Neuromotor Dynamics of Human Locomotion in Challenging Settings

Abstract

Is the control of movement less stable when we walk or run in challenging settings? Intuitively, one might answer that it is, given that challenging locomotion externally (e.g., rough terrain) or internally (e.g., age-related impairments) makes our movements more unstable. Here, we investigated how young and old humans synergistically activate muscles during locomotion when different perturbation levels are introduced. Of these control signals, called muscle synergies, we analyzed the local stability and the complexity (or irregularity) over time. Surprisingly, we found that perturbations force the central nervous system to produce muscle activation patterns that are less unstable and less complex. These outcomes show that robust locomotion control in challenging settings is achieved by producing less complex control signals that are more stable over time, whereas easier tasks allow for more unstable and irregular control.

Lower complexity of motor primitives ensures robust control of high-speed human locomotion

“…Moreover, we and others proposed that the width of motor primitives increases to ensure robust control in the presence of internal and external perturbations [10,19,[25][26][27], suggesting that this might be a compensatory mechanism adopted by the CNS to 75 cope with the postural instability of locomotion in health and pathology [25,26]. We observed the neural strategy of motor primitive widening in wild-type mice [19] and in humans affected by multiple sclerosis [28] or healthy adults undergoing external perturbations [10,11], but not in genetically modified mice that lacked feedback from proprioceptors [19]. Due to these observations, we concluded that intact systems use wider (i.e.…”

“…The cost of running is quasi-linearly correlated with speed, at least if the nonlinear contribution 50 of air resistance is neglected [4][5][6][7][8][9]. Yet, despite the profound mechanical and energetic differences, walking and running seem to be sharing similar neural control [3, 10,11].…”

“…Synergies were divided into time-independent (motor modules) and time-dependent (motor 65 primitives) coefficients. The Higuchi's fractal dimension (HFD) was used to evaluate the complexity of motor primitives, taken as self-affine time series [11,20,21]. Defining robustness as the ability to cope with perturbations [10], it follows that biological systems can manage to maintain function despite disturbances only through robust control [22][23][24].…”

“…Recently, we showed that challenging locomotion conditions (i.e. in the presence of external mechanical perturbations and in aging) manifest lowered complexity of motor primitives [11]. Moreover, we and others proposed that the width of motor primitives increases to ensure robust control in the presence of internal and external perturbations [10,19,[25][26][27], suggesting that this might be a compensatory mechanism adopted by the CNS to 75 cope with the postural instability of locomotion in health and pathology [25,26].…”

“…Due to these observations, we concluded that intact systems use wider (i.e. of longer duration) and less 80 complex control signals to create an overlap between chronologically-adjacent synergies to regulate motor function through robust control [10,11,28].…”