Robot-Driven Locomotor Perturbations Reveal Synergy-Mediated, Context-Dependent Feedforward and Feedback Mechanisms of Adaptation

Abstract

Humans respond to mechanical perturbations that affect their gait by changing their motor control strategy. previous work indicates that adaptation during gait is context dependent, and perturbations altering long-term stability are compensated for even at the cost of higher energy expenditure. However, it is unclear if gait adaptation is driven by unilateral or bilateral mechanisms, and what the roles of feedback and feedforward control are in the generation of compensatory responses. Here, we used a robot-based adaptation paradigm to investigate if feedback/feedforward and unilateral/ bilateral contributions to locomotor adaptation are also context dependent in healthy adults. A robot was used to induce two opposite unilateral mechanical perturbations affecting the step length over multiple gait cycles. electromyographic signals were collected and analyzed to determine how muscle synergies change in response to perturbations. The results unraveled different unilateral modulation dynamics of the muscle-synergy activations during adaptation, characterized by the combination of a slow-progressive feedforward process and a fast-reactive feedback-driven process. the relative unilateral contributions of the two processes to motor-output adjustments, however, depended on which perturbation was delivered. overall, these observations provide evidence that, in humans, both descending and afferent drives project onto the same spinal interneuronal networks that encode locomotor muscle synergies. Humans have the ability to modify their motor plan in response to changes in the walking environment, a phenomenon referred to as locomotor adaptation 1. The study of locomotor adaption has been pursued to improve our understanding of the organization of human locomotor circuits, given the inapplicability, in humans, of the invasive techniques employed in animal models. As a case in point, studies in the lamprey, frog, turtle and cat have consistently shown that locomotor control is accomplished by rhythmic activations of lower-level spinal circuits that regulate the activities of fixed neuromuscular modules 2-6. It has been debated if such modules exist in humans 7 , and if they encode the relative levels of activation across muscles 8 , the temporal relations among the activations of muscle groups 9 , or involve more complex structures 10,11. A study on adaptation during forward/backward walking on a split-belt treadmill has provided evidence that human locomotion is controlled by leg-specific and forward/backward-specific independent networks 12. These observations are compatible with a two-level organization of spinal central pattern generator (CPG) circuits where the higher level regulates the

Forward and backward walking share the same motor modules and locomotor adaptation strategies

“…We extracted, in both experiments, the muscle synergy modules and activation patterns relative to the MTUs, similarly to what usually done in muscle synergies analysis [ 17 ]. In this analysis we only used the MTUs that were mapped from the experimental data and we excluded those which were synthesized to avoid the appearance of synergies that were fully synthetic and not based, at least partially, on recorded data.…”

“…The tolerance parameter was set to 0.15 in our analysis, indicating that the single weights of each MTU were allowed a maximal variability of 15% around its value estimated during baseline. The choice of the semi-fixed algorithm is based on the numerous observations by us and others [ 17 , 27 , 29 , 31 , 68 ] indicating that upper and lower limb motor adaptations are well represented by modulation of the activation patterns of fixed or barely changing synergies, while changes in weights (or recruitment of additional/different synergies) are required only when biomechanical task demands change [ 68 ]. The synergy extraction was performed unilaterally, separating the MTUs on the left and right leg.…”

“…These spinal modules appear to be well represented by the muscle synergy module components of the non-negative matrix factorization-based muscle synergy analysis [ 11 , 12 , 13 ]. Although direct physiological evidence of the existence of these spinal circuits cannot currently be derived in humans, recent studies have reinforced the hypothesis behind their existence by showing that the spatial muscle synergy modules obtained by decomposing neuromuscular activity are shared across different tasks [ 14 , 15 ] and are stable during the response to perturbations [ 16 , 17 ]. In light of this evidence, it is possible that FW and BW share, at least partially, the same muscle synergy modules, given the similar role that some muscle groups perform during the two tasks [ 18 ].…”

Characterization of the Adaptation to Visuomotor Rotations in the Muscle Synergies Space

“…We and others have shown (Gentner et al, 2013;De Marchis et al, 2018;Zych et al, 2019;Severini et al, 2020) that adaptations to perturbations in several different tasks are well represented by the changes in the activation patterns H of fixed sets of muscle weights W extracted by applying the NMF algorithm to sets of EMG signals recorded during unperturbed versions of the tasks under analysis. This analysis is usually performed by altering the NMF algorithm by fixing the values of W while allowing the update rule of the NMF algorithm to modify only the values of H. The validity of the fixed-synergies model is often evaluated by showing that the EMG reconstructed using the fixed set of W and the new H can capture the variance of the data up to an arbitrary satisfactory level of a performance metric (e.g., 90% of the variance accounted for).…”

Converging Robotic Technologies in Targeted Neural Rehabilitation: A Review of Emerging Solutions and Challenges

“…As scientific analysis and understanding of human motor control advances in tandem with modern electronics and computational power, the pursuit of more disruptive therapeutic interventions has become possible. For example, the use of robot-driven locomotor perturbations in order to manipulate an individual's motor control strategy for therapeutic purposes is a radical and particularly promising new such approach [245,246]. Such approaches also offer novel insight into human motor control and adaptation that need to be taken into account during the design of protocols for robot-assisted gait rehabilitation [247].…”