Walking Is Not Like Reaching: Evidence from Periodic Mechanical Perturbations

The control architecture underlying human reaching has been established, at least in broad outline. However, despite extensive research, the control architecture underlying human locomotion remains unclear. Some studies show evidence of high-level control focused on lower-limb trajectories; others suggest that nonlinear oscillators such as lower-level rhythmic central pattern generators (CPGs) play a significant role. To resolve this ambiguity, we reasoned that if a nonlinear oscillator contributes to locomotor control, human walking should exhibit dynamic entrainment to periodic mechanical perturbation; entrainment is a distinctive behavior of nonlinear oscillators. Here we present the first behavioral evidence that nonlinear neuro-mechanical oscillators contribute to the production of human walking, albeit weakly. As unimpaired human subjects walked at constant speed, we applied periodic torque pulses to the ankle at periods different from their preferred cadence. The gait period of 18 out of 19 subjects entrained to this mechanical perturbation, converging to match that of the perturbation. Significantly, entrainment occurred only if the perturbation period was close to subjects’ preferred walking cadence: it exhibited a narrow basin of entrainment. Further, regardless of the phase within the walking cycle at which perturbation was initiated, subjects’ gait synchronized or phase-locked with the mechanical perturbation at a phase of gait where it assisted propulsion. These results were affected neither by auditory feedback nor by a distractor task. However, the convergence to phase-locking was slow. These characteristics indicate that nonlinear neuro-mechanical oscillators make at most a modest contribution to human walking. Our results suggest that human locomotor control is not organized as in reaching to meet a predominantly kinematic specification, but is hierarchically organized with a semi-autonomous peripheral oscillator operating under episodic supervisory control. Citation: Ahn J, Hogan N (2012) Walking Is Not Like Reaching: Evidence from Periodic Mechanical Perturbations. PLoS ONE 7(3): e31767. doi:10.1371/ journal.pone. 0031767 Editor: Paul L. Gribble, The University of Western Ontario, Canada Received July 22, 2011; Accepted January 17, 2012; Published March 27, 2012 Copyright: 2012 Ahn, Hogan. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported in part by the New York State Center of Research Excellence, contract CO19772; the Eric P. and Evelyn E. Newman Fund; and a Samsung Scholarship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: NH holds equity in Interactive Motion Technologies, Inc. that manufactures the robotic technology used in this study. The authors confirm that NH’s affiliation to Interactive Motion Technologies, Inc. does not alter the authors’ adherence to the PLoS ONE policies on sharing data and materials. As declared in Funding, this work was supported in part by Samsung Scholarship. Although it shares the same name as Samsung which is a commercial organization, Samsung Scholarship foundation is a nonprofit organization which supports young scholars without any obligation related with Samsung. (More information about Samsung Scholarship foundation is available from http://www.ssscholarship.com). Therefore, this does not alter the authors’ adherence to all the PLoS ONE policies on sharing data and materials. * E-mail: aje@mit.edu