Damping Actions of the Neuromuscular System With Inertial Loads: Human Flexor Pollicis Longus Muscle

Abstract

Our previous work in an animal model showed that neuromuscular damping properties help maintain limb posture by effectively dissipating mechanical energy arising from disturbances. The purpose of this study was to determine whether similar damping properties were expressed in intact, normal human muscles. To review briefly, when the reflexively active soleus muscle in a decerebrate cat is coupled to an inertial load, application of a force impulse to the load results in lightly damped oscillations. By calculating the logarithmic decrement in muscle velocity following the impulse (the decrement being related to the amount of energy dissipated from the inertia), we found that damping increased with oscillation amplitude, a nonlinear property. This nonlinearity represents an automatic compensation for larger perturbations. Our findings in parallel experiments on the interphalangeal joint of the human thumb were that the long thumb flexor, the flexor pollicis longus (FPL), displayed mechanical and reflex behavior closely comparable to that reported earlier for the cat soleus, despite differences in architectural and metabolic properties between these muscles. Specifically, by selecting experimental trials that did not include voluntary interventions, we observed amplitude-dependent differences in damping in which larger amplitude movements elicited larger damping than did smaller movements. In addition, even after accounting for amplitude-dependent differences in damping, damping was found to be larger in later cycles than in the first cycle. This nonlinearity indicates that both mechanical properties of muscle and reflex mechanisms are dependent on prior movement history. We propose that this history-dependent behavior arises from the effects of prior movement on stretch reflex gain, and these effects are mediated primarily via changes in muscle spindle properties. Recordings of electromyographic activity from the FPL, during the first and second cycles of oscillation supported this postulate of a reduced reflex gain following prior motion. The functional significance of these nonlinear damping properties is that during the initial muscle stretch, the stiffness is high, which helps to preserve the initial position (although at the expense of promoting oscillation). Subsequently, the ensuing increase in damping helps suppress continuing oscillation. This sequence of varying mechanical properties is broadly analogous to the features of a predictive, or feed-forward controller, designed to produce a response that initially maintains position, and subsequently dampens oscillations. These results show that the intrinsic properties of muscle and spinal reflexes automatically provide a complex time-varying response, appropriate for maintenance of stable limb posture.