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      Changes in mechanical work during neural adaptation to asymmetric locomotion

      , , , ,
      The Journal of Experimental Biology
      The Company of Biologists

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          Abstract

          <p id="d6793351e160">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 <sup>−1</sup> 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. </p><p class="first" id="d6793351e167"> <b>Summary:</b> 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. </p>

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          Most cited references31

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          Contributions of the individual ankle plantar flexors to support, forward progression and swing initiation during walking.

          Walking is a motor task requiring coordination of many muscles. Previous biomechanical studies, based primarily on analyses of the net ankle moment during stance, have concluded different functional roles for the plantar flexors. We hypothesize that some of the disparities in interpretation arise because of the effects of the uniarticular and biarticular muscles that comprise the plantar flexor group have not been separated. Furthermore, we believe that an accurate determination of muscle function requires quantification of the contributions of individual plantar flexor muscles to the energetics of individual body segments. In this study, we examined the individual contributions of the ankle plantar flexors (gastrocnemius (GAS); soleus (SOL)) to the body segment energetics using a musculoskeletal model and optimization framework to generate a forward dynamics simulation of normal walking at 1.5 m/s. At any instant in the gait cycle, the contribution of a muscle to support and forward progression was defined by its contribution to trunk vertical and horizontal acceleration, respectively, and its contribution to swing initiation by the mechanical energy it delivers to the leg in pre-swing (i.e., double-leg stance prior to toe-off). GAS and SOL were both found to provide trunk support during single-leg stance and pre-swing. In early single-leg stance, undergoing eccentric and isometric activity, they accelerate the trunk vertically but decelerate forward trunk progression. In mid single-leg stance, while isometric, GAS delivers energy to the leg while SOL decelerates it, and SOL delivers energy to the trunk while GAS decelerates it. In late single-leg stance through pre-swing, though GAS and SOL both undergo concentric activity and accelerate the trunk forward while decelerating the downward motion of the trunk (i.e., providing forward progression and support), they execute different energetic functions. The energy produced from SOL accelerates the trunk forward, whereas GAS delivers almost all its energy to accelerate the leg to initiate swing. Although GAS and SOL maintain or accelerate forward motion in mid single-leg stance through pre-swing, other muscles acting at the beginning of stance contribute comparably to forward progression. In summary, throughout single-leg stance both SOL and GAS provide vertical support, in mid single-leg stance SOL and GAS have opposite energetic effects on the leg and trunk to ensure support and forward progression of both the leg and trunk, and in pre-swing only GAS contributes to swing initiation.
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            Interlimb coordination during locomotion: what can be adapted and stored?

            Interlimb coordination is critically important during bipedal locomotion and often must be adapted to account for varying environmental circumstances. Here we studied adaptation of human interlimb coordination using a split-belt treadmill, where the legs can be made to move at different speeds. Human adults, infants, and spinal cats can alter walking patterns on a split-belt treadmill by prolonging stance and shortening swing on the slower limb and vice versa on the faster limb. It is not known whether other locomotor parameters change or if there is a capacity for storage of a new motor pattern after training. We asked whether adults adapt both intra- and interlimb gait parameters during split-belt walking and show aftereffects from training. Healthy subjects were tested walking with belts tied (baseline), then belts split (adaptation), and again tied (postadaptation). Walking parameters that directly relate to the interlimb relationship changed slowly during adaptation and showed robust aftereffects during postadaptation. These changes paralleled subjective impressions of limping versus no limping. In contrast, parameters calculated from an individual leg changed rapidly to accommodate split-belts and showed no aftereffects. These results suggest some independence of neural control of intra- versus interlimb parameters during walking. They also show that the adult nervous system can adapt and store new interlimb patterns after short bouts of training. The differences in intra- versus interlimb control may be related to the varying complexity of the parameters, task demands, and/or the level of neural control necessary for their adaptation.
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              Energetic consequences of walking like an inverted pendulum: step-to-step transitions.

              Walking like an inverted pendulum reduces muscle-force and work demands during single support, but it also unavoidably requires mechanical work to redirect the body's center of mass in the transition between steps, when one pendular motion is substituted by the next. Production of this work exacts a proportional metabolic cost that is a major determinant of the overall cost of walking.
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                Author and article information

                Journal
                The Journal of Experimental Biology
                J Exp Biol
                The Company of Biologists
                0022-0949
                1477-9145
                August 16 2017
                August 15 2017
                August 15 2017
                June 08 2017
                : 220
                : 16
                : 2993-3000
                Article
                10.1242/jeb.149450
                5576064
                28596214
                10c78ac5-3fc3-49dc-bdec-81c0e2e25620
                © 2017

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