crossing the brachial or axillary artery from the latissimus dorsi to the coraco-brachialis or biceps are derivates. Other slips found crossing the fioor of the axilla, between the adjacent borders of the pectoralis major and latissimus dorsi, are parts of the muscular sheet out of which these two muscles are developed.

(4) The pectoralis externus arises from the 4-5-6 ribs and costal cartilages, beneath the axillary border of the pectoralis major. This is its normal condition in most mammals, but in man it is commonly fused with, and forms part of, the pectoralis major.

(5) The sternalis is a remnant of the primitive rectus sheet (Fig. 445). The pectoralis major is formed from the same ventral longitudinal sheet as the rectus abdominis and sterno-mastoid. The fibres of the sternalis, which lie along the sides of the sternum, superficial to the origin of the pectoralis major, represent a persistent part of the primitive longitudinal sheet.

(6) In the sterno-mastoid four elements are recognized : sterno-mastoid, sterno-occipital, cleido-mastoid, cleido-occipital. The cleido-occipital fibres, which form part of the same sheet as the trapezius, are often absent. On the other hand, the cleido-occipital fibres may be continuous with the trapezius. The sterno-mastoid and trapezius muscles are developed in the occipital segments and are originally connected with gill arches.

(7) The pectoralis minor is sometimes inserted to the capsule of the shoulder and great tuberosity of the humerus as is the case in primates generally. The coracoid insertion, which is the usual one in man and also in the gorilla, is usually regarded as a secondary attachment, but Miss K. Lander ^ has shown that it is also found in primitive types of mammals. When the pectoralis minor is inserted to the coracoid, the former fibres of insertion become fused with, and form part of, the coraco-humeral ligament, which, however, is a distinct structure, and represents a specialized part of the capsule of the shoulder joint.

(8) In some apes (such as the Gibbons) the biceps has four heads — the two usual, the long and short, and two others, one from the inner border of the humerus and one from the bicipital groove. These two extra heads appear frequently in man.

(9) The epitrochleo-anconeus is frequently present. It crosses the ulnar nerve from the internal condyle to the olecranon.

(10) The palmaris longus and its homologue in the leg, the plantaris, are vestigial, aberrant in form, and often absent. The plantar and palmar fasciae represent their divorced tendons. The plantaris and palmaris undergo retrograde changes in the primates with the transformation of claws to nails.

(11) Each digit (fingers and toes) in lower primates, such as monkeys, is provided with three short muscles which arise from the carpus or tarsus. The three muscles are (Fig. 472) : (1) a short flexor on the radial side of the digit ; (2) a short flexor on the ulnar side ; (3) a contrahens or adductor muscle (always absent in the middle digit). The ten short flexor muscles form a deeper sheet than the four contrahentes. Of this form the arrangement of the short muscles in the human hand is a derivative. The remnants in the human hand and foot of the contrahentes are : (1) The adductors of the 1st digit (poUex or hallux) ; (2) fibrous remnants of the others occur over the deep plantar or carpal arch (Fig. 472). The short flexors in man have become (1) the seven interossei ; (2) the flexores breves (ulnar and radial) and opponens of the first digit ; the flexor brevis and opponens of the fifth digit (see Fig. 472). The ulnar flexors of the thumb and great toe are absent or fibrous.

1 Journ. Anat. 1918, vol. 52, p. 292.

(12) The pyramidalis is often absent in man or vestigial. It is the tensor of the linea alba.

(13) Remnants of the extensors and flexors o! the tail may occur between the sacrum and the coccyx (p. 410).

(14) The coccygeus is vestigial ; its superficial part forms the small sacro-sciatic ligament.

(15) Fibres of the biceps of the thigh may be followed into the great sacro-sciatic ligament. This ligament, which is almost peculiar to man — in other primates it is quite thin and slender — may contain fibres derived from the caudo-femoral group of muscles, such as the tenuissimus, a long strap-like muscle which passes from the coccyx to the femur and leg in lower mammals. The sacro-sciatic ligament is mainly derived from the great median sheet, out of which the middle layer of the lumbar fascia is also formed. Parsons regards the short head of the biceps as a derivative of the tenuissimus, while others regard it as part of the muscular sheet which forms the peroneal muscles. Amongst primates, the short head is found only in man, the anthropoids, and some South American apes. It corresponds to the brachialis anticus in the arm, and is supplied by the external popliteal nerve.

Fig. 472. The Morphology of the Short Muscles of the Digits. The muscles shaded are those of the ape's hand or foot ; the positions of the corresponding muscles in the human hand or foot are indicated by dotted outlines.

(16) The psoas parvus is also vestigial. It acts primarily as a flexor of the pelvis on the spine. It begins to disappear in those primates which assume the erect posture.

(17) The scansorius is a separated segment of the gluteus medius and minimus. It rises from the anterior border of the ilium and passes to the great trochanter. It corresponds to the teres minor. It is not constant in any animal.

(18) The flexor brevis digitorum to the little toe and the adductor transversus of the great toe are often fibrous.

The Supra-condylar Process ^ is well developed in lemurs, the lowest primates, and in mammals of many orders. Its function is unknown. It occasionally appears in man. Dr. Rutherford found it represented in a human foetus in the 9th week of development. It is developed from the humerus about two inches above the internal condyle as a hook-like process of bone. It lies in front of the internal intermuscular septum, and when well developed the brachial artery and median nerve may pass beneath it, as they do in such animals as the squirrel and cat.

1 T. Dwight, Amer. Journ, Anat. 1904, vol, 3, p. 221.

Development of Joints

Each limb bone is formed from a centre of chondrification which appears in the 2nd month within the unjointed skeletal blastema of the limb bud. At these centres the mesodermal cells assume the characters of cartilage cells ; growth proceeds most rapidly at the periphery of the cartilage centres ; as the growing centres approach each other, part of the original blastema is left between them. This tissue, which may be named the interchondral disc, forms the first basis of a joint (Fig. 473). The cells in the peripheral part of the blastema condense and form a perichondrium — a membrane which surrounds growing cartilages. In the 8th and 9th weeks, joints begin to appear in the interchondral discs, the more important before the less important. The manner of formation is the same for all joints ; in the periphery of the interchondral disc, the mesenchymal cells begin to disappear, giving rise to the synovial space which spreads towards the centre of the developing joint — the central part being the last to form. The perichondrium is continued from segment to segment over the interchondral discs and thus becomes the basis of the capsular ligament. At first the ends of the cartilages projecting into joint cavities are also covered by an extension of the perichondrium. Peripheral cells of the interchondral disc line the capside and form the synovial membrane, the cells of which, even in the adult, show by their structure that they are cartilaginous in nature. In certain pathological conditions, the synovial villi give rise to cartilaginous nodules.

Fig. 473. Sagittal section of Terminal Joint of Finger of Foetus in 10th week of development. (After Nicolas.)

Interarticular Fibro-cartilages

In every developing joint fringes of synovial membrane, representing remnants of the interchondral disc (intermediate plate), project in the gap between the articular margins of bones (Fig. 473). In the elbow joint they are present, even in the adult ; in the hip and shoulder joint they form the cotyloid and glenoid ligaments. In the knee joint they are much better marked, forming the semilunar cartilages. At the wrist joint the interchondral disc forms the triangular fibro-cartilage, but here it is possible that certain other elements are included. A nodule of cartilage, which may ossify, is present ; within it certain ligaments which united the radius and ulna, and these two bones with the semilunar and cuneiform, have been included (Parsons and Corner). This cartilage is complete in man only ; it plays a part in the mechanism of pronation and supination. In the sterno-clavicular joint two synovial cavities are formed, one on either side of the interchondral disc. In this case it is only in the higher primates that a complete interarticular disc is present. Two synovial cavities are also formed in the temporomandibular joint, the meniscus separating two joints, which are functionally difierent. The upper is for gliding movements, the lower for hinge-like movements.

Fig. 474. Showing the Origin of the Crucial Ligaments of the Knee.

Fig. 475. Showing the Origin of the Ligamentum Teres and Reflected Bundle of the Capsular Ligament.

Capsular Ligaments

Certain parts of the capsule of every joint become thickened and specialized according to the strains to which the joint is subjected. Parsons found that it is the middle gleno-humeral ligament of the shoulder joint which becomes enlarged and projects within the joint of prono grade mammals. In man, the coraco-humeral ligament is by far the strongest. The anterior part of the capsule of the hip joint in man has to withstand the strain of the body when the thigh is extended in the upright posture. Part of it becomes specialized to form the iliofemoral or Y-shaped ligament. In the knee joint the posterior part of the capsule is strengthened to prevent over-extension. The development of the condyles of the femur towards the popHteal space isolates a posterior part of the capsule which thus comes to lie within the joint and form the crucial ligaments (Fig. 474). The ligamentum teres, the best example of an intra-articular ligament, appears in the human foetus, as part of the capsule of the joint ; in reptiles this foetal form is retained. The round ligament is isolated by the development of the head of the femur, which expands as a wing on each side of the ligamentum teres, and by the fusion of the wings isolates it from the capsule (Fig. 475). The reflected ligament on the under surface of the neck of the femur, is the part of the capsule with which the ligamentum teres was continuous.^ Knee Joint. — In Fig. 476 is given a diagrammatic representation of the posterior aspect of the knee joint as seen in a primitive mammalian type. Three interarticular discs are shown ; an internal tibio-femoral, an external tibio-femoral and a fibulo-femoral. When the fibula became excluded from the knee joint, the fibulo-femoral disc, from which fibres of the popliteus took origin, was included in the tendon of that muscle (Carl Ftirst). The popliteus originally passes from the fibula to the tibia like the pronator quadratus in the forearm. The upper fibres migrate to the capsule and to the fibulo-femoral disc, and through the disc and its ligaments gain an attachment to the femur. Thus, instead of rotating the tibia on the fibula, the popliteus muscle now rotates the tibia on the femur. Occasionally the cavity of the human knee joint communicates with the superior tibio-fibular joint through the synovial diverticulum beneath the tendon of the popliteus. The upper end of the fibula is being excluded from the knee joint during the 8th week. There are five separate synovial cavities developed in this joint — one between the patella and femur, two between the femoral condyles and the primitive semilunar cartilages, and two between the cartilages and the upper extremity of the tibia. The five joints become continuous in the 4th month, the crucial and alar ligaments being derived from the primary septa between the cavities (Bardeen).^ The external semilunar cartilage is circular in form and continuous with the posterior crucial ligament in primates, in which the power of rotation at the knee is highly developed ; in man the circular form of the cartilage is lost and it only retains part of its continuity with the posterior crucial ligament (Parsons). The ligamentum mucosum, which in many mammals separates the knee joint into three compartments — two condylar and a patellar — is much reduced in man.

Fig. 476. — Scheme of a Primitive Mammalian Knee-joint to show (1) the Articulation of the Fibula with the Femur ; (2) the Fibulo-fermoral Interarticular CartUage which becomes included in the Tendon of the Popliteus ; (3) the Tibio-fibular Muscle out of which the Popliteus is evolved ; (4) the division of the Tibiofemoral Interarticular Cartilage into external and internal Semilunar Cartilages. (Carl Fiirst.)

Ossification of Bones

The simplest and most primitive manner in which bones pass from the cartilaginous to the osseous stage is seen in the carpus and tarsus (Fig. 477). Bone is entirely deposited witMn the cartilage by a process of endochondral ossification. The various stages in this process may be grouped as follows : (1) calcification of the intercellular matrix in the centre of the bone — a temporary phase in human ossification, but a permanent one in some fishes ; (2) an invasion of vasoformative and osteoblastic cells which, commencing at a point beneath the perichondrium, reach the middle of the central area of calcification and form a centre of ossification (Fig. 477). The osteoblasts and their accompanying vessels, when the cartilage cells are absorbed, deposit bone in the spaces of the calcified matrix. A section through an ossifying and growing carpal bone shows (1) a centre of ossification ; (2) a surrounding narrow area of calcification ; (3) a peripheral area of actively growing cartilage ; (4) a covering membrane or perichondrium. The processes of growth and ossification cease when the cartilage beneath the perichondrium is completely transformed to bone. Not only are the tarsal and carpal bones formed thus, but so are the epiphyseal ends of all long bones.

^ See Walmsley, Journ. Anat. 1917, vol. 51, p. 61, " See reference, p. 425,

Fig. 477. Section of the Tarsus at the 3rd year of development to show pure Endochondral Formation of Bone.

In the shafts of long bones, to the process of endochondral ossification, another — the ectochondral — is added (Fig. 478, A, B, C, D). An endochondral centre is formed as in the tarsal bones, and from this centre the process extends rapidly in every direction. Some of the osteoblasts, instead of invading the cartilage, form a layer beneath the perichondrium, which surrounds the cartilaginous substance of the bone. The perichondrium now becomes periosteum ; the deposit of periosteal bone leads to an increase in the thickness of the shaft (Fig. 478, C) ; the extension of the endochondral ossification into the growing cartilaginous ends of the bone leads to an increase in the length of the shaft. As the periosteal bone is deposited, the endochondral bone within the shaft is absorbed and a medullary cavity is formed, in which red marrow begins to appear in the 6th month (Fig. 478, D). The cartilaginous parts of the bone, at each extremity of the shaft, form the epiphyses. When the endochondral centres appear and grow within the epiphyses, a line of growing cartilage is gradually isolated between them and the endochondral centre of the shaft (Fig. 478, D). At the epiphyseal line the bone grows in length, the addition being made solely at the shaft or diaphyseal side of the line. These g^o^vth discs should therefore be named, not epiphyseal but diaphyseal lines. By the formation of epiphyses at the ends of long bones, the growing line of cartilage is sheltered from the friction and stress to which it would be exposed if situated on the articular ends of the bones. All the cartilage of a bone, except that on the articular surfaces, is ossified when the body is fully grown. The evidence at our disposal points to both the absorption of the cartilage and the deposition of bone as being regulated by secretions derived from the thyroid, pituitary and other glands of internal secretion.^ In the growth of a long bone, such as the humerus, the proximal and distal diaphyseal lines take an unequal share. Digby 2 found that while the proximal line added 4 parts to the length of the humerus the distal line contributed only 1 part. The chief nutrient canal of the shaft of a long bone points to the centre at which endochondral ossification commenced.

Fig. 478. Ossification of a Long Bone by Endochondral and Ectocliondral Ossification. (After Nicolas.)

A, Ossification within the cartilage of the shaft.

B, Complete ossification of the middle part of the shaft.

C, Formation of bone in the shaft outside the cartilage by osteoblasts lying beneath the perichondrium (now named periosteum).

D, Complete absorption of the endochondral bone of the shaft ; formation of a medullary cavity ; appearance of endochondral centres in the epiphyses ; formation of the epiphyseal lines.

1 Keith, Lancet, April 15th, 1911 ; Journ. Anat. 1913, vol. 47, p. 189 ; ibid. 1920, vol. 54, p. 101 ; Lancet, 1913, vol. 1, p. 305.

2 Kenelm Digby, Journ. Anat. 1916, vol. 50, p. 186.

Nature of Epiphyses

Epiphyses are of three kinds : (1) pressure epiphyses, forming the articular extremities of long bones (Fig. 479, B) ; (2) traction epiphyses, which form processes for the insertions of muscles (Fig. 479, B) ; (3) atavistic epiphyses, formed by the union of an element which formerly existed as a separate bone (Fig. 479, A).

The upper extremity of the femur affords typical examples of pressure and traction epiphyses. By the extension of the ossification of the shaft within the cartilage of the upper extremity of the femur, the pressure and traction epiphyses become widely separated to form the head and trochanters. Pressure epiphyses are the first to ossify, their centres appearing in the order of their functional importance ; they are always fitted to the shaft by a species of dovetailing to withstand dislocating forces. The upper extremity of the shaft of the humerus projects as a three-sided pyramid within the epiphysis ; Professor Arthur Thomson has shown that the lower end of the shaft of the femur is fitted within its lower epiphysis by a number of projections not well marked in the human bone but pronounced in those animals which maintain the knee in a flexed position. Epiphyses are mammalian characters ; their rudiments are to be seen in reptilia.

Fig. 479, A. The Epiphyseal Cartilage of the Pubis and Ischium, which arises from the Median Cartilage of the Pelvic Girdle. (Parsons.) B. Traction and Pressure Epiphyses on the upper extremity of the Femur. C. — The Epiphyses of the Olecranon : a, the usual Epiphyses ; b, occasional Epiphyses : both a and b may be present. (Fawcett.)

The great trochanter is the traction epiphysis of the gluteus medius and minimus ; the small trochanter, of the psoas and iliacus ; the third trochanter, in which a centre appears in the 20th year (Dixon), that of the gluteus maximus.

As examples of atavistic epiphyses. Parsons cites the following : those of the ischium and pubis (Fig. 479, A) from the median pelvic bar (Figs. 442, 479) ; the coracoid process ; the epiphysis on the os calcis, the scale like epiphysis of the olecranon (Fig. 479, C). The internal and external condyles of the humerus may be derived from sesamoid ossifications, such as are now seen in the patellae, in the tendons of the popliteus, outer head of gastrocnemius (occasional), peroneus longus, tibialis posticus and at the metacarpo-phalangeal joints of the thumb and great toe. The patella is usually regarded as a sesamoid, but Mile. Bertha Vriese collected evidence to show that it is really a true morphological skeletal element.^

^ The account given by Parsons has been followed. See Journ. Anat. and Physiol. 1903, vol. 37, p. 315 ; 1904, vol. 38, p. 248 ; 1908, vol. 42, p. 388. R. L. Moodie, Amer. Journ. Anat. 1907, vol. 7, p. 443 (Reptilian Epiphyses). A. Kirchner, Anat. Hefte, 1907, vol. 33, p. 513 (Epiphyses of Os Calcis and 5th Metatarsal). T. Walmsley, Journ. Anat. 1919, vol. 53, p. 326.

Lines of Pressure and Tension on Bones

The trabeculae, in which the bony matter is deposited by the osteoblasts, are arranged so as to withstand the forces to which the body is subjected. When a bone, such as th'e astragalus, rib or neck of the femur, is laid open by a section, the trabeculae appear to form straight lines or septa which converge and meet at various angles ; when, how^ever, such bones are examined stereoscopically with the X-rays, the trabeculae are seen to be arranged in a double spiral — one system twisting from right to left, the other from left to right (Haughton and Dixon). ^ By this means, the greatest strength is obtained with the least expenditure of material.

Split Hand and Foot

The extremities are subject to a remarkable series of malformations, which apparently represent arrests of their development. The digits may be abnormally short (brachy-dactyly), owing to an arrest in the differentiation of the blastema of the phalanges, the terminal phalanx being unseparated from the middle.^ Besides errors in the separation of the phalanges, there is an arrest of growth — usually in th^ middle phalanges, while, as Dr. Drinkwater has shown, extra phalanges may be intercalated. This is of frequent occurrence in the fifth digit of the foot. In another series of cases the hand or foot appears as if cleft — an appearance due in some cases to the fact that three or more of the digits on the ulnar side of the hand or fibular side of the foot have remained joined or webbed, as in the embryo of the 2nd month, while in others the condition is due to a splitting or dichotomy of the terminal plate of the limb bud. The condition is hereditary.* In more extreme cases the digits on the radial, or more rarely, those on the ulnar side of the hand, may be absent ; the corresponding bone of the forearm or leg is also undeveloped. Such cases lead one to suppose that the two distal segments of the limbs are developed from a radial and ulnar or tibial and fibular buds, and in such cases only one of these has been affected. Both may be arrested, the extremities terminating at the proximal segment. In extreme cases the limb buds are undeveloped.

1 Bertha de Vriese, Bull, de VAcad. Roy. de Sc. Belgique, 1909, March 27th.

2 Dixon, Journ. Anat. and Physiol. 1910, vol. 44, p. 223.

3 A. Fischel, Anat. Hefte, 1909, vol. 40, p. 1 ; J. D. Fiddes, Anat. Anz. 1912, vol. 40, p. 544 (Supernumerary Hallux) ; J. Symington, Journ. Anat. and Physiol. 1906, vol. 40, p. 100 (Hyper-phalangism in Cetacea) ; H. Drinkwater, Journ. Anat. 1916, vol. 50, p. 177.

4 See T. Lewis, Biometrika, 1908, vol. 6, p. 25.

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Human Embryology and Morphology: 1 Early Ovum and Embryo | 2 Connection between Foetus and Uterus | 3 Primitive Streak Notochord and Somites | 4 Age Changes | 5 Spinal Column and Back | 6 Body Segmentation | 7 Spinal Cord | 8 Mid- and Hind-Brains | 9 Fore-Brain | 10 Fore-Brain Cerebral Vesicles | 11 Cranium | 12 Face | 13 Teeth and Mastication | 14 Nasal and Olfactory | 15 Sense OF Sight | 16 Hearing | 17 Pharynx and Neck | 18 Tongue, Thyroid and Pharynx | 19 Organs of Digestion | 20 Circulatory System | 21 Circulatory System (continued) | 22 Respiratory System | 23 Urogenital System | 24 Urogenital System (Continued) | 25 Body Wall and Pelvic Floor | 26 Limb Buds | 27 Limbs | 28 Skin and Appendages | Figures