Changes in mechanical work during neural adaptation to asymmetric locomotion

ABSTRACT Minimizing whole-body metabolic cost has been suggested to drive the neural processes of locomotor adaptation. Mechanical work performed by the legs should dictate the major changes in whole-body metabolic cost of walking while providing greater insight into temporal and spatial mechanisms of adaptation. We hypothesized that changes in mechanical work by the legs during an asymmetric split-belt walking adaptation task could explain previously observed changes in whole-body metabolic cost. We predicted that subjects would immediately increase mechanical work performed by the legs when first exposed to split-belt walking, followed by a gradual decrease throughout adaptation. Fourteen subjects walked on a dual-belt instrumented treadmill. Baseline trials were followed by a 10-min split-belt adaptation condition with one belt running three times faster than the other. A post-adaptation trial with both belts moving at 0.5 m s−1 demonstrated neural adaptation. As predicted, summed mechanical work from both legs initially increased abruptly and gradually decreased over the adaptation period. The initial increase in work was primarily due to increased positive work by the leg on the fast belt during the pendular phase of the gait cycle. Neural adaptation in asymmetric split-belt walking reflected the reduction of pendular phase work in favor of more economical step-to-step transition work. This may represent a generalizable framework for how humans initially and chronically learn new walking patterns. Summary: Minimizing mechanical work performed by the legs may drive locomotor adaptation, with wide relevance for the control of legged locomotion and motor learning in novel environments.

[1]  Arthur D Kuo,et al.  Energetics of actively powered locomotion using the simplest walking model. , 2002, Journal of biomechanical engineering.

[2]  Peter G Adamczyk,et al.  Redirection of center-of-mass velocity during the step-to-step transition of human walking , 2009, Journal of Experimental Biology.

[3]  A. Ruina,et al.  A collisional model of the energetic cost of support work qualitatively explains leg sequencing in walking and galloping, pseudo-elastic leg behavior in running and the walk-to-run transition. , 2005, Journal of theoretical biology.

[4]  Arthur D Kuo,et al.  The six determinants of gait and the inverted pendulum analogy: A dynamic walking perspective. , 2007, Human movement science.

[5]  Chris J. Hass,et al.  Effects of dopaminergic therapy on locomotor adaptation and adaptive learning in persons with Parkinson's disease , 2014, Behavioural Brain Research.

[6]  Hannah J. Block,et al.  Interlimb coordination during locomotion: what can be adapted and stored? , 2005, Journal of neurophysiology.

[7]  R. Kram,et al.  Mechanical and metabolic determinants of the preferred step width in human walking , 2001, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[8]  Jessica C. Selinger,et al.  Humans Can Continuously Optimize Energetic Cost during Walking , 2015, Current Biology.

[9]  Sukyung Park,et al.  Gait strategy changes with acceleration to accommodate the biomechanical constraint on push-off propulsion. , 2012, Journal of biomechanics.

[10]  James M. Finley,et al.  Learning to be economical: the energy cost of walking tracks motor adaptation , 2013, The Journal of physiology.

[11]  D. Reisman,et al.  Locomotor adaptation on a split-belt treadmill can improve walking symmetry post-stroke. , 2007, Brain : a journal of neurology.

[12]  Young-Hui Chang,et al.  The motor and the brake of the trailing leg in human walking: leg force control through ankle modulation and knee covariance , 2016, Experimental Brain Research.

[13]  J. Donelan,et al.  Force treadmill for measuring vertical and horizontal ground reaction forces. , 1998, Journal of applied physiology.

[14]  A. Bastian,et al.  Thinking about walking: effects of conscious correction versus distraction on locomotor adaptation. , 2010, Journal of neurophysiology.

[15]  Brian P Selgrade,et al.  Locomotor control of limb force switches from minimal intervention principle in early adaptation to noise reduction in late adaptation. , 2015, Journal of neurophysiology.

[16]  J Maxwell Donelan,et al.  Coordination of push-off and collision determine the mechanical work of step-to-step transitions when isolated from human walking. , 2012, Gait & posture.

[17]  Andy Ruina,et al.  Energetic Consequences of Walking Like an Inverted Pendulum: Step-to-Step Transitions , 2005, Exercise and sport sciences reviews.

[18]  Steven H Collins,et al.  A simple method for calibrating force plates and force treadmills using an instrumented pole. , 2009, Gait & posture.

[19]  F. Zajac,et al.  Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking. , 2001, Journal of biomechanics.

[20]  Brian P Selgrade,et al.  Two biomechanical strategies for locomotor adaptation to split-belt treadmill walking in subjects with and without transtibial amputation. , 2017, Journal of biomechanics.

[21]  Raul Benitez,et al.  Motor adaptation as a greedy optimization of error and effort. , 2007, Journal of neurophysiology.

[22]  Rodger Kram,et al.  Simultaneous positive and negative external mechanical work in human walking. , 2002, Journal of biomechanics.

[23]  A. Schneiders,et al.  A Valid and Reliable Clinical Determination of Footedness , 2010, PM & R : the journal of injury, function, and rehabilitation.

[24]  Helen J. Huang,et al.  Reduction of Metabolic Cost during Motor Learning of Arm Reaching Dynamics , 2012, The Journal of Neuroscience.

[25]  Rodger Kram,et al.  The metabolic and mechanical costs of step time asymmetry in walking , 2013, Proceedings of the Royal Society B: Biological Sciences.

[26]  Young-Hui Chang,et al.  Biomechanics of the human walk-to-run gait transition in persons with unilateral transtibial amputation. , 2016, Journal of biomechanics.

[27]  J. Donelan,et al.  Mechanical work for step-to-step transitions is a major determinant of the metabolic cost of human walking. , 2002, The Journal of experimental biology.

[28]  Kelly A Danks,et al.  Repeated Split-Belt Treadmill Training Improves Poststroke Step Length Asymmetry , 2013, Neurorehabilitation and neural repair.

[29]  J. Donelan Motor Control: No Constant but Change , 2016, Current Biology.

[30]  R. Cham,et al.  Slip-related muscle activation patterns in the stance leg during walking. , 2007, Gait & posture.

[31]  Noritaka Kawashima,et al.  Predictive control of ankle stiffness at heel contact is a key element of locomotor adaptation during split-belt treadmill walking in humans. , 2014, Journal of neurophysiology.

[32]  Dominic James Farris,et al.  The mechanics and energetics of human walking and running: a joint level perspective , 2012, Journal of The Royal Society Interface.

[33]  Young-Hui Chang,et al.  Humans robustly adhere to dynamic walking principles by harnessing motor abundance to control forces , 2013, Experimental Brain Research.

[34]  Jill S Higginson,et al.  Gait parameters and stride-to-stride variability during familiarization to walking on a split-belt treadmill. , 2010, Clinical biomechanics.