Monkey (Macaca fascicularis)

Transcription

1 Oka jimas Folia Anat. Jpn., 59(5) , December 1982 Constitution of the Thigh Muscles in the Crab-eating Monkey (Macaca fascicularis) By YUTAKA TAKAHASHI Department of Anatomy, National Defense Medical College, 2, Namiki-3, Tokorozawa 359, Japan (Director : Prof. Kunihiko Kimura)?Received for Publication, September 27, 1982? Key Words : Crab-eating monkey, Macaca fascicularis, Thigh muscle, Innervation, Morphology Summary. The constitution of the muscles of the thigh were examined in 24 male and 26 female crab-eating monkeys (Macaca fascicularis). The boundary of the origin and the insertion of the muscles were defined. The composition of the spinal nerves was observed in two specimens. The n. femoralis, n. obturatorius and n. flexoris femoris arose from the lumbar plexus and ranged from the third to the fifth, the fourth to the sixth and the fifth to the seventh lumbar nerves, respectively. The segmental innervation of the muscles in the same specimens was studied. The muscles of the thigh were categorized into seven groups based on the innervation and their relative positions. More cranially arising muscle groups received a higher segmental nerve. They were inserted more medially because of rotation of the hip joint during embryogenesis. More distally and laterally inserting muscles within the same muscular group received a lower segmental nerve than the others. These findings suggest a uniform mechanism in the myotome arrangement of the lower limb during embryogenesis in man and the monkey. On this basis, the dual innervation and intermuscular septum in the thigh are well explained by the developmental process. In the course of a myological survey of the crab-eating monkey (Macaca fascicularis), the morphology of the upper arm musculature (Kimura and Takai, 1971) and flexor group (Kimura, Takahashi and Konishi, 1980), the adductor group (Kimura, Takahashi, Konishi and Iwamoto, 1981) and the extensor group (Kimura, Takahashi, Konishi and Iwamoto, in press) of the thigh muscles have previously been examined. The results obtained from serial reports on the crab-eating monkey agreed in general with those of the other Macaca species and the new world monkeys proposed. The torsional architecture of the muscle fibers was elucidated in the adductor muscle of the crab-eating monkey (Kimura et al., 1981). Similar features have been reported in other macaques by Waterman (1929), and Howell and Straus (1933). These muscles were clearly classified into proper muscles and subdivisions of these, based on the ramificate pattern of the n. 291

2 292 Y. Takahashi obturatorius according to Uhlmann (1968). Last (1949) proposed some general rules for the segmental innervation of the upper and lower limbs in man. The anterior muscle that moves a given joint is supplied by two consecutive segmental nerves, while the posterior muscle that moves the same joint in the opposite direction is typically supplied by two succeeding nerves. This explains the higher origin of the n. femoralis than the n. flexoris femoris which is a branch of the n. ischiadicus in the thigh. The dermatome of the monkey has been studied by Sherrington (1898), Kuhn (1953), and Kirk and Denny-Brown (1970). Little was done, however, on the correlations of the dermatome and myotome in monkeys. Recently, Dykes and Terzis (1981) studied the organization of the dermatome and afferent myotome in the upper limb of the African green monkey (Cercopithecus aethiops). In the present paper, general rules for the constitution of the thigh muscles with special reference to the arrangement of each of the muscles and nerves are discussed. Materials and Methods The specimens of crab-eating monkey (Macaca fascicularis) used for this study were obtained from the Japan National Institute of Health, and were preserved in 10% formalin solution for at least three months. Since the brain and some parts of the viscera had been removed, the body weights were unknown. From their physical condition, tooth eruption and ossification of the skeleton, all animals were estimated to be young adults. Dissections and descriptions were made according to the routine methods described previously in this series of studies. In addition, two female monkeys were used for observation of the constitution of the lumbosacral plexus and the origin of each muscular branch. The segmental composition of each muscular branch was examined in four thighs up to the ventral proximary rami under the microscope. Results The thigh muscles of the crab-eating monkey (Macaca fascicularis) are composed of three muscle groups : extensors, adductors and flexors. The extensor group comprises the m. sartorius, m. rectus femoris, m. vastus medialis, m. vastus intermedius and m. vastus lateralis. The adductor group comprises the m. pectineus, m. adductor longus, m. gracilis, m. adductor brevis, m. adductor magnus and m. obturatorius externus. The m. adductor brevis and m. adductor magnus are subdivided into a pars brevis and longa, and a pars minima, intermedia and lata, respectively. In the latter, the pars intermedia is usually more or less adherent to or fused with the ventral surface of the pars lata. The pars intermedia was found to be divisible from the pars lata at the insertion in only 23% of cases in a previous study (Kimura et al., 1981). The flexor group comprises the m. semimembranosus accessorius, m. semimembranosus proprius, m. semitendinosus and m. biceps femoris. The m. biceps femoris has only one head (the caput longum) in the monkey. The origin and insertion of each of the muscles are shown in Table 1. Diagrams of the muscle attachments to the pelvis and femur including below the knee are given in Figures 1 and 2. The insertions of the m, sartorius, m. gracilis, m. semimembranosus proprius and m. semitendinosus are illustrated as though they were observed from the antero-medial aspect of the tibia. The positional torsion between the origin and the insertion was observed in

3 Thigh Muscle Constitution in the Crab-eating Monkey 293 Table 1. Origin and insertion of the thigh muscles in the crab-eating monkey. the adductor group. The fleshy origin and insertion of the m. adductor magnus make the muscular bundle arrangement clear throughout its course. Figure 3 depicts the deep layer of the thigh muscles and the n. obturatorius from the antero-lateral aspect. The constitution of the muscular bundle of the m. adductor magnus is shown schematically in Figure 4. As indicated in this figure, an inverted J-shaped formation in the order of the pars minima to lata is visible at the origin of the m. adductor magnus. The arrow with a broken line represents the direction

4 294 Y. Takahashi Figure 1. Lateral view of the right hip bone demonstrating the areas of muscular attachment. of arrangement of the muscles at the origin and insertion. The fleshy insertion lies successively straight on the posterior surface of the femur in the same order. In the adductor brevis, the origin is arranged in a similar manner from the body of the pubis to the inferior public ramus in the order of the pars brevis to longa, while the insertion of the pars brevis is located proximally to that of the pars longa adjoining the insertion of the m. semimembranosus accessorius. The third group of muscles is composed of the m. adductor longus and the m. gracilis. They are arranged in an inverted J-shaped formation on the symphysis and the cranial border of the superior pubic ramus at the origin, while they insert into the middle third of the femur and the tibia from proximal to distal in the above order. The j-shaped formation of the adductor muscles at their origin is composed of three rows on the pubic bone in a craniocaudal direction. At the insertion, these muscles lie in three lines on the posterior aspect of the femur from medial to lateral. The cranio-caudal direction at the origin alters to the medio-lateral order at the insertion. Three peripheral nerves contribute to the innervation of the thigh muscles. The extensor and the m. pectineus which belong to the adductor are innervated by the n. femoralis. The remaining adductors are innervated by the n. obturatorius. The n. obturatorius divides into an anterior and a posterior branch before passing through the m. obturatorius externus as shown in Figure 3. The m. obturatorius externus is supplied by both rami. The anterior branch further divides into two small branches : an inferior and a superior branch. The inferior branch (1 in Figure 3) runs forwards to innervate

5 Thigh Muscle Constitution in the Crab-eating Monkey 295 Figure?.. Posterior view of the right femur demonstrating the areas of muscular attachment. the m. adductor longus and the m. gracilis at their inner surface and the pars brevis of the m. adductor brevis during its course. The superior branch (2 in Figure 3) supplies both the pars brevis and longa of the m. adductor brevis and sends off a small cutaneous twig on the medial surface of the thigh. The posterior branch (3 in Figure 3) gives off branches to the pars minima of the m. adductor magnus on its inner (deep) surface, then runs around its belly and forwards to give off a twig to the pars intermedia, before finally entering the pars lata on its medial margin, in most cases (93%) of this series. Only in the remainder (7%) did the posterior branch pass through the pars minima of the m. adductor magnus. The flexor is innervated by the n. flexoris femoris which is a branch of the n. ischiadicus. Dual innervation was not observed in any case in this study. The composition of the lumbar plexus was examined in two female monkeys. The n. femoralis arose from the third to the fifth lumbar nerves, except in one case where it was composed of the third and the fourth lumbar nerves. The n. obturatorius arose from the fourth and the fifth lumbar nerves, except in one case

6 296 Y. Takahashi Figure 3. Lateral aspect of the right thigh. 1: n. obturatorius ramus anterior inferior, 2: n. obturatorius ramus anterior superior, 3: n. obturatorius ramus posterior. Figure 4. Diagram illustrating the torsional architecture of the m. adductor magnus.

7 Thigh Muscle Constitution in the Crab-eating Monkey 297 Figure 5. Segmental and peripheral nerve supply of the thigh muscles. The segmental constitution of the muscular branch is expressed by the number of asterisks examined in four thighs. where it was composed of the fourth to the sixth. There were various types in the pattern of origin of the n. flexoris femoris. Branches, arising from the fifth to the seventh or two of these, composed the n. flexoris femoris. The n. femoralis is derived from the posterior division, whereas the n. obturatorius and n. flexoris femoris arise from the anterior fasciculi of the plexus. The segmental compositions of each of the muscular branches were examined in four thighs up to the ventral proximary rami as summarized in Figure 5. The frequency of segments of each muscular branch is expressed by the number of asterisks. The muscular branches for the m. sartorius and m. pectineus were comprised of only the third lumbar nerve in three cases. In the other one case, the muscular branch was comprised of a root from the third and fourth lumbar nerves. These muscles are abundant in spinal nerve fibers arising from a higher segment than the others. The m. biceps femoris ranks as the lowest muscle in the thigh. The muscles of the thigh were cate- gorized into seven groups as shown in Figure 6 based on the innervation and their relative positions. The ranks of these were determined by the nature of the innervation as shown at the head of each group and arrow at the left margin of the figure. Also, the relative positions at their origin and insertion were taken as supplementary to the former items. The m. sartorius and the m. pectineus are placed in the first row because of their segmental nerve compositions. The other extensor muscles are categorized into two groups according to their origins and insertion. The fourth to sixth groups

8 298 Y. Takahashi Figure 6. Constitution of the thigh muscles and nerves of the crab-eating monkey. are composed of the adductor muscles corresponding to their nerve supply. The last group is made up of the flexor muscles. In each row, the muscles are arranged from left to right according to the relative positions of insertion : of two muscles, that which inserts more proximal or medial is set to the left, and that which inserts more distal or lateral is arranged to the right in the same row. The direction of the sequence is shown by the arrow in the upper margin of Figure 6. The muscular arrangement in Figure 6 reveals the following facts. More cranially arising muscles receive higher segmental nerves. The m. sartorius, m. adductor longus and m. semimembranosus accessorius arise more cranially and have higher segmental nerve supplies than the others within the same muscular groups. More distally and laterally inserting muscles tend to receive lower segmental nerve supplies than the others in each group. The m. vastus lateralis, m. adductor magnus pars lata and m. biceps femoris insert the more lateral and distal portion of the femur and tibia than the other muscles in the same group as shown in Figure 2. Their muscular branches are rich in lower segmental nerves compared with the other muscles in their group as shown in Figure 5. The cranio-caudal direction of the muscular sequence at the origin corresponds to the level of the segmental innervation. The direction alters its axis during embryogenesis from craniocaudal to medio-lateral at the insertion. Rotation of the hip joint brings about the positional change between the origin and the insertion. Before the rotation of the hip joint, the muscular attachment to the given area on the bone is completed and intrusion of the innervating nerve is effected. The thigh muscles of the monkey are well organized in segmental innervation up to the adult form. Discussion Positional torsion between the origin and the insertion was observed in the adductor group. The torsional architecture of the adductor muscle has been described in other macaques by Waterman (1929), and Howell and Straus (1933). They did not discuss the fiber constitution and nerve supply. The fleshy origin and

9 Thigh Muscle Constitution in the Crab-eating Monkey 299 insertion of this muscle make it easy to understand the constitution clearly. This is barely discernible in man, however, because of the tendinous insertion of this muscle. The fan-shaped origin derives from the embryogenic process. The foramen of the obturator is encircled by the pubic and ischiadic processes in the posterior and anterior directions, respectively. In accordance with elongation of the skeletal elements, the origin of the adductor muscles conforms to the original features of the attachment to the bone. Finally, the adductor group is arranged into inverted J-shaped rows on the outer surface of the pubic bone in accordance with the branching pattern of the n. obturatorius. The muscular branch of the n. obturatorius maintains the original course until the later period. The muscular branch to the pars lata, in the adult thigh, was found to run around the pars minima in almost all cases in a previous study (Kimura et al., 1981). The topographic situation of the muscle and nerve in the thigh can be retraced from the adult to the embryonic stage in the monkey. The n. femoralis, n. obturatorius and n. flexoris femoris were found to be comprised of the third to the seventh lumbar nerve in the present study. They arose frequently from the third to the fifth, the third to the fifth, and the fifth to the seventh lumbar nerve in Macaca mulatta (Takeuchi, 1960 and 1961) and also in Macaca fascicuralis (Urbanowicz and Zaluska, 1969 ; Zaluska, 171; Zaluska and Urbanowicz, 1971 and 1972 ; Urbanowicz, 1972, respec tively. The present results are not so different from those of other studies on macaques, except as regards the origin of the n. obturatorius which receives no branch from the third lumbar nerve. In man, the composition of the plexus is usually shifted to higher segments than that of the monkey (Paterson, 1894b). There are no compatible data for the segmental innervation pattern of the thigh muscle in macaques. The findings obtained in the present studies on the crab-eating monkey are not so different from those of man (Paterson, 1894a). The level is shifted higher in man, although the relative projection pattern tends to be similarly distribute in each muscular group. The m. sartorius and m. pectineus are ranked at the highest order according to their segmental nerve supply in man and also in the crab-eating monkey. The m. biceps femoris is the lowest muscle in terms of the nature of the segmental innervation as in the monkey. Herringham (1886) provided an anatomical scheme for the innervation of the musculature of the upper limb in man. He formulated three rules for the manner of innervation : a muscle tends to be supplied by a higher nerve when it is nearer the head-end, long axis and surface compared with others. Sherrington (1898), and Dykes and Terzis (1981) agreed with Herringham's first two propositions based on their studies of the monkey. The present investigation reveals a similar pattern of distribution of spinal nerves in the thigh of the crab-eating monkey to the former two items of Herringham's rules. Application of his third rule, however, is more or less complex. The superficial muscle of the extensor is the m. rectus femoris. Its segmental innervation is expanded to higher segments than the deeper one. The pars lata which forms the superficial part of the m. adductor magnus, lacks in higher segmental nerves of the n. obturatorius. Herringham's rule in the third item is true in the extensor but not critical in the adductor. A superficial muscle has more a cranial (proximal) origin or more caudal (distal) insertion than a muscle which is covered

10 300 Y. Takahashi by the former. A more cranially arising part tends to have a higher segmental innervation. A more distally inserting part tends to show a lower segmental innervation. The quadriceps muscles of the thigh vary in their origin with their own respective natures but are not so differ in their insertion area. In other words, the m. rectus femoris has a more cranial origin and higher innervation. The pars lata of the m. adductor magnus has a more distal insertion than the others and has a lower segmental innervation. The process of limb formation in the human embryo has been studied by Bardeen (1906) employing micro-dissection, and by Miyazaki (1959) and Sato (1961) using histological cross-sections. Lance- Jones (1979) observed the differentiation of the thigh muscle of the embryonic mouse based on serial cross-sections and a reconstruction method. Landmesser and Morris (1975), Landmesser (1978a, 1978b), and Lance-Jones and Landmesser (1981) studied the projection pattern of motoneurons in the anterior segment of the lumbosacral spinal cord of the chick embryo by electrophysiological and HRP labelling methods. Figure 7 represents suppositionally a medial view of the right thigh at the beginning of limb formation during embryogenesis according to the data obtained. The muscular anlagen for the thigh muscle appear at the proximal site of the femoral shaft as two muscular masses. The dorsal mass further divides into iliac and extensor muscular groups. The ventral one becomes the adductor and flexor muscles. The former is innervated by the n. femoralis ; the latter is innervated by the n. obturatorius and the n. flexoris femoris. M. pectineus derives from the iliac muscular mass. Figure 7. Schematic diagram illustrating the developmental process of the muscles and nerves during limb morphogenesis. Large arrows indicate the direction of muscular growth. The two lines show the discontinuous plane of the muscular anlagen at the medial (M) and the lateral (L) aspect of the thigh. E : extensor, I : iliac, A : adductor, F : flexor anlagen. The pubic (p) and iliac (i) processes are not fused at this stage.

11 Thigh Muscle Constitution in the Crab-eating Monkey 301 At this stage, as the posterior surface of the femur faces the body wall, its medial margin shifts to the cranial. The pubic (p) and ischiadic (i) bones are discriminated only as a process. The obturator foramen is not developed as yet. The muscular anlagen for each muscular group (E : extensor, I iliac, A: adductor, and F: flexor group) share their position at the proximal region of the femoral shaft. The area of the iliac anlage is distinct in the proximal region. The boundary of the dorsal and the ventral mass (M in Figure 7) runs through the cranial aspect of the thigh. Spinal nerves from the lumbar segment enter into the muscular mass and some of them may reach to underneath the skin. The muscular mass grows and expands to the distal along the shaft and opposite side from anteriorly (dorsally) by the extensor and posteriorly (ventrally) by the flexor anlagen, respectively, as shown by the large arrows in Figure 7. After these modifications have taken place, the thigh muscles have two ontogenetically discontinuous planes at their lateral and medial aspects. The lateral one (L in Figure 7) runs between the extensor and the flexor group. It is clearly defined in the adult thigh as the septum intermusculare femoris lateralis. The medial one (M in Figure 7) is not so clear as the former. The reason is that the extensor and the flexor come in contact with each other after migration to the opposite side in the lateral aspect of the thigh, On the other hand, the extensor and the adductor develop side by side. The vertical rank of the seven muscular groups in Figure 6 corresponds well to the situation of these anlagen in the proximal region of the femoral shaft in Figure 7. Further muscular elongation to the distal and the cleavage into each muscle also resemble the sequence of each row from left to right in Figure 6. They gain the distal insertion successively corresponding to the left to right sequence in the row. As mentioned above, the situation of Figure 6 bears a strong resemblance to the manner of muscular formation of the thigh during embryogenesis. The process of dual innervation in some thigh muscles can be reasonably explained on the basis of the classification of thigh muscles presented this study as shown in Figures 6 and 7. At the early period of thigh development, the muscular branch of a lumbar nerve intrudes into the given muscular anlage from their proximal plane. The boundary of the muscle may not be defined so precisely at this period. Boundaries are often extended or invade each other. Two compartments, having different nerve supplies, fuse together and form a dual innervated muscle. The dual innervation of the muscle appears at the marginal zone of two ontogenetically different muscular masses. In man, the m. semimembranosus accessorius is completely united with the m. adductor magnus. The former should be fused with the latter during embryogenesis in man. Similar ideas were proposed by Paterson (1894b) and Last (1949) for the upper and lower limb musculature in man. They explained the dual innervation of the m. pectineus and the short head of the m. biceps femoris in this way. These two were not observed in the present study. References 1) Bardeen, C. R. : Development and variation of the nerves and the musculature of the inferior extremity and the neighboring regions of the trunk in man. Amer. J. Anat., 6: , ) Dykeg, R. W. and Terzis, J. K.: Spinal nerve distributions in the upper limb. :

12 302 Y. Takahashi The organization of the dermatome and afferent myotome. Phil. Trans. R. Soc. London, B, 293: , ) Herringham, W. P.: The minute anatomy of the brachial plexus. Proc. R. Soc. London, B, 41 : , ) Howell, A. B. and Straus, Jr. W. L.: The muscular system. In : The Anatomy of the Rhesus Monkey. ed. by Hartman, C. G. and Straus, Jr. W. L., Williams and Wilkins, Baltimore, ) Kimura, K., Takahashi, Y. and Konishi, M.: Flexor muscles of the thigh of crab-eating monkeys (Macaca fascicularis). Primates, 21 : , ) Kimura, K., Takahashi, Y., Konishi, M. and Iwamoto, S.: Adductor muscles of the thigh of crab-eating monkeys (Macaca fascicularis). Primates, 22 : , ) Kimura, K., Takahashi, Y., Konishi, M. and Iwamoto, S.: Extensor muscles of the thigh of crab-eating monkeys (Macaca fascicularis). Primates, in press 8) Kimura, K. and Takai, S.: On the musculature of the forelimb of crabeating monkey. Primates, 11: , ) Kirk, E. J. and Denny-Brown, D.: Functional variation in dermatomes in the macaque monkey following dorsal root lesions. J. Comp. Neur., 139: , ) Kuhn, R. A.: Organization of tactile dermatomes in cat and monkey. J. Neurophysiol. 16: , ) Lance-Jones, C.: The morphogenesis of the thigh of the mouse with special reference to tetrapod muscle homologie. J. Morphol., 162: , ) Lance-Jones, C. and Landmesser, L.: Pathway selection by chick lumbosacral motoneurons during normal development. Proc. R. Soc. London, B, 214: 1-18, ) Landmesser, L.: The distribution of motoneurons supplying chick hind limb muscles. J. Physiol., 284: , 1978a. 14) Landmesser, L.: The development of motor projection patterns in the chick hind limb. J. Physiol., 284 : , 1978b. 15) Landmesser, L. and Morris, D. G. : The development of functional innervation in the hind limb of the chick embryo. J. Physiol., 249 : , ) Last, R. J. : Innervation of the limbs. J. Bone and Joint Surg., 31-B: , ) Miyazaki, R.: Anatomical studies on differentiation of muscles of thigh. Part II. Histological investigation on the muscles of the thigh in an embryo of 6 to 13 weeks old. Kagoshima Med. J. 32: , (in Japanese) 18) Paterson, A. M., The origin and distribution of the nerves to the lower limb. J. Anat., 28: 84-95, 1894a. 19) Paterson, A. M., The origin and distribution of the nerves to the lower limb. HI. Distribution of the nerves of the lumbo-sacral plexus. J. Anat., 28: , 1894b. 20) Sato, M.: La frua disvolvigo de lamembraj muskooj ce homa feto predipe pri la relato inter muskolo kaj nervo. Nippon Igaku Zasshi, 20: , (in Japanese) 21) Sherrington, C. S.: Experiments in the examination of the peripheral distribution of the fibers of the posterior roots of some spinal nerves. II. Phil. Trans. R. Soc. London, B, 190: , ) Takeuchi, R.: On the lumbar plexus of the rhesus monkey. Acta Anat. Nippon., 35: , (in Japanese) 23) Takeuchi, R.: On the sacral plexus of the rhesus monkey. Nippon Igaku Zasshi, 20: , (in Japanese) 24) Urbanowicz, Z.: The femoral nerve in man and in macacus. Acta Biol. et Med. Soc. Sc. Gedan., 17: 81-91, ) Urbanowicz, Z. and Zaluska, S.: Formation of the lumbar plexus in man and macaca. Folia Morphol. (Warcsz.) 28: , ) Uhlmann, K.: Cercopithecidae. In : HiiftundOberschenkelmuskulatur systematische und vergleichende Anatomie. Primatologia, vol. 4 (10) : , ed. by Hofer, H., Schultz, A. H. and Starck, D., Karger, Basel ) Waterman, H. C. : Studies on the evolu-

13 Thigh Muscle Constitution in the Crab-eating Monkey 303 tion of the pelvis of man and other primates. Bull. Amer. Mus. Nat. Hist., 58: , ) Zaluska, S.: The obturator nerve in man and macaca. Folia Morphol. (Warsaw), 30: 89-96, (in Polish) 29) Zaluska, S. and Urbanowicz, Z.: The tibial and common peroneal nerves in man and macaca. Folia Morphol. (Warsaw), 30: , ) Zaluska, S. and Urbanowicz, Z.: Origin of the sacral plexus in man and macacus. Acta Biol. et Med. Soc. Sc. Gedan., 17: , 1972.