The stability of synergy in agonists during the execution of a simple voluntary movement

Electroencephalography and Clinical Neurophysiology, 1977, 42:543--551

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© Elsevier/North-Holland Scientific Publishers, Ltd.

THE STABILITY OF S Y N E R G Y IN AGONISTS DURING THE EXECUTION OF A SIMPLE V O L U N T A R Y MOVEMENT S. BOUISSET, F. LESTIENNE and B. MATON Laboratoire de Physiologie du Mouvernent, Universit~ de Paris Sud, 91405 Orsay, et Laboratoire de Physiologic du Travail, CHU Piti~ Salp~tri~re, 91 Boulevard de l'Hbpital, 75634 Paris Cedex 13 (France)

(Accepted for publication: July 17, 1976)

Muscular synergy is expressed as the existence of patterns of activity (Gelfand et al. 1971) between the different muscles participating in the given m o t o r task: If we a t t e m p t to outline the classification proposed by Wright (1952), the following participating muscles can be distinguished: (a) agonists, whose activity initiates the movement; (b) antagonists, which counteract the movement; (c) stabilizers, which stabilize the position of the limb articulations which are not directly related to the movement; and (d) postural muscles, which regulate and re-establish the general balance of the body. When peripheral conditions vary, movement remains possible due to the neuromuscular system's ability to adapt to such changes. This property appears at the level of muscular synergy as what could be called 'the plasticity of muscular synergy' (Livingston et al. 1951). When we consider the case of very simple voluntary movements, such as elbow flexion, from both theperceptual and biomechanical points of view, this plasticity becomes apparent in the agonist--antagonist synergy (Wachholder 1928; Lestienne and Bouisset 1971). We shall study herein the characteristics of muscle synergy existing between the principal agonists, i.e., those muscles which initiate movement. This investigation was performed on the three main elbow flexors (biceps brachii, brachialis and brachio-radialis) which, according to classical data (Fick 1911), provide approximately 85% of the total torque.

It is a quantitative study of the activity of these 3 muscles recorded simultaneously under closely controlled experimental conditions at varying velocities and against different inertias, using a combination of surface and intramuscular detection by wire electrodes (Bouisset and Maton 1972).

Methods The EMGs of biceps brachii (B), brachialis (BA) and brachio-radialis (BR) muscles were recorded simultaneously. The intramuscular B, BA and BR activities were recorded by means of bipolar platinum wire electrodes of weak selectivity (Maton et al. 1969) (diameter 100 p, sharpened to a diameter of about 30 p at the tip and insulated with araldite). The recording area of each wire was lateral and provided an active surface of 3--8.104 p2. Surface EMG activity of B and BR were recorded from bipolar derivations. Silver disc electrodes, 50 mm 2, were stuck to the skin with adhesive tape. The inter-electrode impedance was usually less than 30 k~2 and inter-electrode distance varied from 2 to 7.5 cm, depending on where the wire electrodes were placed. After amplification (linear bandpass between 20 c/sec and 10 kc/sec) the different EMGs were recorded on magnetic tape which limited the bandpass to 2500 c/sec. They were then integrated using an analogue--digi-

544 tal converter (Feuer 1967). Integration of the area delimited by the EMG signal, regardless of polarity, was proportional to the number o f impulses delivered by the integrator. The data recorded on magnetic tape were then transcribed on paper using an ink-jet recorder whose bandpass was limited to 700 c/sec (3 dB). The m o v e m e n t studied was the flexion of the right forearm. Subjects were seated, with their arm and forearm positioned on the same horizontal plane. The forearm was semi-prone and fastened in a splint which was part of a movable mechanical system which rotated in a horizontal plane about a vertical axis. The position o f the elbow coincided approximatly with this rotational axis. The mobile part o f this mechanical system was equipped with an accelerometer (Schlumberger, ACB, 32220) and a linear p o t e n t i o m e t e r (M.C.B. veritable Alter) which allowed recording of the tangential acceleration and angular displacement respectively. The inertia of the movable system could be adjusted by the addition of weights from 1 to 10 kg at a distance of 25.5 cm from the axis, corresponding to inertias from 0.070 kgm 2 to 0.640 kgm 2. Five normal subjects aged 30--66 years and accustomed to this t ype of performance were each tested three times, making a total of 15 tests. For each test, 3 inertia conditions were observed and for each inertia condition, each subject p er f o rm e d approximately 15 movements at slower and faster velocities. These varied according to the instructions given by the experimenter. The amplitude of flexion was voluntarily limited by guide marks located 30 ° on either side of the reference position, defined by the orthogonal position of the arm and forearm. Between two movements, sufficient rest -- about 2 min -- was given to the subject to decrease the risks of fatigue (Scherrer and Monod 1960). At the beginning and the end of each test, static work trials were performed. With the forearm in a semi-prone position and forming an angle of 90 ° with the arm, the subjects were required to hold 3 weights, which did

S. BOUISSET ET AL. not exceed 8 kg (at a distance of 25.5 cm from the elbow axis). Possible modifications of activity, related either to fatigue or to displacement of intramuscular electrodes (Jonsson and Reichmann 1969) could thus be detected. A series of c o m p l e m e n t a r y trials of static work was carried out either at the beginning or the end of each test with the forearm in a prone or supine position. This was done to ensure that the electrodes were properly inserted in the branchialis, as will be explained in the Discussion.

Results The experimental results are of two kinds: (A) a chronology of different flexor activities; and (B) a comparison of the activity levels of the flexors. A. The sequences of contractions of the different muscles were studied on the basis of paper records, with an absolute error of about 10 msec, the onset and the end of EMG activity being defined in relation to the noise level. As can be seen in Fig. 1, the activation of

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S T A B I L I T Y O F S Y N E R G Y IN A G O N I S T S

545

the principal elbow flexors as well as the cessation of their activity occur almost simultaneously. This holds true regardless of the intensity of muscular contraction. However, if the time intervals between the activities of the different muscles are quantified, slight differences are revealed between their moments of activation and their moments of cessation of activity. In the case of the onset of the activities BA was activated an average of 11 msec after B (SD, 18 msec) in 376 movements, while in 559 movements BR activity as determined by its surface EMG began 7 msec after that of B (SD, 17 msec). At the interruption of activity, in 244 movements studied, BA ceased being active 5 msec before B (SD, 17 msec), while in 517 movements, BR ceased 4 msec before B (SD, 16 msec). The significance of the time intervals be-

tween the onsets as well as between the cessations of BR and BA activities was tested by the Student t method. The intervals between onsets thus appeared very significant at P = 0.01 (t = 3.44), while those between cessations were not found to be significant (t = 1.05). This test reveals that while the muscles are activated in the sequence, B, BR, BA the inverse chronology cannot be assumed with regard to the cessations of their activity, which tended to be simultaneous. Furthermore, it is important to note that these intervals were independent of the velocity and inertia of the movement (Fig. 2 and 3). Various tests were carried out to determine to what extent the intramuscular EMGs really take into account the phases of muscular activity. These tests measured: (a) the interval between the beginning of the intramuscular EMG in BR and that of the surface EMG in B.

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546

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In 269 movements, the Bit activity occurred 7 msec after the beginning of the B activity (SD, 18 msec), i.e., the same as for the surface EMG; (b) the interval between the beginning of the intramuscular EMG of B and the beginning of its surface EMG. In 428 movements, the intramuscular EMG began 2 msec after the surface EMG (SD, 4 msec) which obviously does not constitute a significant difference. B. The excitation level of each of the muscles considered was evaluated by integrating the EMG between the onset of activity and the end of the acceleration phase. The integrated EMG activities (Q), expressed in numbers of impulses, were related to the corresponding values of the work (W). The latter was calculated from the variation of kinetic energy 1/2 IV 2 where I represents the inertia opposed to the movement and V the peak

velocity reached in the course of the movement. For' each test, linear relations were found between the work and the integrated surface EMG of B and Bit, and the integrated intramuscular EMG of BA (Fig. 4). It should be noted that in each case these relations were: (a) independent of the inertia opposed to the movement; (b) little scattered, as proved by the very significant values {0.84 ~< r ~< 0.98) of the correlation coefficients; and (c) perfectly reproducible from one subject and one test to another. However, the linearity of these relations cannot be considered demonstrated for work values above 15 J. In fact, above this level, the integrated EMG tends, in certain cases, to increase less rapidly than the work. It is likely, that this non-linearity is due to technical causes, such as a possible clipping of the signals due to amplifier saturation or a

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too-high selectivity of the electrodes. In the latter case, it seems possible (Bouisset and Maton 1972) that, for the highest values of work, all m o t o r units which can be recorded by the wires are firing. Furthermore, some very significant linear correlations (Fig. 5) have been revealed; on the one hand, between the integrated surface EMG of B and integrated intramuscular EMG of BA (0.77 ~< r ~< 0.95), and on the other, between the integrated surface EMG of B and that of BR {0.82 ~< r ~< 0.97). These correlations can be seen for values of work up to 1 5 J .

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S. BOUISSET ET AL.

Discussion

Before discussing the results, it is necessary to test their validity. Essentially two points should be considered. First, the possibility that the wire electrodes were inserted in B (instead of BA) must be excluded. The risk of this happening is real, given the proximity of the two muscles. The isometric contractions performed with the forearm successively in the prone and supine positions permit an electrophysiological differentiation of the two muscles. It seems well established (Sullivan et al. 1950; Basmajian 1962; Pauly et al. 1967; Simons and Zuniga 1970; Goubel and Lestienne 1974; Maton 1974) that the movement from a prone to a supine position provokes a significant increase of B activity, while that of BA remains relatively stable. Fig. 6 gives an example of the experimental confirmation that was obtained. It must be observed, however, that while in all cases the B activity was greater when the forearm was supine than when it was prone, stable BA activity was only found in 50% of the cases. In the other cases, as shown in the same Figure, the activity of this muscle varied inversely to that of B, with the magnitude of this variation depending on the position of the forearm. It must also be noted that the results are significant only to the extent that the intramuscular activities recorded are really representative of the activity of the muscle as a whole. Now it seems that the intramuscular EMGs recorded with wire electrodes of

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weak selectivity are indeed representative of this activity. This assertion is supported: (i) by the linear relations between the integrated values of the surface EMG and the intramuscular EMG of the same muscle (B), which have been demonstrated in the case of both isometric (Maton et al. 1969) and anisometric (Bouisset and Maton 1972) contractions; (ii) by the comparison made here between the periods of muscular activity which were determined by using the intramuscular EMG and the surface EMG. We shall now discuss both the chronology of the activities of each of the muscles in question and their excitation levels. The existence of a well-determined chronology of the activities of the main flexors is shown. Generally speaking, the phases of activity of the different muscles are practically simultaneous, whatever the velocity and inertia of the movement. There is, however, a slight tendency for them to appear in the following order: B, BR, BA. These results complete the study of the synergy between B and BA made by Wachholder and Altenburger (1926) and also the data concerning the temporal relations between B and BR (Goubel and Lestienne 1974). On the other hand, such results differ from the data presented by Basmajian and Latif (1957) who described a non-systematic order in the activation of the different flexors. This difference might be attributed to the fact that in the present study, movements could be executed in only one way given the experimental conditions while in those of Basmajian and Latif, the position of the upper limb in particular and that of the subject in general was not strictly determined. It may also be that, since the time intervals between the onsets and between the cessations of flexor activities are small, only a statistical study of the data would reveal a definite chronology. For the excitation levels, the following three points will be considered: 1. The results confirm those previously reported for B and BR, i.e., linear and highly consistent relations between the work and

STABILITY OF SYNERGY IN AGONISTS the integrated EMG of B (Bouisset and Goubel 1973) and BR (Goubel and Lestienne 1974). The validity of these data, however, is extended here since the angular amplitude of the movements was increased (+30 ° in relation to elbow flexion at 90 ° , instead of-+15 ° ) and the tested values of inertia were higher. 2. On the other hand, the existence of a linear relation between the integrated EMG of BA and the external work, is a new finding. This relation presents the same properties of consistency and independence of inertia that are revealed by the two other flexors considered. To a certain extent this finding may seem to be implied by the data of Wachholder and Altenburger (1926) who were the only ones, to our knowledge, to make reference to this same type of movement. Furthermore, the interest of these findings is strengthened by the fact that BA is considered to be the main elbow flexor for both anatomical (Braune and Fischer 1889) and electrophysiological (Duchenne de Boulogne 1867; Mac Gregor 1950; Basmajian and Latif 1957) reasons. 3. The demonstration of linear relations between work and the integrated EMG of the three main flexors implies a proportionality between the integrated EMG of the biceps and t h a t of each of the other flexors. Assuming that the work performed by a muscle is a m o n o t o n o u s function of its integrated EMG and taking into account that the extemal work is equal to the sum of the individual work of each muscle, these results lead to the conclusion that the work performed by each muscle is proportional to its integrated EMG and a constant fraction of the total external work. These results confirm the notion of Flexor Equivalent (Bouisset 1973) since they show, first, that there is a constant relation between the excitation levels of the different muscles, and second, that the activity of the biceps just precedes those of the other flexors and stops at the same time as they do. This work demonstrates, moreover, the stability of the synergy between agonist mus-

549 cles in elbow flexion. In fact, when peripheral conditions vary, the order in which the muscles are activated remains the same and the relations between their excitation levels remain constant. In this way, the synergy between agonist muscles must be distinguished from that between agonists and antagonists, the latter being characterized by a chronology which varies according to velocity (Wachholder and Altenburger 1926; Lestienne et Bouisset 1973) and inertia (Wagner 1925; Lestienne and Bouisset 1971). It is also distinguishable from the synergy of stabilizer muscles which is marked by a progressive spread of activity to muscles farther and farther away as the intensity of the contraction increases (Waterland and Hellebrandt 1964; Belen'kii et al. 1967). In particulm', it is interesting to observe that the intensity of contraction is regulated by a gradual change in the excitation level of each muscle and not through the order in which the different muscles are recruited.

Summary The characteristics of muscular synergy between the main elbow flexors (biceps brachii, brachialis, brachioradialis) were considered. The activities of these different muscles were recorded simultaneously with surface and wire electrodes. A quantitative analysis of the activity of each of these muscles and of their excitation levels was carried out during movements performed at various velocities and against different inertias. It was shown that: (1) the onset as well as the cessation of activity in the different muscles occur practically simultaneously and independently of the velocity and inertia of the movement; (2) the well-known linear relation between the integrated EMG of biceps brachii and the work can be extended to the other main flexors. This implies that the relation between the activities of the main flexors remains constant whatever the velocity and inertia may be. These results confirm the

550

notion of 'Flexor Equivalent'. They also demonstrate a stability of the synergy between agonist muscles which must be distinguished particularly from the synergy between agonists and antagonists.

R6sum6 Stabilit~ d'une synergie entre agonistes au cours de l'exdcution d'un m o u v e m e n t volontaire simple

Le present travail concerne les caract~res de la synergie musculaire existant entre les principaux fl6chisseurs du coude (biceps brachial, brachial ant~rieur, brachioradial). L'activit~ des diff~rents muscles est simultan~ment d~tect~e ~ l'aide d'~lectrodes de surface et d'~lectrodes-fils. Une analyse quantifi~e de la chronologie des activit~s de chacun de ces muscles, ainsi que de leur niveau d'excitation a 6t~ r~alis~e au cours de mouvements effectu~s ~ des vitesses vari~es et contre diff~rentes inerties. I1 est montr~ que: (1) la mise en jeu de m~me que la cessation d'activit6 des diff6rents muscles s'effectue de fa~on pratiquement simultan~e, ind~pendemment de la vitesse et de l'inertie du mouvement; (2) la relation lin~aire entre I'EMG global du biceps brachia! et le travail pourrait ~tre g~n~ralis~e ~ chacun des principaux fl~chisseurs, ce qui implique que les activit~s des principaux fl~chisseurs restent dans un rapport constant quelles que soient la vitesse et l'inertie. Ces r~sultats confirment la notion de 'Fl~chisseur Equivalent'. Ils montrent 6galement la stabilit~ de la synergie entre muscles agonistes, qui distingue notamment celle-ci de la synergie entre agonistes et antagonistes.

References Basmajian, J.V. Muscles alive. Their functions revealed by electromyography. Wilkins Co., Baltimore, Md., 1962, 1 vol., 267 p.

S. BOUISSET ET AL. Basmajian, J.V. and Latif, A. Integrated actions and functions of the chief flexors of the elbow (A detailed electromyographic analysis). J. Bone Jt. Surg., 1957, 39-A (5): 1106--1118. Belen'kii, Y.Y., Gurfinkei, V. and Pal'tsev, Ye.I. Elements of control of voluntary movements. Biofizika, 1967, 12 (1): 135--141. Bouisset, S. EMG and muscle force in normal motor activities. In J.E. Desmedt (Ed.), 'New developments in electromyography and clinical neurophysiology'. Vol. I. Karger, Basel, 1973: 547--583. Bouisset, S. and Goubel, F. Integrated electromyographical activity and muscle work. J. appl. Physiol., 1973, 35 (5): 696--702. Bouisset, S. et Maton, B. The quantitative relation between surface and intramuscular electromyographic activities for voluntary movement. Amer. J. phys. Med., 1972, 51: 285--295. Braune, W. und Fischer, O. Die Rotationsmomente der Beugemuskeln am Ellbogengelenk des Menschen. Abhandl. d.K.S. Ges. d. Wiss., 1889, 26: 245--310. Duchenne de Boulogne, G.B. Physiologie des mouvements. Bailliere et fils, 1867, 1 vol., 872 p. Feuer, D. Int~grateur convertisseur (analogiquenum~rique). Application ~ l'~valuation de l'activit6 61ectrique cellulaire. J. Physiol. (Paris), 1967, 59, 319--321. Fick, R. Speziellegelenk und Muskelmechanic. Gustav Fischer, Iena, 1911, 1 vol. Gelfand, I.M., Gurfinkel, I.M. Tsetlin, M.L. and Shik, M.L. (1971): Some problems in the analysis of movements. In Models of the structural functional organization of certain biological systems: M.I.T. Press, Cambridge, Mass., 1971: 329--345. Goubel, F. et Lestienne, F. Influence de la position de prono-supination sur l'activit6 ~lectrique de deux fl~chisseurs de coude au cours du mouvement. J. Physiol. (Paris), 1974a, 69: 155A. Goubel, F. et Lestienne, F. Influence du caract~re plurifonctionnel du muscle sur l'allure de la relation EMG int6gr6---travail m6canique. Electromyography clin. Neurophysiol., 1974b, 14: 537-546. Jonsson, B. and Reichmann, S. Displacement and deformation of wire electrodes in electromyography. Electromyography, 1969, 9 (2): 201--211. Lestienne, F. and Bouisset, S. Quantification of the biceps-triceps synergy in simple voluntary movements. In Visual information processing and control of motor activity. Symposium Acad. Sci. Bulgaria, Sofia, July 1969, 1971. 445--449. Lestienne, F. and Bouisset, S. Role played by the antagonist in the control of voluntary movement. In Gavrilovit~ and Wilson (Eds.), Advances in external control of human extremities. IVth Int. Syrup. on external control of human extremities, Dubrovnik. ETAN, Belgrade, 1973, 1 vol: 1221.

STABILITY OF SYNERGY IN AGONISTS Livingston, R.B., Paillard, J., Tournay, A. et Fessard, A. Plasticit~ d'une synergie musculaire dans l'~x~cution d'un mouvement volontaire chez l'homme. J. Physiol. (Paris), 1951, 43: 605--619. MacGregor, A.L. Synopsis of surgical anatomy. Williams and Wilkins, Baltimore, Md., 1950. Maton, B. Etude quantitative d'une synergie musculaire. Tray. Hum., 1974, 37: 334--336. Maton, B., Bouisset, S. et Metral, S. Comparaison des activit~s ~lectromyographiques globale et ~l~mentaire au cours de la contraction statique volontaire. Electromyography, 1969, 9: 311--323. Pauly, J.E., Rushing, J.L. and Scheving, L.E. An electromyographic study of some muscles crossing the elbow joint. Anat. Rec., 1967, 159: 47--54. Scherrer, J. et Monod, H. Le travail musculaire local et la fatigue chez l'homme. J. Physiol. (Paris), 1960, 52: 419--501. Simons, D.G. and Zuniga, E.N. Effect of wrist rotation on the XY plot of averaged biceps EMG and isometric tension. Amer. J. phys. Med., 1970, 49 (4): 253--256. Sullivan, W.E., Mortensen, O.A., Miles, M. and

551 Greene, L.S. Electromyographic studies of m. biceps brachii during normal voluntary movement at the elbow. Anat. Rec., 1950, 107 : 243--251. Wachholder, K. Willkiirliche Haltung und Bewegung in besondere im Lichte elektrophysiologischen Untersuchungen. Ergebn. Physiol., 1928, 26: 568--775. Wachholder, K. und Altenburger, H. Beitr~ige zur Physiologie der willkiirlichen B e w e g u n g . . V I I I Mitteilung: fiber die Beziehungen verschiedener synergisch arbeitender Muskelteile und Muskeln bei willkiirlichen Bewegungen. Pfli]gers Archly. ges. Physiol., 1926, 212: 666--675. Wagner, R. Uber die Zusammenarbeit der Antagonisten bei der Willkiirbewegung. II Mitteilung: Gelenkfixierung und versteifte Bewegung. Z. Biol., 1925, 83: 120--144. Waterland, J.C. and Hellebrandt, F.A. Involuntary patterning associated with willed movement performed against progressively increasing resistance. Amer. J. phys. Med., 1964, 43: 13--29. Wright, S. Applied physiology 9th ed. Oxford University Press, London, 1952, 1 vol.: 1190 p.