Succinic Dehydrogenase Activity of Skeltral Muscle and Its Electrophysiological Function
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1 26 Succinic Dehydrogenase Activity of Skeltral Muscle and Its Electrophysiological Function Shusaku TSUICAMOTO and Masahiko MORI Department of Oral Surgery, Osaka University Dental School, Osaka. Introduction In order to pursue a spatial distribution of the white and the red muscle fibers in the skeletal muscles in mammals, applications of histochemical observations are made in reference to succinic dehydrogenase and other oxidative enzymes. There are obtained identical findings in enzyme histochemistry of the localization of succinic dehydrogenase5,10,12), that is, the red muscle fiber abundantly contains this enzyme, but, white fiber contains a small amount of dehydrogenase. An electrophysiological aspect related with the skeletal muscles and their innervation has been explained. In this experiment, we have shown a spatial distribution of succinic dehydogenase activity in the muscle fibers of the limbs and jaws of normal rats, rabbits and cats. Discussions have been made of relations between histochemical findings on the muscle and its electrophysiological function which is clearly clarified. Methods - Normal adult rats, rabbits and cats were used in this experiment. Under a deep anesthesia, M. gastrocnemius, M. soleus, M. quadriceps femoris, M. biceps femoris, M. masseter, M. temporalis, M. pterygoideus internus and M. digastricus (M. occipito-mandibularis of cat) of these animals were removed. Cross sections were made of muscle belly through a muscle entire cut at 10 and 20ƒÊ, thick in the cryostat at -20 Ž. These sections were incubated at 37 Ž for 20 minutes in a substrate solution described in the tnethod of Nachlas et al.10). Results In the succinic dehydrogenase activity of the muscles in mammals, the muscle fibers can be divided into three types, i. e. white fiber with a low succinic dehydrogenase activity, red fiber contained a high succinic dehydrogenase activity and medium fiber with an intermediate degree of succinic dehydrogenase activity. The fiber of a low amount of enzymatic activity, being with a large diameter, showed a slight or no reaction, while the fiber of a high activity, being with a small diameter, was stained dark blue. The fiber of an intermediate degree of the activity was stained purple showing an intermediate diameter. In the present study, the skeletal muscles employed were of two or three types of muscle fibers ; no fiber of a single type was
2 27 observed. M. gastrocnemius, M. quadriceps femoris and M. biceps femoris in three species, and M. masseter and M. digastricus in the cat consisted of three types of fibers. M. soleus of three animals, M. masseter in the rat and rabbit, M. temporalis in the rat and cat, M. pterygoideus internus in the rabbit and M. digastricus in the rat contained two types, red and medium of muscle fibers. Only M. digastricus in the rabbit showed a mixture of medium and white fibers. The distribution of three types of fibers in certain muscles was shown in Table 1. Concerning the same named muscles of three animals, there was no great difference among the percentages of three types of fibers of M. gastrocnemius, M. soleus, M. quadriceps femoris and M. biceps femoris. On the other hand, an increase of percentage of medium fibers and appearance of white fibers in M. masseter and M. digastricus were observed in the rat, rabbit and cat in descending order. Concerning functionally different muscles, M. gastrocnemius showed an increase of white muscle and M. soleus showed an increase of red muscle. In M. quadriceps femoris and M. biceps femoris which are known as antagonistic muscles, there was no great difference in the percentages of muscle fibers in the rat, rabbit and cat. Whereas, a comparison of M. masseter (jaw closing muscle) and M. digastricus (jaw opening muscle) in the cat, the percentage of white fibers in M. masseter was lower than that in M. digastricus ; and in the rabbit, M. masseter was composed of red and medium fibers but M. digatricus contained medium and white fiber. However, the percentage of three types of fibers of M. masseter and M. digastricus of the rat was almost the same. In the rabbit muscle, a spatial distribution of three types of fibers extending from the periphery to the depth in a cross section was determined. That is, the percentages of the fibers which are contained in a unit area (0.7 ~ Table 1. Percentages of three types of muscle fibers in each muscle.
3 mm) were continuously calculated. The percentage of white fibers in M. gastrconemius shows a marked decrease and that of red and medium fibers reveals a gradual increase in the central part (Fig. 1 a). Both M. soleus and M. masseter present a gradual decrease in the percentage of medium fibers and an increase in that of red fibers from the periphery to the depth (Fig. 1b and e). In M. quadriceps femoris and M. biceps femoris, the percentage of each type fiber is similar through the whole muscle (Fig. 1c and d). Specific patterns of the spatial distribution of each muscle fiber are demonstrated in M. pterygoideus internus (Fig. 1f). That is, medium fibers are markedly decreased and red fibers appear in the central portion and then intensely increase extending from the central part to the depth. In M. digastricus, white fibers show a descending curve and medium fibers show an ascending curve starting from the periphery to the depth (Fig. 1g). a b d e f g Ordinate indicates the percentages of three types of \red fiber muscle fibers and abscissa indicates the number of medium fiber \ a unit area from the periphery to the depth in a white fiber cross section of each muscle \. Fig. 1. Spatial distribution of each muscle fiber in the rabbit. Discussion In ancient years, several authors indicated the correlations between the muscle function and its histology. Regarding the activity of succinic dehydrogenase in the skeletal muscle, Wachstein and Meisel16) first stated that this enzyme showed different reactions depending upon different muscles of the rat and rabbit. They reported that the strongest reactive fiber was found in
4 29 masseter while less activity was found in the skeletal muscle, in agreement with the present results. The relationship between succinic dehydrogenase activity and the size of the fiber was first reported by Nachmias and Padykula11). Ogatai12) reported that three types of muscle fiber were found in muscles of certain mammals and other creatures. We indicated in agreement with Ogata's report, that the muscle fibers of the rat, rabbit and cat consist of three types, i. e., red, medium and white fibers, on the basis of succinic dehydrogenase activity. There have been numerous reports made concerning the physiological function of the muscle and muscle fiber. Ranvier18) demonstrated two types of muscle, white and red muscle, with discussion on the physiological difference between them. Denny-Brown" pointed out that the white muscle contains mostly white muscle fibers. Cooper and Eccles" reported that M. gastrocnemius shows a rapid contraction time, while M. soleus has a slow contraction time. It seems generally accepted that the pattern of contraction curve depends upon the rate of distribution of fibers in a muscle2). Recently, Tokizane15) functionally differentiated kinetic and tonic muscle fibers using the deviation in the discharge intervals of neuromuscular unit. And it was found that the maximal conduction velocity of the motor fiber in M. gastrocnemius is faster than that in the soleus nerve14). Granit et al.7,8) stated that there are two systems of ventral horn cells for extensor muscles, large phasic and small tonic cells. The specificity occurring after hyperpolarization in these two cells was reported by Eccles et al.6). These reports mentioned above indicate that the muscles are divided morphologically and functionally into two kinds and innervated by two systems of nerve fibers and motoneurones, and that they are composed of two types of muscle fibers. Hence, a question what physiological functions are referred to red, medium and white fibers, respectively, arises. Concerning this problem, Kondo9) postulated that white, medium and red muscle fibers correlate to phasic contraction, plastic tonus and contractile tonus, respectively. Buchthal1) indicated the existence of two or three different muscle fibers in the primary fascicle of a muscle by an electrophysiological method. Further attempt is keenly desired to clarify relations between the physiological function of muscle and the histochemical patterns of the three types of muscle fibers. A comparison among the same named muscles of limb muscles, M. gastrocnecnemius, M. soleus, M. quadriceps femoris and M. biceps femoris, resulted in no great difference in the proportion of the three types of muscle fibers in rat, rabbit and cat. Whereas, the proporion of the three types of muscle fibers of the jaw muscles, M. masseter and M. digastricus, varied according to different animals. An increase of medium fibers and the appearance of white fibers in the jaw muscles were most frequently observed in the rat, followed by rabbit and cat in order. As to the succinic dehydrogenase activity in the jaw muscles, Wachstein and Meisel16) demonstrated that M. masseter of rat and rabbit were composed of the muscle fibers which present the higher succinic dehydrogenase activity than in the limb muscle fibers. Therefore, these findings indicate that the proportion of each muscle fiber composing
5 30 the limb muscles is constant in these three animals. However, the proportion in the jaw muscles varied in these animals. From the present study of a spatial distribution of muscle fibers in vertebrates, it has never been reported in previous papers, that white muscle fibers are rather situated at the periphery and red muscle fibers rather at the central part of the muscle, although much distribution is not so clearly demonstrated. Summary 1. A histochemical study was made in the succinic dehydrogenase activity of M. gastrocnemius, M. soleus, M. quadriceps femoris, M. biceps femoris, M. masseter, M. temporalis, M. pterygoideus internus and M. digastricus in rat, rabbit and cat. 2. By the succinic dehydrogenase activity, the muscle fibers were divided into three types, i. e., white muscle fibers with a low enzymatic activity, red muscle fiber with a high enzymatic activity and medium muscle fiber with an intermediate enzymatic activity. The muscle studied were composed of two or three types of muscle fibers, and never of a single type of fiber. 3. The proportion of three types of muscle fibers varied in different muscles. 4. Extending from the periphery to the depth of the muscle, a spatial distribution of these types of muscle fibers was observed in rabbit. 5. It is asserted that the same named muscles of the limb have a constant proportion of these muscle fibers in rat, rabbit and cat, and that the proportion in jaw muscles varied in different animals. 6. Relations between the histochemical results obtained and electrophysio logical events in skeletal muscles were discussed. References 1) Buchthal, F. An Introduction to Electromyograraphy. Scandinavian University Books, 44p (1957). 2) Cobb, S. Physiol. Rec., 5, (1925). 3) Cooper, S. and Eccles, J. C. J. Physiol., 69, (1930). 4) Denny-Brown, D. E. Proc. Roy. Soc. (London), Series B., 104, (1929). 5) Dubowitz, V. and Pearse, A. G. E. Histochemie, 2, (1960). 6) Eccles, J. C., Eccles, R. M. and Lundberg, A. Nature, 179, (1957). 7) Granit, R., Menatsch, H. -D. and Steg, G. Acta Physiol. Scand., 37, (1956). 8) Granit, R., Phillips, C. G., Skoglund, S. and Steg, G. J. Neuropnysiol., 20, (1957). 9) Kondo, M. Okayama Igakkai Zassi, 71, (1959) (in japanease). 10) Nachlas, M. M., Tsou, K. C., Souza, E. D., Cheng, C. H. and Seligman, A. M. J. Histochem. Cytochem., 5, (1957). 11) Nachmias, V. T. and Padykula, H. A. J. Biophysic. and Biochem. Cytlo., 4, (1958). 12) Ogata, T. Acta Medicinae Okayama, 12, (1958). 13) Ranvier, L. Lecons d' Anatomic Generale sur le Systeme Musculaire. Paris. (1880). 14) Sumi, H. Seitainokagaku, 11, (1960) (in japanese). 15) Tokizane, T. and Tsuyama, N. Clinical EMG, Kyodo Isho Shuppan Sha, (1956). (in japanese). 16) Wachstein, M. and Meisel, E. J. biophys. biochem. Cytol., 1, (1955).
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