Unconstrained muscle-tendon workloops indicate resonance tuning as a mechanism for elastic limb behavior during terrestrial locomotion

Abstract

In terrestrial locomotion, there is a missing link between observed spring-like limb mechanics and the physiological systems driving their emergence. Previous modeling and experimental studies of bouncing gait (e.g., walking, running, hopping) identified muscletendon interactions that cycle large amounts of energy in series tendon as a source of elastic limb behavior. The neural, biomechanical, and environmental origins of these tuned mechanics, however, have remained elusive. To examine the dynamic interplay between these factors, we developed an experimental platform comprised of a feedback-controlled servo-motor coupled to a biological muscletendon. Our novel motor controller mimicked in vivo inertial/gravitational loading experienced by muscles during terrestrial locomotion, and rhythmic patterns of muscle activation were applied via stimulation of intact nerve. This approach was based on classical workloop studies, but avoided predetermined patterns of muscle strain and activation-constraints not imposed during real-world locomotion. Our unconstrained approach to position control allowed observation of emergent muscle-tendon mechanics resulting from dynamic interaction of neural control, active muscle, and system material/inertial properties. This study demonstrated that, despite the complex nonlinear nature of musculotendon systems, cyclic muscle contractions at the passive natural frequency of the underlying biomechanical system yielded maximal forces and fractions of mechanical work recovered from previously stored elastic energy in seriescompliant tissues. By matching movement frequency to the natural frequency of the passive biomechanical system (i.e., resonance tuning), muscle-tendon interactions resulting in spring-like behavior emerged naturally, without closed-loop neural control. This conceptual framework may explain the basis for elastic limb behavior during terrestrial locomotion.muscle-tendon mechanics | elastic limb behavior | neural control | resonance | terrestrial locomotion E lastic limb behavior is a hallmark of terrestrial locomotion; the mechanics can be described by the physics of spring-mass interaction (1-4). Simple models that treat the entire leg as a linear spring loaded inverted pendulum (SLIP), and the body as a point mass can predict the mechanics of hopping (3), walking (4), and running (1, 4), as well as more subtle features of gait like the importance of swing-leg retraction for dynamic stability (5, 6). This simplified mechanical framework for describing whole limb behavior has led to breakthroughs in understanding of control targets in both biological locomotion (7) and bio-inspired walking robots (8, 9).Although these mechanics are simple conceptually, understanding how they emerge from a biological limb has proven to be a far greater challenge. Every skeletal muscle exhibits nonlinear excitation-contraction coupling (10), nonlinear dependence of active muscle force on fascicle strain (11) and rate of strain (12), nonlinear force-displacement dynamics in tendon (13) and p...

Distinct muscle-tendon interaction during running at different speeds and in different loading conditions

“…The advantage of the greater time availability may be linked to the way mechanical resonance of the system was altered when adding mass. In vitro data suggest that spring-like limb behavior during locomotion may be naturally regulated, by matching muscle strain patterns to the resonance frequency of the MTU (29). Hence, by increasing body mass without increasing running speed, the neuromuscular system may adopt an activation pattern in resonance with a lower natural frequency, maximizing force production and utilization of elastic energy.…”

Operating length and velocity of human vastus lateralis muscle during walking and running

“…The muscle activation pattern (onset, duration and amplitude) can affect the interaction within the MTU and, thus, the operating length and velocity of the fascicle 17 – 20 . By adjusting the stimulation onset timing during a work loop paradigm of an isolated bullfrog’s plantaris MTU subjected to cyclic strain, Sawicki and colleagues (2015) 18 were able to influence the degree of decoupling of muscle fascicle and MTU trajectories.…”

“…Only a specific stimulation onset timing condition led to zero net mechanical work of the MTU, which compares to terrestrial locomotion, featuring relatively small length changes of the fascicles and consequently lower fascicle shortening velocity compared to the MTU 18 . Moreover, when the cyclic contractions were matched with the natural frequency of a biological MTU in a more unconstrained work loop, this resulted in a naturally emerging spring-like behaviour with maximal muscle forces and maximal fractions of mechanical work performed by the series elastic elements 20 . Although in vitro studies may not directly reflect the complex interactions during human locomotion in vivo , apparently the muscle activation pattern plays a key role for the interaction of the MTU components 21 and an adjusted activation pattern may facilitate fascicle operating conditions towards high force potentials.…”

Tuning of feedforward control enables stable muscle force-length dynamics after loss of autogenic proprioceptive feedback

“…In addition to widely recognized force-length and force-velocity ‘Hill-type’ properties, muscle exhibits short and long-term history-dependent changes in force capacity in response to stretch and shortening ( Edman, 1975 ; Edman et al, 1978 ; Edman, 1980 ; Josephson, 1999 ; Herzog, 2004 ; Edman, 2012 ; Herzog, 2014 ; Rode et al, 2009 ; Nishikawa et al, 2012 ; Yeo et al, 2013 ; Nishikawa et al, 2018 ). Recent developments in biorobotic platforms that enable controlled muscle experiments with realistic loading and length trajectories are promising tools for advancing our understanding of the role of intrinsic muscle dynamics in the control of movement ( Clemente and Richards, 2012 ; Richards, 2011 ; Robertson and Sawicki, 2015 ). Integrative neuromechanical studies using multiple techniques will be essential for unravelling mechanisms of muscle function, sensorimotor integration and plasticity.…”