Are muscles mechanically independent?

MOST PHYSIOLOGY TEXTS imply that the mechanism by which force is transmitted from sarcomeres to muscle insertions is simple: when skeletal muscles contract, cross-bridge forces are transmitted along myofibrils, through the sarcolemma and extracellular matrix to tendons and, ultimately, bones. At each level of organization, myofibrils, muscle fibers, and muscles behave as mechanically independent force generators. Muscle fiber tension is the sum of the tensions generated by individual myofibrils, muscle tension is the sum of the tensions generated by individual fibers, and the torque generated at a joint is the sum of torques produced by individual muscles crossing the joint. In the last two decades most of this simple picture has come under suspicion, or been shown to be wrong (3, 9–11). Myofibrils transmit force not only longitudinally, but also to adjacent myofibrils and the sarcolemma. Muscle fibers transmit force not only to tendon, but also to adjacent muscle fibers and in-series fibers. Tendons are arranged partly in series and partly in parallel with muscle fibers. And, perhaps most surprisingly, it has been claimed that muscles transmit force not only through their own tendons, but also to adjacent structures, including other muscles. Transmission of force from muscles to adjacent nonmuscle structures has been called “extramuscular myofascial force transmission.” Transmission of force from muscles to adjacent muscles has been called “intermuscular myofascial force transmission.” The collective term for extramuscular and intermuscular myofascial force transmission is “epimuscular myofascial force transmission” (5). To avoid presuming a mechanism, we refer to transmission of force between muscles as “intermuscular force transmission.” Intermuscular force transmission implies that two muscles are not mechanically independent. That is, it implies the muscles are arranged in series (or partly in series and partly in parallel) and that their joint torques sum nonlinearly. One view holds that intermuscular force transmission is ubiquitous and significant (5). If true, this would have important implications for muscle physiology. It would imply that the neural regulation of force is more complex than previously thought and that previously ignored mechanisms of muscle adaptation and pathophysiology need to be revisited. Significant intermuscular force transmission would also present a major impediment to biomechanical modeling of muscles. Many structures provide potential anatomic substrates for intermuscular force transmission. Most obviously, some muscles (such as triceps surae in some species) share common tendons. Occasionally the tendons of one muscle branch and connect to adjacent tendons. An example is the vincula longa, which in humans connects flexor digitorum superficialis to flexor digitorum profundus. Last, an extensive network of “myofascial” connective tissue envelopes and connects muscles to each other (1, 2, 6). These structures provide a potential pathway for the transmission of force between muscles. It is also theoretically possible that intermuscular force transmission could occur even in the absence of connecting structures if muscles generated significant frictional forces when they moved relative to each other. In the last decade, one productive laboratory in the Netherlands has reported many cleverly designed experiments investigating epimuscular force transmission (for review, see 5). The experiments were conducted on muscle preparations in which, as far as possible, myofascial connections were preserved. The following observations support the existence of epimuscular force transmission: 1) force measured at a muscle’s proximal tendon does not always equal the force measured at its distal tendon (6, 8); 2) surgical isolation of a muscle, which frees the muscle from its myofascial connections, changes the muscle’s length-tension properties and abolishes differences between forces measured at proximal and distal tendons (6); and 3) changes in the length of one muscle change the lengthtension properties of a second muscle (8). These observations provide evidence of epimuscular force transmission, but only the last observation provides evidence of intermuscular force transmission. That is, only the last observation demonstrates that force is transmitted from one muscle to another. There are reasons to be concerned about the physiological relevance of these findings. Under physiological conditions, muscles are displaced relative to other structures (2). The significance of intermuscle displacements is that they determine the strains experienced by myofascial tissue, and therefore also (if intermuscular force transmission is mediated by myofascial connections) the magnitude of intermuscular force transmission. A major criticism of the observations used to demonstrate intermuscular force transmission is that it is not clear that they were made within usual physiological ranges of displacements between muscles and other structures. In a study in the Journal of Applied Physiology, Maas and Sandercock (8a) describe an alternative approach to test the importance of intermuscular force transmission. For the primary experiment, they used a cat hindlimb preparation in which the myofascial network remained nearly completely intact. They showed that changing the knee angle did not influence the ankle torque produced by selective stimulation of the soleus muscle. (Changing the knee angle changes the length of the gastrocnemius, but not the soleus.) These data suggest there is little or no intermuscular force transmission between the cat gastrocnemius and soleus muscles at physiological lengths. Maas and Sandercock’s approach was to leave the gastrocnemius and soleus muscles’ insertions attached and to change muscle lengths by manipulating the position of the ankle and knee. With this approach the displacements between the resting gastrocnemius and soleus muscles were necessarily within the ranges that occur in vivo, and thus this experimental preparaAddress for reprint requests and other correspondence: R. D. Herbert, The George Institute for International Health, PO Box M201, Camperdown NSW 2050, Australia (e-mail: [email protected]). J Appl Physiol 104: 1549–1550, 2008; doi:10.1152/japplphysiol.90511.2008.