Fiber Type Composition of Abdominal Muscles in Japanese Macaques(Macaca fuscata) Junji ITO

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1 Okajimas Folia Anat. Jpn., 74(6): , March, 1998 Fiber Type Composition of Abdominal Muscles in Japanese Macaques(Macaca fuscata) By Junji ITO Department of Anatomy, Showa University School of Medicine, Hatanodai, Shinagawa-ku, Tokyo , Japan -Received for Publication, September 29, Key Words: Muscle fiber type, Fiber type composition, Abdominal muscle, Japanese macaque Summary: The muscle fiber composition and cross-sectional area of muscle fiber types were investigated histochemically in the abdominal muscles (rectus abdominis muscle, obliquus externus abdominis muscle, obliquus internus abdominis muscle and transversus abdominis muscle) of three Japanese macaques (Macaca fuscata). Muscle fibers were classified into three fiber types (Type I, II A and II B) by myosin ATPase activity and succinate dehydrogenase activity. Each abdominal musde in Japanese macaques contained high proportion of Type II B fibers and there were no large differences in the fiber type composition between the abdominal muscles. The range of mean fiber type percent was 26-32% Type I, 21-22% Type II A, and 46-52% Type II B fibers. Thus, based on the histochemical fiber type composition, the separate abdominal musdes appear to have a similar functional capacity. The cross-sectional area was larger for Type II than for Type I fibers, and the areas were similar in Type II A and Type II B fibers in each muscle. The rectus abdominis showed larger fibers of each type compared to the lateral abdominal muscles. The high proportion of Type II B fibers and large fiber size for Type II B fibers suggest that the abdominal muscles of Japanese macaques have properties similar to the propulsive and locomotory muscles in the limbs. Skeletal muscle fibers in mammals have been classified commonly into three types, as Types I, II A and II B (Brooke and Kaiser, 1970) or as slow-twitch/oxidative (SO), fast-twitch/oxidative/ glycolytic (FOG), and fast-twitch/glycolytic (FG) types (Peter et al., 1972), based on differences in their histochemical, biochemical and physiological profiles. The composition of fiber types in skeletal muscles varies from muscle to muscle, and the fiber type composition of a muscle gives an indication of its functional capacity, with postural and antigravity muscles contains many Type I fibers and propulsive and locomotory muscles contains many Type II fibers (Ariano et al, 1973; Armstrong et al., 1982; Petter and Jouffroy, 1993). There is abundant information about fiber type composition of the locomotory fore- or hind limb muscles, but information is scarce regarding the trunk muscles. The muscles of the abdominal wall (rectus abdominis muscle, RA; obliquus extemus abdominis muscle, OE; obliquus internus abdominis muscle, CM and transversus abdominis muscle, Tr) regulate the pressure within the abdominal cavity and control the movements of the trunk and pelvis supporting locomotion. The regulation of the intra-abdominal pressure contributes to respiration, defection, vomiting and parturition, and the movement control contributes to flexion, rotation and deflection of the trunk and pelvis, which are involved in climbing, jumping, walking and running in the primate's terrestrial and arboreal habitat. Differences in the anatomical arrangement among the four abdominal muscles would influence their separate contributions to these functions. In this study, to investigate the functional capacity of the abdominal muscles in Japanese macaques, we analyzed the fiber type composition and fiber size for the separate abdominal muscles and compared the results with those for the hind limb muscles in the same macaques. Materials and Methods Muscle samples were obtained from three Japanese macaques (Macaca fuscata) kept at the Primate Research Institute of Kyoto University (Table 1). Whole transverse sections (1 cm thick) of the RA and rectangular sections (1 x 3 cm sides) of the OE, OI, and Tr were taken at the umbilical 199

2 200 J. Ito Table 1. Age and body weight of Japanese macaques examined level. Muscle samples were embedded in Tissue- Tek OCT compound (Miles Inc., USA), and frozen in a mixture of acetone and dry ice. Serial sections (10pm thick) were cut on a cryostat at 20 C and stained for myosin ATPase after two different preincubation procedures (ph 4.3 and 10.5) according to the methods described by Guth and Samaha (1969). Other sections were stained for succinate dehydrogenase (SDH) activity (Nachlas et al., 1957). Based on the ATPase reaction, the muscle fibers were classified into main two types: Type I, darkly stained after acid preincubation and lightly stained after alkaline preincubation, and Type II, with staining pattern opposite to that for Type I fibers. The Type II fibers were then subclassified as either Type II A, which react more strongly on SDH reaction, or as Type II B, which react weakly on SDH reaction. Classification of fiber types, counting of fiber type proportions (percentage fibers of each fiber type, % fibers) and measurement of the crosssectional area (fiber size) were performed using photomicrographs of serial sections. For some of the hind limb muscles [gastrocnemius muscle lateral head (GL) and medial head (GM); soleus muscle (Sol); plantaris muscle (P1); tibialis anterior muscle (TA) and extensor digitorum longus muscle (EDL)] in the same macaque, the muscle fibers were classified into Type I and Type II fibers by the same methods as used for the abdominal muscles. Results Composition by muscle fiber types (% fibers) The three types of muscle fibers could be distinguished in the abdominal muscles of the Japanese macaques. Fibers that could not be classified into three types (Type II C; stained darkly after acid and after alkaline preincubation) accounted for less than 3% of the total number of muscle fibers, and data for them were not included in the analysis. The different fiber types were, in general, evenly distributed across the muscle cross-sections in all abdominal muscles. The proportions (% fibers) of muscle fiber types in the abdominal and the leg muscles of individual Japanese macaques are shown in Table 2. Each abdominal muscle contained high proportion of Type II B fibers except the RA and CH in Ml, contained more Type I fibers. The proportion of Type II B fibers in the RA ranged from 32.5 to 54.2%, from 36.0 to 56.3% in the OE, from 30.9 to 58.3% in the CH and from 36.8 to 59.7% in the Tr. The ranges of the mean fiber type proportions in the abdominal muscles were 26-32% Type I, 21-22% Type II A, and 46-52% Type II B fibers and the large differences in the fiber type composition between the abdominal muscles were not observed. The comparison of the fiber type composition in the abdominal muscles with those in the hind limb muscles (GM, GL, Sol, Pl, TA and EDL) in individual Japanese macaques is shown in Figure 1. Of the leg muscles, the Sol contained the highest percentage Type I fibers (about 80%) and the other leg muscles, like the abdominal muscles, consisted mainly of Type II fibers ( %). Cross-sectional areas of muscle fibers by types The muscle fiber sizes of each type in the abdominal muscles are shown in Table 3 and Figure 2. Of the fiber types, the Type I fibers were the smallest except for those in the Tr in Ml. The difference of fiber size is expressed as the area ratio in Table 4. The area ratios of Type II to Type I fibers (Type II/Type I) ranged from 1.4 to 2.7. Type II A fibers were similar to or slightly larger in area than Type II B fibers (area ratio range: ). Among the three macaques, M1 had the largest fiber size in each muscle. Of the abdominal muscles, the RA showed larger muscle fibers of each type than did the lateral abdominal muscles (OE, OI and Tr) in each macaque. Discussion The skeletal muscle fibers have been classified into three types in most mammals except the house shrew (Suzuki, 1990), slow loris (Sickles and Pinkstaff, 1981a, b) and dog (Snow et al., 1982) which respectively lack Type I, FG and Type II B fibers. In the present study, the three types of muscle fibers (Type I, II A and II B) could be distinguished in the abdominal muscles of Japanese macaques, as have

3 Muscle Fiber Composition in Macaque Abdominal Muscle 201 Table 2. Proportion (%) of muscle fiber types in the abdominal and the hindlimb muscles of individual Japanese macaques. The muscle fibers in abdominal muscles were classified into three types and those in the leg muscles into two types * RA, rectus abdominis muscle; OE, obliquus externus abdominis muscle; OI, obliquus internus abdominis muscle; Tr, transversus abdominis muscle; GL, gastrocnemius muscle lateral head and GM, medial head; Sol, soleus muscle; Pl, plantaris muscle; TA, tibialis anterior muscle; EDL, extensor digitorum longus muscle. **The Sol in Ml could not be examined. been observed in the leg (Suzuki and Hayama, 1994) and epaxial muscles (Kojima and Okada, 1996) in this species. The fiber type composition in each muscle gives an indication of its functional capacity. Of the limb muscles, the postural and antigravity muscles, such as the vastus intermedius or soleus, show high percentage of Type I fibers whereas the propulsive and locomotory muscles show low percentage of Type I and high percentage of Type II B fibers (Arian et al., 1973; Armstrong et al., 1982; Petter and Jouffroy, 1993). In nonlocomotor muscles, the heart, diaphragm and masseter which are continuously active or often in use have a high proportion of Type I fibers. In contrast, the cutaneus trunci, one of the instant active muscles, has the largest proportion of Type II B fibers (Karlatriim et al., 1994). In this study, each abdominal muscle in Japanese macaques contained high proportion of Type II B fibers and there were no large differences in the fiber type composition between the abdominal muscles. Thus, based on the histochemical fiber type composition, the separate abdominal muscles appear to have a similar functional capacity. The abdominal muscles in these Japanese macaques showed the similar proportion to those in the hindlimb muscles except the Sol in the same macaque. The low % fibers of Type I and the high % fibers of Type II B suggest that the abdominal muscles in Japanese macaques have similar character to the propulsive and locomotory muscles in the limb. Among other species, humans show % fibers of Type I of 55-58% in the abdominal muscles (Haggmark and Thorstensson, 1979) and dogs show that of 48-59% (Armstrong et al, 1982). The differences of the proportion of Type I fiber in the abdominal muscles among the three species are possibly due to their characteristic locomotion patterns. Macaques engage in quadrupedal locomotion in terrestrial or arboreal space involving climbing and jumping, human locomotion is bipedalism in erect posture, and dogs belong in terrestrial quadr-

4 202 J. Ito Fig. 1. Fiber type composition in the abdominal and the leg muscles of individual Japanese macaques. The percentages, expressed as quantities, of each fiber type and the abbreviations for the muscles are shown in Table 2. Table 3. Cross-sectional area (pm2) of muscle fibers in the abdominal muscles of individual Japanese macaques * Muscle names are abbreviated as in Table 2. pedal locomotion. Crab-eating macaques, which show similar locomotion to Japanese macaques, have high % fibers of Type II in the abdominal muscles (Inokuchi et al., 1990). Most limb muscles show regional variations in the fiber type composition within the muscle, with the proportion of Type I fibers increasing toward the deeper layer and that of Type II fibers declining. Furthermore, the deeply located muscles contain more Type I fibers than do the superficially located muscles (Acosta and Roy, 1987; McIntosh et al, 1985). These intra-muscle and inter-muscle

5 Muscle Fiber Composition in Macaque Abdominal Muscle 203 Fig. 2. Cross-sectional area of fibers of each type in the abdominal muscles of individual Japanese macaques. Table 4. Area ratios of muscle fibers of each type in the abdominal muscles of individual Japanese macaques * Muscle names are abbreviated as in Table 2. variations in the fiber type distribution are not observed in the abdominal muscles of Japanese macaques, humans, or dogs. In this study, the muscle specimens of the lateral abdominal muscles were all obtained at the umbilical level. Variation in fiber type composition may exist in the different parts of the lateral abdominal muscles, as in the human trapezius muscle (Lindman et al., 1990, 1991). Interindividual differences in fiber type composition are observed in the macaques leg (Suzuki and Hayama, 1994) and epaxial muscles (Kojima and Okada, 1996) and in the human trapezius muscles (Lindman et al, 1990). Lindman et al. (1990) have suggested that interindividual differences in fiber type composition in human muscles are due, at least in part, to genetic factors. Suzulci and Hayama

6 204 J. Ito (1994) pointed out the potential transformation of fiber types in the Japanese macaque caused by postural or locomotory requirements in the life environment. In this study, the fiber type composition in adult M1 differed from those in younger M2 and M3. Interindividual differences in fiber types may be due to differences between the locomotory patterns in young and adult animals. Suspensory activities in Japanese macaques are known to change with transition from young to adulthood (Chatani, 1996). Muscle fibers also undergo transformation from Type II to Type I during the postnatal growth period. The growth-associated transformation of fiber types is presumed to be completed by 6 years of age in Japanese macaques. In this study, M2 and M3, both under 4 years, may have had on-going transformation of fiber type. The Type II fibers showed larger cross-sectional area than that of Type I fibers in the abdominal muscles of Japanese macaques as in the other limb muscles. The fiber size difference between Type II A and Type II B fibers was slight. In general, Type II B fibers have a large fiber area in the propulsive locomotory muscles of the limb, Type II A fibers show intermediate area, and Type I fibers show smallarea (Newsholme et al., 1988). Postural muscles in the pectoral girdle, which are required for stabilizing the shoulder and brachium and for supporting the trunk, contain high percentage of SO fibers, and SO fibers of large fiber size (Suzuki, 1991). Totland and Kryvi (1991)indicated a covariation between the proportion of Type I and Type II fibers and their cross-sectional area. This indication is consistent with our observations in the abdominal muscles of Japanese macaques. The high proportion and large fiber size of Type II B fibers indicate that the abdominal muscles of these macaques have the character of muscles with the primary function of powerful contraction, and seem to contribute chiefly to the movement of the trunk and pelvis. Type II A fibers, which show fiber size as large as that of Type II B fibers, would function well to regulate the intra-abdominal pressure because of their resistance to fatigue. Among the three macaques, M1 showed abdominal muscles consisting of larger fibers of each type compared to the other two macaques. This difference is due to the development of body mass with growth that is observed in skeletal muscles generally (Moore et al., 1971). Muscle fiber area is known to be related to muscle use and force. The area of muscle fibers increases with training and decreases with inactivity (Inokuchi et al, 1980). In these Japanese macaques, the RA had the largest muscle fiber size of each fiber type among the abdominal muscles examined. This result shows that the load and power of the RA is greater than those of the lateral abdominal muscles (OE, CH and Tr) during muscle movement. Of the human abdominal muscles, the CH has the largest muscle fibers (Ito and Inokuchi, 1989). 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