Common motor patterns of asymmetrical and symmetrical bipedal gaits

Abstract

Background Synergy modules have been used to describe activation of lower limb muscles during locomotion and hence to understand how the system controls movement. Walking and running have been shown shared synergy patterns suggesting common motor control of both symmetrical gaits. Unilateral skipping, an equivalent gait to the quadrupedal gallop in humans, has been defined as the third locomotion paradigm but the use by humans is limited due to its high metabolic cost. Synergies in skipping have been little investigated. In particular, to the best of our knowledge, the joint study of both trailing and leading limbs has never been addressed before. Research question How are organized muscle activation patterns in unilateral skipping? Are they organized in the same way that in symmetrical gaits? If yes, which are the muscle activation patterns in skipping that make it a different gait to walking or running? In the present research, we investigate if there are shared control strategies for all gaits in locomotion. Addressing these questions in terms of muscle synergies could suggest possible determinants of the scarce use of unilateral skipping in humans. Methods Electromyographic data of fourteen bilateral muscles were collected from volunteers while performing walking, running and unilateral skipping on a treadmill. Also, spatiotemporal gait parameters were computed from 3D kinematics. The modular composition and activation timing extracted by non-negative matrix factorization were analyzed to detect similarities and differences among symmetrical gaits and unilateral skipping. Results Synergy modules showed high similarity throughout the different gaits and between trailing and leading limbs during unilateral skipping. The synergy associated with the propulsion force operated by calf muscles was anticipated in bouncing gaits. Temporal features of synergies in the leading leg were very similar to those observed for running. The different role of trailing and leading legs in unilateral skipping was reflected by the different timing in two modules. Activation for weight acceptance was anticipated and extended in the trailing leg, preparing the body for landing impact after the flight phase. A different behaviour was detected in the leading leg, which only deals with a pendular weight transference. Significance The evidence gathered in this work supports the hypothesis of shared modules among symmetrical and asymmetrical gaits, suggesting a common motor control despite of the infrequent use of unilateral skipping in humans. Unilateral skipping results from phase-shifted activation of similar muscular groups used in symmetrical gaits, without the need for new muscular groups. The high and anticipated muscle activation in the trailing leg for landing could be the key distinctive event of unilateral skipping.

Skipping without and with hurdles in bipedal macaque: global mechanics

“…Human bipedal gallopers used a higher leg stiffness as compared with macaques. This was also confirmed in a recent study where kinematic parameters were used to estimate leg stiffness during unilateral skipping or galloping ( Pequera et al, 2021 ). In that study, the stiffness of the trailing leg by far exceeded the values obtained for the leading leg and the values obtained in our study for the macaques (from regression v Fr =1: k trail =46.4 [ m g / l e0 ]; k lead =23.8 [ m g / l e0 ]; Pequera et al, 2021 ).…”

“…This was also confirmed in a recent study where kinematic parameters were used to estimate leg stiffness during unilateral skipping or galloping ( Pequera et al, 2021 ). In that study, the stiffness of the trailing leg by far exceeded the values obtained for the leading leg and the values obtained in our study for the macaques (from regression v Fr =1: k trail =46.4 [ m g / l e0 ]; k lead =23.8 [ m g / l e0 ]; Pequera et al, 2021 ). In our study of human unilateral skipping, stiffness of the leading leg was enhanced as in the macaque ( v Fr ≈1: k trail =34.9 [ m g / l e0 ]; k lead =44.1 [ m g / l e0 ]; Müller and Andrada, 2018 ).…”

“…Bipedal galloping seems to represent a quite natural gait. In human skipping, the coordination at the hip joint enforces a differential operation of trailing and leading legs facilitating skipping (Pequera et al, 2021). We assume that, despite of the limited hip extension, the compliant legs identified in the macaques (Blickhan et al, 2018) allow for a differential function of the leading and trailing leg.…”

Brain’s Energy After Stroke: From a Cellular Perspective Toward Behavior

“…Lower limb muscles during walking are organized in four synergy modules, corresponding to specific parts of the stance (weight acceptance, midstance, and toe-off) and swing phases ( Pequera et al, 2021 ). However, in post-stroke patients, a reduction of the number of synergy modules in the paretic limb has been observed, and most of them only require two or three modules ( Clark et al, 2010 ).…”

Differential leg and trunk operation during skipping without and with hurdles in bipedal Japanese macaque

“…The similarity of peak ground‐reaction forces and impulses has been documented for human skipping (Fiers et al, 2013). However, during bipedal grounded and aerial running, macaques utilize a more compliant leg compared to humans (Blickhan et al, 2018, 2023; Müller & Andrada, 2018; Pequera et al, 2021). The compliant legs along with their consequences were accentuated as being typical for nonhuman primates in general, and possibly advantageous also for our ancestors (Schmitt, 2003).…”