Understanding muscle coordination of the human leg with dynamical simulations

Abstract

Muscles coordinate multijoint motion by generating forces that cause reaction forces throughout the body. Thus, a muscle can redistribute existing segmental energy by accelerating some segments and decelerating others. In the process, a muscle may also produce or absorb energy, in which case its summed energetic effect on the segments is positive or negative, respectively. This Borelli Lecture shows how dynamical simulations derived from musculoskeletal models reveal muscle-induced segmental energy redistribution and muscle co-functions and synergies. Synergy occurs when co-excited muscles distribute segmental energy differently to execute the motor task. In maximum height jumping, high vertical velocity at lift-off occurs desirably at full body extension because biarticular leg muscles redistribute the energy produced by the uniarticular leg muscles. In pedaling, synergistic ankle plantarflexor force generation during leg extension allows the high energy produced by the uniarticular hip and knee extensors to be delivered to the crank. An analogous less-powerful flexor synergy exists during leg flexion. Hamstrings reduce crank deceleration during the leg extension-to-flexion transition by not only producing energy but delivering it to the crank through its contribution to the tangential (accelerating) crank force, though this hamstrings function occurs at the opposite (flexion-extension) transition when pedaling backwards. In walking, the eccentric quadriceps activity in early stance not only decelerates the leg but also accelerates the trunk. In mid-stance, the uni- and biarticular plantarflexors, by having opposite segmental energetic effects, act in synergy to support the whole body, so segmental potential and kinetic energy exchange can occur. To conclude, the extraction of unmeasurable variables from dynamical simulations emulating task kinematics, kinetics, and EMGs shows how the production of force and energy by individual muscles contribute to the energy flow among the individual segments during task execution.

Introduction

Muscles participate critically in the execution of human motor tasks. When muscle strength, power, or coordination is impaired, task execution is compromised. So what is the exact role of a muscle in a specific task?

Fortunately for us, a muscle can perform many mechanical functions. A muscle can develop force and power, and over time produce work output. Or it can dissipate mechanical energy if its active fibers are stretched. When its tendon, aponeurosis, and other in-series elastic elements are stretched, energy is stored. The force–length–velocity property of muscle can stabilize movement with its impedance-like function before reflexes become operative (Brown and Loeb, 2000; Gerritsen et al., 1998; Loeb et al., 1999). Less appreciated is a muscle's critical role to redistribute mechanical energy among the body segments during task execution (Fregly and Zajac, 1996; Neptune et al., 2001).

Muscles redistribute the net mechanical energy of the body segments because each muscle force causes reaction forces throughout the body with the net effect being to accelerate some segments and decelerate others. If the segments are not at rest, segmental energy increases in the accelerated segments and decreases in the decelerated ones. If a muscle is isometric while generating force, the net energy change among the segments caused by the muscle is zero, although energy distribution among segments can occur. The isometric force generated by the muscle can cause energy to increase in some segments and decrease in others by the same amount. This function of a muscle to cause energy to be exchanged among segments, whether the muscle is isometric, eccentric, or concentric, can be more important to task execution than its role in producing energy and delivering that energy to the segments (Zajac et al., 2002a).

By working co-functionally, or synergistically, muscles coordinate force generation so individual segments gain and lose energy consonant with the task. Usually no one muscle can cause the required segmental energetic exchanges. At times, multiple muscles will cause similar segmental exchanges to occur by accelerating the same segments and decelerating others. The co-excited muscles are then called co-functional (Zajac et al., 2002a). Co-functional muscle activity may be required, for example, when segmental energetic exchanges are so high that force production in one muscle is insufficient.

At other times co-excited muscles work synergistically but not co-functionally; i.e., the segments accelerated by muscles differ causing oppositely directed segmental exchanges to occur (Zajac et al., 2002a). Such synergistic muscle activity may occur, for example, when one muscle produces the energy required in task execution but is unable to deliver it to a target segment because its force does not accelerate the segment; instead its force acts to accelerate other segments. Another muscle, which may not produce energy, may be co-excited because its generation of force opposes the acceleration of the other segments while accelerating the target segment. In this example of muscle synergy, therefore, one muscle produces the energy and another causes opposing segmental accelerations and decelerations so the energy reaches the target segment.

Unfortunately, the contributions of individual muscle forces to the reaction forces throughout the body and to the acceleration and deceleration of segments cannot be measured. In fact, rarely can the muscle forces in humans (or animals) be recorded, much less from many muscles simultaneously (however, see Gregor et al., 1987; Herzog et al., 1993). Given that we are usually limited to measurements of muscle (EMG) activity, the kinematics of the movement, and the forces exerted by the body on contact objects (e.g., the ground in walking), many musculoskeletal variables escape direct observation. But fortunately these and other kinetic quantities can be estimated from dynamical musculoskeletal simulations.

In the context of segmental energy redistribution, this paper summarizes some of the results found from simulations of motor tasks by me and my collaborators over the past 25 yr. Jumping is reviewed somewhat, but pedaling and walking are emphasized because concepts can be espoused better. The concept that a muscle can act to accelerate all joints (even unspanned ones) into rotation and that a biarticular muscle can act to accelerate one of its spanned joints into rotation opposite to its anatomical classification (i.e., opposite to its joint moment) are not reviewed here (see Zajac, 1993; Zajac and Gordon, 1989).