Differential Fatiguability between the One and Two-Joint Muscles
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1 Differential Fatiguability between the One and Two-Joint Muscles Masahiko SATO*, Atsushi HAYAMI** and Haruhiko SATO** Since the end of the nineteen-twenties, it has long been known that the skeletal muscles of the mammalian are of two kinds, red and pale, the former is tonic and the latter phasic (DENNY-BROWN 1929 a, b ; CREED et al. 1932). In the human, from analyses of activities of many neuro-muscular units, TOKIZANE (1955) pointed out that deeper muscles were of tonic nature and superficial muscles were phasic, and he suggested that the one- and two-joint muscles were generally correspondent to deeper and superficial muscles respectively. Attempting to find the difference in fatigue between one- and two-joint muscles, KoNDo and his associates investigated changes in the ratios of 25 cps component to 48 cps component, during isometric contractions of the vastus medialis and the rectus femoris, with band pass filters having the peak at 25 cps and 48 cps respectively and an integrator. From the results that there was little significant change in the ratio for the vastus medialis whereas the ratio for the rectus lemons increased in the course of time, they concluded that the two-joint muscle was much more f atiguable as compared with the one-joint muscle (KONDO 1960; KoNDO & SATO 1960). Recently, as the general knowledge concerning the frequency spectra of the electromyogram (EMG) advanced, it was gradually disclosed that there were some problems in the evaluation of the muscle fatigue by the lowering in the frequency spectra. The present study was designed to confirm the differential f atiguability between the one- and two-joint muscles by means of using improved technics of the frequency analysis and adding the other synergistically operating pairs of one- and two-joint muscles to the pair of the knee extensors. METHODS Six normal healthy adults were examined for this study. Action potentials were recorded simultaneously from each pair of elbow flexors (M. biceps brachii and M. brachioradialis), knee extensors (M. rectus lemons and M. vastus medialis, in some cases M. vastus lateralis was added), or ankle extensors (M. gastrocnemius and M, soleus), with bipolar surface electrodes put in parallel with the direction of muscle fibers. The interelectrodes distance was about 3 cm. Sustained isometric contractions were performed by supporting a load in cases of the elbow This study was partialy financed by a grant from the Ministry of Education.
2 Differential Fatiguability between the One and Two-Joint Muscles 83 flexors and the knee extensors and by rising up on the toes of one leg in the case of the ankle extensors. The global EMG was analyzed by an automatic frequency analyzing integrator which has seven separate filtering frequency bands, i. e. 0-20, 20-40, 40-60, , , , 300-0o cps, whose frequency characteristics have already been described (SATO 1964). Integration time was five seconds which was enough to obtain steady frequency spectra (KoGI & HA- KAMADA 1962). The analyzing integrator had been made for one channel, and it could not analyze activities of two muscles at once. Therefore, when the frequency components of the EMG of two muscles or more were compared, the Fig. 1 Validity of the electrodes sites for the gastrocnemius and the soleus is verified by respective clear records of EMG from both the muscles. these muscles were chosen (Fig. 1). global EMG of test muscles had to be analyzed alternately, and averages of the integrated values were calculated for every continuous analyses of each muscle. As for the ankle extensors, the electrode positions which indicated the clearest record of each activity of The biceps brachii, the rectus f emoris, and the gastrocnemius are all known anatomically to cross two joints and electromyographically to have action on both joints. RESULTS It is general understanding that the EMG led with surface electrodes increases. and its frequency spectra deviate towards lower ranges as muscle fatigue progresses. Recently, it was found that frequency spectra of the EMG were modified by the electrode condition and that the lowering in the spectra could be producedd by simply lengthening test muscles without NADA et al. 1965; NoMIYA et al. 1965). the present investigation, the length any relation to the fatigue (SATO 1964; SA- Sni- In of test muscles and the electrode condition were maintained as constant as possible during each experiment. NASTOS MEDIALIS RECTOS FEMORIS Fig. 2 Changes in the ratios of each frequency component to the total electrical activities are indicated continuously until the end of the contraction of the vastus. medialis (left) and that of the rectus femoris (right). Numbers to the right of each line correspond to frequency bands of the analyzer used respectively. Note that there is little significant difference in the degree of the lowering between both test muscles. (15)
3 84 Masahiko SATO, Atsushi HAYAMI and Haruhiko SATO RECTUS FEMORIS VASTUS LATERALIS VASTUS MEDIALIS Fig. 3. Changes in the ratios of each frequency component to the total activities of the rectus femoris (left), the vastus lateralis (centre), and the vastus medialis (right) are shown during a knee extension endured until the 'exhaustion'. Marks to the left of each line correspond to the elapsed time after the beginning of the contraction as shown in the respective insets. Note that the lowering in the spectra is rather little in the rectus femoris as compared with that in the synergistically operating one-joint muscles. The experiment began with the intention of confirming the previous results TOTAL ACTIVITIES A: RECTOS FE1IORIS B: VASTUS LATERALIS C: VASTUS MEDIALIS Fig. 4 Comparison of the total activities between the rectus f emoris (A), the vastus lateralis (B), and the vastus medialis (C) during the same contraction to the previous figure. The activities are larger in order of B, A, and C. (KONiDO 1960; KONDO & SATO 1960) using the same posture and electrode sites for the quadriceps femoris. Continuous changes in the ratios of each frequency component to the total electrical activities were compared between the vastus medialis and the rectus femoris (Fig. 2). As apparent from the figure the lowering was observed in both muscles to almost the same extent. In some cases change in the frequency spectra of the EMG of the vastus lateralis was simultaneously compared with them (Fig. 3). The lowering seemed to be rather marked in the vastus lateralis than in the rectus f emoris. Throughout all the present experiments, any remarkable difference could not be detected between the lowering in the spectra of the rectus femoris and that of the synergistically operating one-joint muscles. These results differ from those obtained by KONDO and his associates. Changes in the total discharges of the test muscles were also investigated during (16)
4 Differential Fatiguability between the One and Two-Joint Muscles 85 the fatiguing contractions (Fig. 4). Transient decreases in the total activities were frequently observed in the onset of the contraction as already pointed out (EDWARDS & LIPPOLD 1956; LIPPOLD et al. 1960). As shown in the figure, a gradual decrease in the total activities of the vastus lateralis was indicated during fatiguing contraction together with the lowering in the frequency spectra. However, this sort of decrease in the activity seems to have no positive significance as the indica- BICEPS BEACHII BRACHIORADIALIS Fig. 5 Changes in the ratios of each frequency component to the total activities of the biceps brachii (left) and the brachioradialis (right) are indicated during an isometric flexion. of the elbow joint. Almost the same degree of the lowering is observed in changes in the spectra of both the muscles. tion of the fatigue (SATO 1965). The most interesting matter in Fig. 4 lies in the TOTAL A : BICEPS ACTIVITIES BRACHII B : BRACIIIORADIALIS Fig. 6 Comparison of the electrical activities between the biceps brachii (A) and the brachioradialis (B) during the sustained contraction as shown in the previous figure. The EMG of both the muscles increases with time, and the discharges of the biceps brachii are larger than that of the brachioradialis from the beginning to the end of the contraction. fact that electrical activities were larger in order of the vastus lateralis, the rectus f emoris, and the vastus medialis. Therefore, it could not be considered that no remarkable difference in the loweringbetween the knee extensors was brought about from a weak contraction of the rectus femoris as compared with the synergistically operating onejoint muscles. Similar results were obtained from the elbow flexors. The brachioradialis and the biceps brachii acted intensely during supporting a load when the forearm was flexed at semiprone position. As shown in Fig. 5, the lowering in the spectra was indicated to almost the same degree both in the EMG of the brachioradialis and that of the biceps brachii. In this case, the increase in the total activities with the fatigue was also observed in both muscles, and the total activities were greater in the biceps brachii than in the brachioradialis (Fig. 6). Therefore, it may be also difficult to consider that weaker contraction of the biceps brachii produced the similarity of the lowering of (17)
5 86 Masahiko SATO, Atsushi HAYAMI and Haruhiko SATO both muscles as shown in above. These results mean no significant difference in the fatiguability between the brachioradialis and the biceps brachii. On the other hand, a tendency of the differential f atiguability was observed in the cases of the ankle extensors. The continuous changes in the ratios of each frequency component to the total activities were compared between the soleus and the gastrocnemius. As pointed out by Sm- NOMIYA et al. (1965), changes in the frequency spectra were relatively small in the calf muscles as compared with the other limb muscles tested. GASTROCNEMIUS SOLE US Fig. 7 Changes in the ratios of each frequency component to the total activities of the gastrocnemius (left) and the soleus (right) are indicated continuously during an ankle extension endured until the 'exhaustion'. Note that degree of the lowering in the spectra of the gastrocnemius after 2 minutes corresponds almost to that of the soleus at the 'exhaustion', and that the peak frequency component shifts from 150*300 cps to 60*100 cps in the case of the gastrocnemius. The lowering in the spectra is much more marked in the gastrocnemius than in the soleus. A typical result is shown in Fig. 7. It was confirmed that the lowering in the TOTAL ACTIVITIES A: GASTROCNEMIUS B:SOLEUS spectra was much more marked in the gastrocnemius than in the soleus. Continuous changes in the total activities were shown in Fig. 8. It was observed that the activities of the soleus were almost the same to those of the gastrocnemius in the onset of the contraction, and that there was little significant change in the activities of the former whereas those Fig. 8 Comparison of changes in the integrated value of the discharges between the gastrocnemius (A) and the soleus (B) during the same ankle extension that indicated in the previous figure. The increasing tendency with time is much more marked in the gastrocnemius than in the soleus. Note that there is little difference in the total activities of both the muscles at the onset of the extension. of the latter increased in the course of time. Considering almost the same activities in the onset of the contraction of both muscles and the comparison of the lowering with the total activities in the cases of the knee extensors and the elbow flexors, it is not valid to conclude that a (18)
6 Differential Fatiguability between the One and Two-Joint Muscles 87 more intense contraction produced the more remarkable lowering in the EMG of the ~astrccnemius. DISCUSSION In the electromyographic studies, it becomes often problem that the surface electrodes induce the EMG from considerably wide region. In fact, even the activities of the antagonist can be induced (SATO 1959 ; SATO 1963). However, it goes without saying that, in general, activities of muscles below the surface electrodes are most intensely induced (Fig. 1). Furthermore, although the experimental conditions were maintained as constant as possible in each series of the experiments, it is extremely difficult to unify the length of test muscles. In these points, the present investigation may be wanting in the strictness. Therefore, the conclusion from the present results should be restricted in the qualitative judgement. For the comparative evaluation of muscle fatigue by frequency analysis of the EMG of different muscles, it was suggested that simple and fragmentary comparisons of the spectra of different muscles were questionable (SATO 1965). The previous investigations (op. cit.) and the present one were performed by means of continuous comparisons of the degree of the lowering in the spectra. However, the present experiments fail to show a clear-cut association of the degree of the lowering with the difference between the one and two-joint muscles except the cases of the ankle extensors. One of the considerable interpretations for this disagreement may be a suggestion of differences in the analyzing method between the previous and present experiments, since it is inevitable for these sorts of purpose to analyze the EMG around over-all its frequency ranges (KOGI & HAKAMADA 1962; SATO 1965). The biceps brachii is known to act as a abductor and a flexor of the shoulderjoint and a flexor of the elbow-joint, however, it was suggested that the main role of this muscle was a elbow flexor (BASMAJIAN & LATIF 1957). It might be considered that such a sort of disproportional nature as two-joint muscle brought about similar degree of the lowering to that of the one-joint muscle. On the other hand, the rectus femoris was reported to have an important action on flexion of the hip-joint and on extension of the knee-joint (BASMAJIAN 1957). From morphological studies in the human and functional investigations in the dog, MARKEE et al. (1955) stated that two-joint muscles of the thigh could act one end without influencing the other end. BA5MAJIAN objected against this consideration from electromyographical investigation using a row of several electrodes in each muscle tested. It seems to us that the general principle of the muscle function stands by the latter. In fact, HOUTZ et al. (1957) suggested (19)
7 88 Masahiko SATO, Atsushi HAYAMTI and Haruhiko SATO that much intense knee extensions were always associated with hip extensions. In the present experiments, the hip-joint was fixed at flexed position (about 90 ). Comparing magnitude of the electrical activities of the rectus lemons with those of the other knee extensors tested, it may be difficult to conclude that such a flexed hip posture is reckoned among reasons of little difference in the lowering between the rectus femoris and the synergists. Although the gastrocnemius is regarded as a two-joint muscle in the present study, KONDO (1960) did not recognize the action as a knee-flexor in the muscle. For this point further invetigation might be required. It is well-established fact that the gastrocnemius is of phasic nature and the soleus is tonic (T0KIZANF 1955; GRANIT et al. 1956; ECOLLS et al. 1958). Considering that the term "tonic" means resistant characteristic to the fatigue as well as slow contracting characteristic, the present results seem to be valid. Originally, Denny-Brown's statement concerning a more fatiguable nature of the 'doublejoint' muscle was performed in the process of the description that deeper muscles were composed of more slowly contracting fibers. TOKIZANE (1955) described that there was a sort of functional differentiation within the major muscle, such as the tibialis anterior, into kinetic superficial layer and tonic deep layer. From the anatomical fact that the two-joint muscle exists mainly in the superficial layer, it appears that the functional classification as the one- and two-joint muscles derived from the original classification as the deep and superficial muscles. However, the present investigation indicates that the deep one-joint muscle is difficult to fatigue as compared with the synergistically operating superficial two-joint muscle, and that there are little significant differences in the fatiguablity of the superficial one and two-joint muscles. Further investigations should be required to formulate the differential f atiguability between one and two-joint muscles. SUMMARY The present study was designed to confirm the differential f atiguability between the one and two-joint muscles by the frequency analysis of the EMG activities of each pair of elbow flexors (M. biceps brachii and M. brachioradialis), knee extensors (M. rectus femoris, M. vastus medialis, and M. vastus lateralis), and ankle extensors (M. gastrocnemius and M. soleus). The results are summarized as follows : (1) The lowering in the frequency spectra was indicated to almost the same degree between the biceps brachii and the brachioradialis. (2) Any remarkable difference could not be detected between the lowering in the frequency spectra of the rectus femoris and those of the synergisticarlly (20)
8 Differential Fatiguability between the One and Two-Joint Muscles 89 operating one-joint muscles. (3) When the above results were obtained, it was confirmed that the total EMG activities of the two-joint muscles tested were never smaller than those of the synergistically operating one-joint muscles. (4) The lowering in the spectra was much more marked in the gastrocnemius than in the soleus, whereas there was little difference in the contraction level between the gastrocnemius and the soleus. (5) It was concluded that the deep one-joint muscle was difficult to fatigue as compared with the synergistically operating superficial two-joint muscle, and that there were little significant differences in the fatiguability of the superficial one- and two-joint musles. REFERENCES BASMAJIAN, J. V., 1957 : Electromyography of two-joint muscles. Anat. Rec., 129, BASMAJIAN, J. V. & A. LATIF, 1957: Integrated actions and functions of the chief flexors of the elbow. a detailed electromyographic analysis. J. Bone Joint Surg., 39-A, CREED, R. S. D., DENNY-BROWN, J. C. ECCLES, E. G. T. LIDDELL & C. S. SHERRINGTON, 1932: Reflex activity of the spinal cord. The Clarendon Press, 184 pp. DENNY-BROWN, D., 1929 a : On the nature of postural reflexes. Proc. roy. Soc., 104 B, DENNY-BROWN, D., 1929 b : The histological features of striped muscle in relation to its functional activity. Proc. roy. Soc., 104 B, ECCLES, J. C., R. M. ECCLES & A. LUNDBERG, 1958: The action potentials of the alpha motoneurones supplying fast and slow muscles. J. Physiol., 137, EDWARDS, R. G. & 0. C. J. L1PP OLD, 1956 : The relation between force and integrated electrical activity in fatigued muscle. J. Physiol., 132, GRANT, R., H. D. HENATSCH & G. STEG, 1956: Tonic and phasic ventral horn cells differentiated by post-tetanic potentiation in cat extensors. Acta physiol. stand., 37, HoUTZ, S. J., M. J. LEBOW & F. R. BEYER, 1957: Effect of posture on strength of the knee flexor and extensor muscles. J. Appl. Physiol., 11, KoG1, K. & T. HAKAMADA, 1962: Frequency analysis of the surface electromyogram in muscle fatigue. J. Sci. Labour, 33, (in Japanese with English abstract). KONDO, S., 1960: Anthropological study on human posture and locomotion. J. Fac. Sci. Univ. Tokyo, V-II-2, KONDO, S. & M. SATO, 1960: Functional Differentiation between one- and two-joint muscles. Proc. 13th Anual Meet. Jap. EMG Soc. LIPPOLD 0. C. J., J. W. T. REDFEARN & J. VUCO, 1960: The electromyography of fatigue. Ergonomics, 3, MARKEE, E. J., J. T. LOGUE, M. WILLIAVS, W. B. SIANTON, R. N. WRENN & L. B. WALKER, 1955 : Two-joint muscles of the thigh. J. Bone Joint Surg., 37-A, SANADA J., K. SHINOMIYA & M. SATO, 1965: Frequency analysis of the electromyogram. Proc. 19th Joint Meet. Anthropol. Soc. Nippon & Jap. Soc. Ethnol. (in Japanese; in the press). (21)
9 90 Masahiko SATO, Atsushi HAYAM1 and Haruhiko SATU SATU, M., 1959: Fatigue and trainning effect in the rapidly repeating movement. Proc. 12th Anual Meet. Jap. EMG Soc., SATU, M., 1963: Electromyographical study on the skilled movement. J. Fac. Sci. Univ. Tokyo, V-II-4, SATU, M., 1964: Frequency components of the electromyogram led with the bipolar surface electrodes. J. Anthrop. Soc. Nippon, 72, (in Japanese with English abstract). SATU, M., 1965: Some problems in the quantitative evaluation of muscle fatigue by frequency analysis of the electromyogram. J. Anthrop. Soc. Nippon, 73, SHINOMIYA, K., J. SANADA & M. SATU, 1965: Changes in the electromyogram with muscle fatigue. Proc. 19th Joint Meet. Anthropol. Soc. Nippon & Jap. Soc. Ethnol. (in Japanese; in the press). TOKIZANE, T., 1955: Functional differentiation of human skeletal muscles. Kagaku, 25, (in Japanese). The authors are greatly indebted to Dr. Saburo YAtiIADA of Department of Agricultural Economics of the University of Tokyo for his invaluable suggestions in revising English. * Division of Anthropology and Kinesiology, Japan Women's College of Physical Education, Matsubara , Setagaya-ku, Tokyo. ** Department of Anthropology, Faculty of Science, Tokyo University, Hon go 7-3, Bunkyo-ku, Tokyo.
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