Muscle Tendon Kinetics ROBERT CHASE, M.D., _Palo Alto, California
From the Department of Surgery, Stanford University School of Medicine, Palo Alto, California.
NATOMIC STUDIES of the human hand emphasize the difficulties in estimating the number of intricate, myriad possibilities of complicated function that occur. The advanced cerebral mechanisms of man have made his hand superior to even the most advanced anthropoid apes. The peripheral anatomy is so similar in both, yet the :'ttr;ction never reaches the complexity and intricate coordination as it does in man. How easily the hand is reduced to a primitive structure by interruptions of the complicated central nervous controlling mechanisms. A small vascular lesion, injury, or ablative procedure can result in derangement which, when projected to the hand, causes it to function in disunion and chaos as a pitiful shell containing normal musculotendinous, articular, and architectural elements. In studying the complex mechanisms of integration we must start at both ends and work toward the middle. On the one hand, we must study the gross mechanisms of antagonism and synergism for major muscle groups; on the other, we must start with the single axon and its muscle unit. As one works toward an understanding of the motion modifying influences, he soon realizes that he is dealing with problems of major computer complexity. This fact should not discourage the continued probing of motor functions, however, since the important by-product is likely to be new concepts and improved approaches in muscle tendon transfer, reinnervation, 3elected arthrodesis, neurectomy, mid other attempts at improving function. The only target organ of the central nervous system's great motor complex is musele~ Muscle bulk accounts for 40 to 45 per cent of total body weight, and a study of Vat. 109, March 1965
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this muscular tissue is our only index of the normality or abnormality of the central nervous system's motor complex. My own concept of the kinetics of muscle and tendon kinetics is based on the work of Guillaume Benjamin Amand Duchenne [1], a nineteenth century product of the Medical School of Paris. Although we have known him through the years, he was really brought close to us by Emanuel B. Kaplan [2] through his masterful translation of "Physiology of Motion." Faradic current application was a populax form of therapy for all manner of disease in Duchenne's era. Like the unusual student of today's medical schools, Duchenne saw the investigation application of muscle stimulation. He used it as a foundation upon which he constructed a system of knowledge of muscle and tendon kinetics which is unique in its completeness. Early in his studies Duchenne made the cogent observation that, although simple muscle stimulation is valuable for anatomic study, isolated action of muscles is not physiologic. Studies on faradic stimulation, coupled with observations by this astute clinical observer, led to a mass of accurate, new knowledge in motion physiology. He demonstrated t h e concept of synergistic function of muscle groups; the concept of muscle tone maintaining the extremity in a normal position at rest "as so many springs which act to maintain the posit i o n of the e x t r e m i t y . " Paralytic weakening of one spring sets the stage for creating an unbalanced and abnormal position by pull of the tone in those remaining. How frequently Duchenne in his studies noted'that the resultant motion from stimulation of a single muscle was remarkably dependent upon the position of the bones and joints involved by virtue of influence of other muscles.. For example, in studying the action of the adductor pollicis
Chase muscle and the deep head of the flexor pollicis brevis muscle, he remarks t h a t m o v e m e n t of the first m e t a c a r p a l is directed differently in accordance with the position which the first m e t a c a r p a l occupies at the m o m e n t of contraction. If the first m e t a c a r p a l is in abduction, the a d d u c t o r moves it in a medial direction. If it is in flexion in relation to the carpus, extension is produced. If it is in m a x i m u m opposition, the a d d u c t o r moves it slightly to reach the lateral aspect of the second metacarpal. Obviously, the mechanism of v o l u n t a r y m o v e m e n t s of the t h u m b or a n y o t h e r joint d e m a n d s a c o n s t a n t synergistic action of m a n y muscles. D u c h e n n e states, " I hoped t h a t the electrophysiologic studies which I h a v e undertaken would be sufficient to foresee the differe n t functional disturbances which could result from a t r o p h y or partial paralysis of these muscles. B u t I was wrong because a m o n g the muscles which participate in the s a m e movements, some muscles m a i n t a i n e d more or less actively the normal balance of the t h u m b or participate in the m o v e m e n t s required by different uses of the hand. Only clinical observations, w i t h the aid of electrophysiologic experiment, can clarify completely this imp o r t a n t problem of muscular physiology, and t h a t is w h a t I i n t e n d to establish b y fact." Since the classical studies of D u e h e n n e , m a n has recognized electrical stimulation and a s t u d y of action potentials to be excellent tools for s t u d y i n g function. T o d a y , with refined electronic tectmics and sensitive cathode ray oscilloscopes, these studies are becoming even more meaningful. Close and associates [3] noted t h a t although electronic c o u n t s are taken from small portions of muscle, these counts do represent the p a t t e r n for the whole muscle. Detailed studies of the phasic activities of muscles in the u p p e r e x t r e m i t y are badly needed. T h e fact t h a t phasic a c t i v i t y p a t t e r n s exist a n d are generally u n d e r s t o o d is helpful in t e n d o n transfers. A ~tudy of the v o l u n t a r y action of specific muscles is not enough. T h e timing in relationship to action and reciprocal a c t i v i t y in o t h e r muscles using m u l t i e h a n n e l recording is essential in m a p p i n g o u t proper r e a d j u s t m e n t s for pathologic states. S t u d e n t s of kinetics h a v e r e p e a t e d l y emphasized t h a t single muscles never function as such. T h e influence which a muscle has on a joint depends upon m a n y factors. I m p o r t a n t in assessing a single muscle's influences are the joint axes,
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synergistic or antagonistic modifying muscles, the degree of contraction from central influences, a n d the stretch passively applied by other muscles and gravity. I n the hand, e l e c t r o m y o g r a p h i c studies of kinesiology were pioneered a n d have been refined during the last decade by Lake, Eyler a n d M a r k e e [4], Backhouse and C a t t o n [5], a n d others. Charles Long [6-8] has combined m u l t i c h a n n e l e l e c t r o m y o g r a p h y and m o t i o n pictures to s t u d y interacting muscles producing h a n d motion and posture. T h e s t u d y of single frames from motion pictures allows measurem e n t of joint ar~gles with d e v e l o p m e n t of joint displacement d a t a which can be m a t h e m a t i c a l l y reduced to d a t a for c o m p u t e r analysis. D a t a are plotted on joint m o t i o n curves and combined w i t h electromyograms to show muscle action w i t h resultant function. L o n g has shown by these techniques t h a t the dorsal interosseus muscles are primarily extensors of the interphalangeal joints, playing little role in flexion of the m e t a c a r p o p h a l a n g e a l joints. This is especially true when the metacarpophalangeal joint is flexing. T h e extrinsic long extensor is m o r e responsible for extension of the interphalangeal joints during extension of the m e t a e a r p o p h a l a n g e a l joints. While these findings give good objective evidence of the active participation of muscles in specific functions, t h e y alone tell n o t h i n g of the passive role muscles p l a y in various joint activities. T h e i m p o r t a n c e of sensory receptors in regulating musculotendinous function has been n o t e d b y m a n y observers over the years. A comprehensive review of K a p l a n ' s extensive studies on gross nerve supply is found in his excellent book on h a n d a n a t o m y . I n n e r v a t i o n of the deep structures of the h a n d is described in detail b y Stilwell [9] at Stanford. T h e y demo n s t r a t e d proprioceptive afferent nerves arising from a variety, of these h a n d structures. Such stretch-sensitive endings are u n d o u b t e d l y concerned w i t h muscular reflexes a n d knowledge of orientation and motion d u r i n g movements. I quote from Stilwell: "Several investigators h a v e sho-crn t h a t central nervous connections are m a d e and t h a t qualitative a n d q u a n t i t a t i v e alterations in motor p a t t e r n s can be evolved b y propreoceptive reinforcement." M a n ' s ability to separate his own a c t i v i t y first b y muscle groups, t h e n single muscles, and finally specific motor units within muscle has been d e m o n s t r a t e d . F e e d b a c k from senses is American Journal of Surgery
Muscle Tendon Kinetics built by Duchenne, Tubiana [13] and Stack and the studies of freshly dissected fingers with artificial muscle pull (Chase [14,15] and White, Tubiana, Markee, Eyler, Kaplan, etc.) are useful in understanding the contribution of muscles to integrated digital function. These are not precise, but, for all muscles save one, the active contraction can be substituted for. T h a t muscle, of course, is the lumbricale. In models the lumbricale does not contract, thus acting as another elastic retinacular l i g a m e n t - b u t it does act, even in this capacity, to aid flexion of the metacarpophalangeal joint: This it can do with no contraction at all. A study of muscle function with models and dissections, therefore, is incomplete. By the same token, electromyographic studies provide an incomplete assessment of the lumbricales' contribution to metacarpophalangeal joint flexion. To conclude t h a t the lumbricale does not contribute to metacarpophalangeal joint flexion during interphalangeal joint flexion by electromyographic evidence only is as inadequate as our inability to duplicate its true function in metacarpophalangeal joint flexion by dissections and in models. Models and dissections show the lumbricales' passive effect on joint position, and electremyography documents its active effect during contraction in integrated function. Eyler an d Markee alluded to the importance of passive changes in the length of the lumbricales with profundus contraction. T h e y also pointed out t h a t with flexion of the interphalangeal joints under profundus influence, the lumbricale is stretched to the point where it is physiologically in position to contribute most to flexion of the metacarpophalangeal joint. T h e y further suggested its passive function by stretch tension. Such isometric function of the lumbricale would be siinilar to function of the retinaculum described by Stack, Tubiana and L~ndsmeer [16-20], effeeting the distal interphalangeal joint when the proximal interphalangeal joint is extended. I would like to focus on th e lumbricales as an example of a single muscle of great complexity and varying function. Actually, t h e action of the lumbricales was described by Galen in the second c e n t u r y A.D. Baekhouse and Catton, after making a study of the lumbrieales in 1954, believed t h a t they were important in interphalangeal extension. Sunderland [21], in 1945, pointed o u t the importance
responsible in large measure for man's dexterity. T h e accomplishment of deftness of fine movement is a m a t t e r of training. One's own assessment of achievement which is requisite to training comes through sensory feedback. At the highest level of breakdown, it is possible for man to control action in single muscle units. A monitor, played through the visual or auditory receptors; can be used in the training for this accomplishment. Basmajian [10,11], of Queens University, has demonstrated man's ability to single out motor units and control their isolated contraction. He used oscilloscopic and sound monitors to train the patient in control of tiny muscle units down to t h a t controlled by a single anterior horn cell. T h e finesse of conscious motor control is astounding. In the gross, practical sense, man's vision, kinesthetic and special skin sensation are the monitors which allow training for special skilled movements. The anesthetic "blind h a n d " is clumsy by comparison with the normal hand. It is more dependent upon visual control with a resultant loss in dexterity. The addition of blindness to extremity anesthesia essentially destroys fine function. With normal sensory feedback man develops trained dexterity by a lifetime of experimentation and observation. This, again, emphasizes the fact t h a t the mere presence of normal a na t om y means nothing without the integrated and complicated central nervous system pathways. Integration resulting from long experience and training results in patterns of muscular activity t h a t emerge as specific desired motion. The programming o f that motion in the central nervous system results in graded contraction or relaxation of antagonists, protagonists, and modifier muscles. This obviously is done without conscious delineation of which muscles.are contracted or relaxed. H. G r a h a m Stack [12] has studied the interplay of various structures by constructing an ingenious model of the finger. He has been able to demonstrate the angles of insertion and the direction of pull of various tendons, thus showing the influence of various motors on the metacarpophalangeal and interphalangeal joints. He has also shown the importance of retinacular ligaments on digital function by duplicating them on his models. William L. W hi t e and I also have studied the dissected finger with each tendon attached to strings and pulleys. I believe t h a t the models Vol. 109, March 1965
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Chase of the lumbricales and interossei in extension of the interphalangeal joints. Sunderland emphasized the function of these intrinsic muscles in preventing hyperextension of the proximal phalanx by the extensor digitorum. This allows the long extensor to exert a more efficient pull on the dorsal expansion in extending the interphalangeal joints. Backhouse and Carton, as well as Long, noted on their electromyographic studies t h a t the lumbricales are silent during total flexion of the entire finger but are very active whenever the proximal or distal interphalangeal joints are extended actively. T h e y are also active when these joints are held extended and the metacarpophalangeal joint is flexed actively. The lumbricales can be kept very quiet during metacarpophalangeal movements in any direction by keeping the interphalangeal joints fully flexed. Kaplan has observed in hum a n beings the activity of lumbricales during surgery under local anesthesia. He noted the degree of contraction with the patient moving his fingers through a range of motion and also by faradic stimulation and observation of the resultant digital posture. He has observed, as m a n y others have, t h a t a paralysis of the radial two lumbricales causes little disturbance in the flexion of the metacarpophalangeal joints and extension of the interphalangeal joints of the index and middle fingers. The profundus tendon has its primary action at the distal interphalangeal joint which i t flexes. I t secondarily flexes all other joints between its origin and insertion. If one fuses the d i s t a l joint, the profundus flexes primarily the proximal interphalangeal joint (now acts similar to a sublimis tendon in its function). If both the distal and proximal interphalangeal joints are fused, the profundus flexes primarily the metaearpophalangeal joint (like the intrinsies). Now, if instead of fusion, the joints are fixed by the prime a n t a g o n i s t - - t h e lumbricales--the profundus acts as a metacarpophalangeal joint flexor when the interphalangeal joints are extended. Consider the lumbricale as the controllable regulator of the length of a loop around the interphalangeal joints. The profundus tendon forms the palmar aspect of the loop and the extensor mechanism the d o r s ~ aspect. The lumbricale closes the loop by bridging across from the extensor to the flexor mechanism at
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the proximal phalanx. A pull on tile relaxed profundus stretches the lumbricale by separating its origin and insertion. The origin is moved proximal by the contracting profundus. The insertion is moved distal as the distal phalanges flex under the profundus influence. As long as the lumbricale does not offer resistance, the distal, then middle phalanges flex with little influence oi1 the metacarpophalangeal joints. If the lumbricale does not stretch b u t remains static, the profundus pull is transmitted to it and the metacarpophalangeal joint flexes. If the lumbricale actually contracts, the loop relationship changes and the interphalangeaI joints extend making the profnndus primarily a flexor of the metacarpophalangeal joint through the lumbricale. Leont'ev and Zaporozhets [22] in their interesting monograph, "Rehabilitation of Hand Function," explore the last dimension in coordinated function, the central factors of psychologic origin. For example, they point out the widely known phenomenon that there are patients with restricted movement of their fingers who cannot, upon request, approximate the tips of the index finger and th u m b closer than 10 to 15 ram. Immediately afterward, however, and without difficulty, they are able to lift a pencil whose diameter is not more than half this length. We must now add to the anatomic and physiologic factors in motor function the emotional attitude of the patient. "The magnitude of the range of movement is determined not by the limits of motor activity of the affected organ as a whole but by the limits of its function under the given conditions and measurements." T h e reduction in motor response to testing in the first situation is probably due to a form of "protective" inhibition developing in the cortex from stimuli resulting from peripheral trauma. These inhibiting stimuli are removed during transfer to the subsequent task which introduces fresh overriding stimulation. This example suggests the assumption t h a t trauma has disrupted or altered the proprioceptive system from the original pattern of afferent supply. This interferes with the established, automatic coordinated motor patterns usually developed in lower centers by central control. Coordination of movement is therefore not developed afresh every time; it is a product of individually accumulated motor experience (propriomotor). T h e motor experience can be cancelled by American Journal of Surgery
Muscle T e n d o n Kinetics trauma through a confused sensory feedback picture and by immobilization of the limb. Any injury to the bones, joints and muscles requiring anatomic reorganization of the limb produces disturbances of movement coordination regardless of preservation of peripheral nerves. I t is particularly interesting that these disturbances become smoothed out by movements which have a spatial target and are carried out under visual control. Autonmticity is developed centrally by altering the synthesis of combined visual and proprioceptive afferent playback with ontogenetically accumulated motor experience. Charpentier's illusion is a good example of such synthesis. If a normal subject is instructed to compare two weights which are objectively equal in weight but of unequal dimension, a sharp iliusion develops. The weight which is smaller in size appears heavier than the larger weight. The illusion disappears with the eyes closed. With stereognostic disruption (Krukenberg) the opposite effect takes place, the large weight is called the heaviest. In the first stages of recovery after limb trauma, the patient listens very attentively to sensations coming from the injured limb. The purpose is protection of the injured organ from harmful influences. The motor reaction is a dynamic immobilization. This is fine in the early phase of recovery; but should the protective mechanisms become fixed, this dynamic immobiliza.tion like any other prolonged immobilization will become a hindrance and delay the recovery. There is one point I should like to emphasize in this discussion of the technics for study of muscle tendon kinetics. It is that no single technic of evaluation and study is adequate for gaining a proper assessment of the activity resulting in peripheral controlled movement. The combination of sophisticated electronic technics, anatomic studies, functional physiologic analyses and studies of specific paralyses are all contributory in understanding integrated muscle tendon kinetics. In effect, it becomes obvious from study that: (1) Any muscle which, by its action tends to increase the distance between the origin and insertion of anotb2r muscle, makes t h a t muscle more effective on the joints i t influences. (profundus effect on the lumbricale). ( 2 ) Antagonistic muscles potentiate one another in their effect on all joints other than the one around which the antagonism exists; (wrist extensor Vol. 109. March 1965
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digital flexor). (3) If a muscle influence extends across more than one joint, it selectively influences one through stabilization of all others by the muscle antagonists (the abductor pollicis brevis extends the distal phalanx, stabilized by the abductor pollicis. (4) A muscle's action on one of several joints it crosses may actually be the reverse of its prime function on that joint by increasing the effect of its own antagonist by secondarily increasing the tension of the antagonist. (Recurvatum at the proximal interphalangeal joint is increased by a pull o~ the profundus tendon as it acts through the extensor mechanism.) Finally, ]Duchenne's humility in dealing with a biologic subject which cannot be reduced to precise analysis is a lesson for any of us dealing with this complex subject. He wrote: " I would not dare to state that my interpretation was always correct, although I have never written a single paper without profound conviction of its truthfulness. I hope my readers will consider the difficulties connected with this work." REFERENCES 1. DUCHE~NB, G. B. Physiologie des Mouvements. (Physiology of Motion). Translated b y Emanucl B. Kaplan. Philadelphia a n d London° 1959. W. B. Saunders. 2. KAPLAN, E. B. Function and Surgical A n a t o m y of the H a n d . Philadelphia, 1953. J. B. Lippincott. 3. CLOSB, J. R. M o t o r Function in the Lower Ext r e m i t y ; Analysis b y Electronic I n s t r u m e n t a t i o n . American Lecture Series, Publication #551, American Lectures in Orthopedic Surgery, 156 pp. Springfield, Ill., 1964. Charles C Thomas. 4. ~rLBR, D. L. and MARKB~, J. E. T h e a n a t o m y of the intrinsic musculature of the fingers..7. Bone ¢~" Joint Surg., 36A: 1, 1954. 5. BAck'~otrs~, K. M. and CATTON, W. T. An experim e n t a l s t u d y of tlle functions of the lumbrical muscles in the h u m a n hand. 3". Anat., 88: 133, 1954. 6. LONG, C., BROWN, M. E . a n d WEISS, G. An elect r o m y o g r a p h l c s t u d y of the extrinsic and intrinsic kinesiology of the h a n d : preliminary report. Arch. _Phys. 21led., 41: 175, 1~60. 7. LONO, C., BRowN, M. E. a n d W m s s , G. Electrom y o g r a p h i c kinesiology of the hand. H. T h i r d dorsal interosseus and extensor digitorum of the long finger: Arch. Phys..~[ed., 42: 559, 1961. 8. LONO, C., BROWN, M. E. and WBISS, G. Electromyographic kinesiology of the hand. xv~, Lumbricales and flexor digltorum. Profundus to
the long finger. Arch. Phys. M'ed., 43: 450, 1962.
9. STILW~LL, D. L., JR. The innervation of deep structures of the hand. A m . J. Anat., 101: 75, 1957. 10. B^SM^JIAN, J. V. Muscles A l i v e - - T h e i r Functions
Chase
11. 12. 13. 14. 15.
16.
Revealed by Electromyogr~aphy. Baltimore, 1962. Williams and Wilkius (20. B,~sM^JtaN, J. V. Control and training of individual motor units. Science, 141: 440, 1963. STACK, H, G. A study of muscle function in the fingers. Ann. Roy. Coll. Surgeons England, 33: 307, 1963. TUBI^NA, R. and VALBNTIN, P. L'extension des doigts. Rev. chir. orthop., 49: 543, 1963. CI~As~, R. A. M a n a g e m e n t of nerve injuries in the upper extremity. S. Clin. North Auwrica, 40: 287, 1960. CuAs~, R. A. and LXTTLBR,J. W. A concept of hand anatomy. I n : A Textbook of Plastic Surgery. Edited by J. M. Converse and J. W. Littler. Baltimore, 1964. Williams and Wilkins Co. LASDSMEER, J. M. F. A report on the co-ordination of the interphalangeal joints of the human finger and its disturbances. Acta morphol. Neerl. Stand., 2: 59, 1958.
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17. LANDSMI~I~R, J. ~[. F. Studies in tile a n a t o m y of articulation, xI. Patterns of movement of bimuscular, bi-articular systems. Acla morphoL Need. Stand., 3: 304, 1960. 18. LANDSMEER, J. 1~. F. Studies in thc a n a t o m y of articulation. I. Tile equilibrium of the "intercalated" bone. Acta morphol. Neerl. Scand., 3: 287, 303, 1960. 19. LANDSME~R, J. ~I. F. Power grip and precision handling. Ann. Rheun~at. Dis., 21: 164, 1962. 20. L^NVSM~ER, J. M. F. The coordination of fingerjoint motions..I. Bone ~" Joint Surg., 45A: 1654, 1963. 21. SUNVERLAND, S. The actions of the extensor digitorum communis, interosseous and lmnbrical muscles. Am. J. Anat., 77: 189, 1945. 22. LBONT'~V, A. N. and ZAPOROZHETS, A. V. Rehabilitation of Hand Function. (Translated from the Russian by Basil Haigh.) New York, 1960. Pergamon Press.
A merican Journal of Surgery