Multiple strategies to correct errors in foot placement and control speed in human walking

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RESEARCH ARTICLE

Multiple strategies to correct errors in foot placement and control speed in human walking Shakiba Rafiee1,2   · Tim Kiemel1,2 Received: 29 March 2020 / Accepted: 6 October 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Abstract Neural feedback plays a key role in maintaining locomotor stability in the face of perturbations. In this study, we systematically identified properties of neural feedback that contribute to stabilizing human walking by examining how the nervous system responds to small kinematic deviations away from the desired gait pattern. We collected data from 20 participants (9 men and 11 women). We simultaneously applied (1) small continuous mechanical perturbations, forces at the ankles that affected foot placement, and (2) small continuous sensory perturbations, movement of a virtual visual scene that produced the illusion of change in walking speed, to compare how neural feedback responds to actual and illusory kinematic deviations. We computed phasedependent impulse response functions that describe kinematic and muscular responses to small brief perturbations to identify critical phases of the gait cycle when the nervous system modulates muscle activity. In addition to the known foot-placement strategies that counteract kinematic displacement, such as the modulation of the hamstring muscle group during swing, we identified phase-specific muscle modulations that compensated for the perturbations. In particular, our results suggested that an early-stance modulation of anterior leg muscles (i.e., dorsiflexors and quadriceps) is a general control mechanism that serves to control forward body propulsion and compensates for errors in foot placement. Another detected general compensatory strategy was the late-stance modulation of the rectus femoris and gastrocnemius muscles, which controls walking speed in the next cycle. Keywords  System Identification · Impulse Response · Mechanical Perturbation · Visual Perturbation · Stability

Introduction Humans are able to produce and maintain stable rhythmic locomotion in face of constant perturbations that arise from internal sources, e.g., neuromuscular and sensory noise (Faisal et al. 2008), and external sources. To control gait, the nervous system actively modulates the rhythmic stimulation of muscles. For example, two strategies for speed control are the late-stance modulation of the foot plantar flexors that Communicated by Francesco Lacquaniti. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0022​1-020-05949​-x) contains supplementary material, which is available to authorized users. * Shakiba Rafiee [email protected] 1



Department of Kinesiology, University of Maryland, College Park, MD 20742, USA



Neuroscience and Cognitive Science Program, University of Maryland, College Park, MD 20742, USA

2

serves to control push-off (Yang et al. 1991; Grey et al. 2004) and the stance-to-swing modulation of the rectus femoris muscle that serves to control cadence (Nene et al