Comparative Morphology of Skeletal Muscles in Man and Macaque

Transcription

1 Showa Univ. 1. Med. Sci. 5(2), , December 1993 Review Comparative Morphology of Skeletal Muscles in Man Macaque Seuchiro INOKUCHI, Tadanao KIMURA, Masataka Suzuiu, Junji ITO Hiroo KUMAKURA Abstract: Anatomical features (shape, weight myofibrous composition) of skeletal muscles reflect the muscular functions. In this study, we histologically analyzed the myofibrous composition of corresponding muscles compared their functions in man the macaque. Among the intrinsic h foot muscles, the h muscles for gripping pinching movements were well developed in humans those for hanging were well developed in the hs feet of the macaque. Of the spinohumeral muscles, morphological differences (thickness of muscle layer muscle fiber size) were observed in different regions. In the muscles in the upper lower extremities, the relative weight myofibrous composition were correlated with the characteristics of their respective motions. There were differences in myofibrous composition among those muscle groups due to bipedal or quadrupedal walking by man the macaque. The differences in the myofibrous composition of the muscles for vocalization (laryngeal muscles), the innervation ratios of the muscle fibers reflected vocal ability. Key words: comparative anatomy, muscle composition, skeletal muscle, macaque Introduction In general, the number the thickness of skeletal muscle fibers vary within each muscle, due to differences in functions. Muscle fibers are known to be thicker in muscles engaged in powerful movements thinner in muscles engaged in fine movements1. On the other h, muscle fibers are divided histochemically into 3 types, type I, type II intermediate type2). Fig. 1 shows a muscle section stained with Sudan Black B. The thinner type I fibers, the so-called red fibers or slow twitch fibers, are stained black. The thicker type II fibers, the so-called white fibers or fast twitch fibers, are not stained. The occurrence of the three types of muscle fibers in a given muscle varies among species. In this paper, the differences of muscle fiber composition are compared in some muscles of the human macaque. Materials Methods For the muscle fiber composition of the muscle, the number, the size the density of muscle fibers were estimated for transverse muscle sections. The muscle samples from Department of Anatomy, Showa University School o f Medicine, Hatanodai, Shinagawa-ku, Tokyo 142, Japan,

2 138 Seiichiro Fig. extremities 20 Đm were thickness laryngeal fibers were Results 1. routinely muscles 1. were differentiated Muscle fibers fixed in stained with embedded into stained by formalin, types: gelatin Sudan Black embedded hematoxylin in 3 INOKUCHI, et al. Type I, stained II B in eosin with ( ~ 200). celloidin, (H.E.) Sudan cross-sectioned dye. Black The B, into samples the from muscle intermediate. Discussion Lower extremity muscles3) Figure 2 shows the total number the size of muscle fibers in the femoral muscle of man the macaque. They were generally rather thin in macaques comparatively thick in humans. According to the individual differences, muscles were divided into four groups: those in which the total number the size of the muscle fiber were much larger in man (e.g. mm. vastus lateralis, adductor longus adductor brevis); those in which the size in macaques was almost the same as in man (e.g. mm. semitendinosus, rectus femoris gracilis); those in which the total number in macaques was almost the same as in man (such as mm. vastus intermedius); those in which there were no remarkable differences between humans macaques (this group ircluded the biceps femoris sartorius muscle). From these comparisons, it can be generalized that the bi-articular muscles of the macaque are equivalent to those in man, whereas there is a tendency for the other macaque femoral muscles to be fewer have thinner fibers than those in humans. In the lower leg, shown in Fig. 3, three muscle types can be observed. These are muscles corresponding to the vastus lateralis type (mm. gastrocnemius, soleus, tibialis anterior); those of the vastus intermedius type (mm. extensor hallucis longus, extensor digitorum longus, plantaris, flexor hallucis longus fiburalis brevis); those comparable to m. biceps femoris (mm. popliteus, fibularis longus, tibialis posterior flexor digitorum longus). Muscles that differ widely in myofibrous composition between man macaque are

3 Skeletal Muscles in Man Macaque 139 Fig. 2. Comparison between the total number the size of muscle fibers of thigh muscles in the macaque ( ~) in humans ( œ). Fig. 3. Comparison between the total number the size of muscle fibers of the lower leg muscles in the macaque ( ~) in humans ( œ). those that participate in special functions of the lower extremities, e.g. bipedalism in man quadripedalism in the macaque. 2. Foot muscles4,5) Table 1 is a comparison of the total numbers of muscle fibers in the muscle groups of the foot. In the thenar muscle the dorsal interossei, the number of muscle fibers was slightly higher in racaques, but those of the flexor hypothenar muscles were much

4 140 Seiichiro INOKUCHI, et al. Table 1. Total number of muscle fibers in foot muscles in humans macaque. m.f.: muscle fiber. Fig. 4. Muscle fiber size of foot muscles in the humans macaque. lower than in humans. These differences obviously are due to prehensility in macaques to bipedal walking in man. The average size of muscle fibers in the foot muscles is shown in Fig. 4. In macaques, the highest values are around 2000 Đm2 were found in the m, interosseus plantaris I, in the oblique transverse heads of the m. adductor hallucis muscle. These muscles act to close the toe grip (gather the toe). In man, the fibers of the m. adductor hallucis flexor hallucis brevis reach the size of 3000 Đm2. The fiber size in the m. flexor brevis digiti

5 Skeletal Muscles in Man Macaque 141 Table 2. Total number of muscle fibers in h muscles of humans macaque. m.f.: muscle fiber. Fig. 5. Mean size of muscle fibers of h muscles in the human macaque. I, II are around 2500 Đm2, they are much thicker than the fibers of the conesponding muscles in the macaque foot. This strong development of the muscles may indicate the kick exerted by digiti I II to produce propelling force in bipedal walking. 3. H muscles6 Table 2 is a comparison of the total numbers of muscle fibers in the h muscles in man macaque. In the monkey, the thenar muscle possesses relatively fewer, the hypothenar muscles relatively more fibers than in humans. Figure 5 shows the mean size of the muscle fibers in the h muscles. In the macaque h, the thickest fibers (about 2000 Đm2) were found in the m, interosseus plantaris I, II

6 142 Seiichiro INOKucHI, et a!. Table 3. Comparison of the thickness of muscle layer of truncobranchial muscles in humans macaque. Table 4. Comparison of the muscle fiber size of truncobranchial muscles humans macaque.

7 Skeletal Muscles in Man Macaque 143 Table 5. Comparison of the relative weight of the upper extremity muscle group on macaque humans. m. contrahens digitorum III. In the human h, the largest values (1700 Đm2) occur in the m. interosseus dorsalis I. Consequently, each of these muscle fibers in the macaque were thicker than those in humans. 4. Truncobrachial muscles7,8) Regarding the truncobrachial muscles, the thickness of the muscle layer, as can be seen from Table 3, is largest in the cranial portion of the anterior serratus muscle, the intermediate portion of the m. trapezius the cranial portion of the m. rhomboideus major in humans. In the macaque, however, it was largest in the caudal portions of the anterior serratus muscle, the trapezius the rhomboideus. The thickness of muscle fibers in the human truncobrachial muscles are shown in Table 4. It is the greatest in the cranial portion of the m. serratus anterior, in the intermediate portion of the trapezius muscle the cranial portion of the m. rhomboideus. The white muscle fibers in the same muscles of the macaque are largest in the caudal portions of all muscles. The results suggest that the parts of the muscles that are enhanced in humans are those that are used for lifting objects in macaques those that are used to suspend the trunk on the forelimb. 5. Upper extremity muscles9,10) Table 5 sets out the proportions of muscle groups on the free upper extremities. The data include information about the chimpanzee. The extensors of the elbow joint occupy the highest proportion in humans, followed by the flexors of the elbow flexors of the wrist finger which have similar values. In macaques, the extensors of the elbow the flexors of the wrist h have similar values; no difference was found between the flexors of the elbow the extensors of the wrist fingers. The relative weights of individual muscles in the upper extremity muscles are summarized in Fig. 6. The branchial triceps muscle is the largest, occupying 30.6%. This is followed by the mm. brachialis, biceps brachii, the deep digital flexors the superficial digital flexors. It is tempting to relate the marked development of the extensors of the upper arm in humans to the throwing movement the finger flexors, next in size, probably participate in the powerful movement of the h by flexing the fingers or wrists. 6. Laryngeal muscle11-13) In Fig. 7, the percentages of the three types of muscle fibers in the laryngeal muscles are shown. In man, the red fibers occupy about 40%, which is much more than in the macaque. On the other h, in macaques, the white fibers occupy about 50% this ratio is almost equal to that of the lower extremity muscles. The laryngeal muscles of humans are better equipped with red fibers tonic elements, whereas those of macaques contain

8 144 Seiichiro INOKucm, et al. Fig. 6. Percentage of total muscle weight on the upper extremity in the human macaque. Fig. 7. Comparison of the percentage of 3 muscle fiber types in laryngeal muscles in humans crab-eating macaque,

9 Skeletal Muscles in Man Macaque 145 Fig. 8. Comparison of the size of red muscle fibers in each laryngeal muscle of primates dog. Table 6. Comparison of the relations between the number of muscle fibers nerve fibers of laryngeal muscles in humans macaque. m.f: muscle fibre, n.f.: nerve fiber, m/n: number of m.f./number of n.f. more white fibers physic elements. Figure 8 shows the mean diameters of laryngeal muscle fibers in several species. In macaques, the fibers are thinner than in man. This seems to be related to the loudness of the voice. Table 6 shows the number of muscle fibers of myelinated nerve fibers in the laryngeal muscles. The number of muscle fibers innervated per nerve fiber is larger in macaques than

10 1.46 Seiichiro INoxucHI, et al. in humans. In other words, each laryngeal muscle of the macaque is less densely innervated than those of man. Therefore it is more difficult for the monkey to produce complicated, modulated sounds as humans do in speaking. In general the number of the muscle fibers depending on one nerve fiber is larger in the muscles engaged in gross movements smaller in muscle engaged in fine movement, the range of variation being in lower extremity muscles 2-5 in ocular muscles. References 1) Kohashi Y: Histologische Untersuchungen der verschiedenen Skelettmuskeln beim Menschen. I. Untersuchunnen beim Erwachsenen. Folia Anal Jpn, 15: (1937) 2) Kimura T lnokuchi S: Distribution pattern of muscle fiber type in musculus biceps brachii of white-hed gibbon. J Anthropol Soc Nippon, 93: (1985) 3) Kimura T: Myofibrous development of the lower extremity muscles of rhesus monkey (Macaca mulatta). J Showa Med Assoc, 38: (1978) (in Japanese, English abstract) 4) Nakanishi H: Studies on myofibrous organization of intrinsic muscles in human foot. J Showa Med Assoc. 41: (1981) (in Japanese, English abstract) 5) Suzuki M, lnokuchi S, Nakanishi H, Ajiri T, Kimura T Matsumoto Y: Comparative anatomical studies of myofibrous organization of monkey aid human h foot muscles-especially monkey foot muscles-. J Showa Med Assoc, 42: (1982) (in Japanese, English abstract) 6) Ajiri T: Comparative study on muscle fiber organization in human h muscles. J Showa Med Assoc, 41: (1981) (in Japanese, English abstract) 7) Ito R, Ihara K, Onda S, Kimura T, Ajiri T, Nakanishi H Inokuchi S: Myofibrous organization of spinohumeral muscles in crab-eating monkey. J Showa Med Assoc, 40: (1980) (in Japanese, English abstract) 8) Ito R: Studies on the myofibrous organization of human spinohumeral muscles. J Showa Med Assoc, 43: (1983) (in Japanese, English abstract) 9) Kaneuchi Y, Inokuchi S, Ito R Matsuyama Y: Relative weight myofibrous organization of the upper extremity muscles in primates, in reference to a comparison with pig-tailed macaque. J Showa Med Assoc, 44: (1984) (in Japanese, English abstract) 10) Teratani T, Ito J, Ito R, Inokuchi S Matsuyama Y: Studies on the myofibrous organization of upper extremity muscles in man-comparison of the function of upper extremity in man monkey. J Showa Med Assoc, 45: (1985) (in Japanese, English abstract) 11) Sato I Inokuchi S: Myofibrous organization of human laryngeal muscles. J Anthropol Soc Nippon, 93: (1985) (in Japanese, English abstract) 12) Matsumoto Y, Sato I, Onda S, Yasumuro T Inokuchi S: Comparative studies of myofibrous organization of the laryngeal muscles. 1. Human crab-eating monkey. J S/iowa Med Assoc, 46: (1986) (in Japanese, English abstract) 13) Mimaru 0, Sato I, Inokuchi S, Suzuki M, Ito J Kumakura H: Comparative studies of the myofibrous organization in laryngeal muscle. 2. Galago, Japanese monkey chimpanzee. Anthropol Rep, 45: 1-10 (1988) (in Japanese, English abstract) [Received June 30, 1993: Accepted July 16, 1993]