Muscle Coordination Is Habitual Rather than Optimal

Abstract

When sharing load among multiple muscles, humans appear to select an optimal pattern of activation that minimizes costs such as the effort or variability of movement. How the nervous system achieves this behavior, however, is unknown. Here we show that contrary to predictions from optimal control theory, habitual muscle activation patterns are surprisingly robust to changes in limb biomechanics. We first developed a method to simulate joint forces in real time from electromyographic recordings of the wrist muscles. When the model was altered to simulate the effects of paralyzing a muscle, the subjects simply increased the recruitment of all muscles to accomplish the task, rather than recruiting only the useful muscles. When the model was altered to make the force output of one muscle unusually noisy, the subjects again persisted in recruiting all muscles rather than eliminating the noisy one. Such habitual coordination patterns were also unaffected by real modifications of biomechanics produced by selectively damaging a muscle without affecting sensory feedback. Subjects naturally use different patterns of muscle contraction to produce the same forces in different pronation-supination postures, but when the simulation was based on a posture different from the actual posture, the recruitment patterns tended to agree with the actual rather than the simulated posture. The results appear inconsistent with computation of motor programs by an optimal controller in the brain. Rather, the brain may learn and recall command programs that result in muscle coordination patterns generated by lower sensorimotor circuitry that are functionally "good-enough."

The Striatum: Where Skills and Habits Meet

“…However, these observations need to be tempered in light of the fact that, in many situations, optimality is not essential. Instead, muscle synergies seem to be built on habits that are "good enough" rather than optimal (de Rugy et al 2012). …”

Unexpected acoustic stimulation during action preparation reveals gradual re-specification of movement direction

“…The experiments involved isometric wrist contractions using a custom-built device (see de Rugy et al, 2012)) that held the hand and forearm in a neutral position throughout the experiment (see Figure 1A). Participants had their hands snugly fit into the device to reduce any time lag between muscle contractions and recording of forces generate by their wrists.…”

Nature of the coupling between neural drive and force-generating capacity in the human quadriceps muscle

“…For example, during a task where the mechanical advantage of the first dorsal interosseous muscle is increased by increasing its moment arm through altered thumb posture, there is an adaptive increase in the neural drive to that muscle [3]. This adaptive change in drive to match mechanical efficacy is not universal; when the force-generating capacity of a muscle is acutely decreased by muscle damage, activation of all synergist muscles (including the injured muscle) increases rather than recruitment of only the noninjured muscles [4]. This strategy appears suboptimal and may be explained by the limited potential for a short-term redistribution of neural drive between some synergist muscles [5,6].…”