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      Corrective Muscle Activity Reveals Subject-Specific Sensorimotor Recalibration

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      1 , 2 , 1 , 2 ,
      eNeuro
      Society for Neuroscience
      EMG, locomotion, motor learning, split-belt walking

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          Abstract

          Recent studies suggest that planned and corrective actions are recalibrated during some forms of motor adaptation. However, corrective (also known as reactive) movements in human locomotion are thought to simply reflect sudden environmental changes independently from sensorimotor recalibration. Thus, we asked whether corrective responses can indicate the motor system’s adapted state following prolonged exposure to a novel walking situation inducing sensorimotor adaptation. We recorded electromyographic (EMG) signals bilaterally on 15 leg muscles before, during, and after split-belts walking (i.e., novel walking situation), in which the legs move at different speeds. We exploited the rapid temporal dynamics of corrective responses upon unexpected speed transitions to isolate them from the overall motor output. We found that corrective muscle activity was structurally different following short versus long exposures to split-belts walking. Only after a long exposure, removal of the novel environment elicited corrective muscle patterns that matched those expected in response to a perturbation opposite to the one originally experienced. This indicated that individuals who recalibrated their motor system adopted split-belts environment as their new “normal” and transitioning back to the original walking environment causes subjects to react as if it was novel to them. Interestingly, this learning declined with age, but steady state modulation of muscle activity during split-belts walking did not, suggesting potentially different neural mechanisms underlying these motor patterns. Taken together, our results show that corrective motor commands reflect the adapted state of the motor system, which is less flexible as we age.

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          Most cited references44

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          Efficient bipedal robots based on passive-dynamic walkers.

          Passive-dynamic walkers are simple mechanical devices, composed of solid parts connected by joints, that walk stably down a slope. They have no motors or controllers, yet can have remarkably humanlike motions. This suggests that these machines are useful models of human locomotion; however, they cannot walk on level ground. Here we present three robots based on passive-dynamics, with small active power sources substituted for gravity, which can walk on level ground. These robots use less control and less energy than other powered robots, yet walk more naturally, further suggesting the importance of passive-dynamics in human locomotion.
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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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              Muscle synergies characterizing human postural responses.

              Postural control is a natural behavior that requires the spatial and temporal coordination of multiple muscles. Complex muscle activation patterns characterizing postural responses suggest the need for independent muscle control. However, our previous work shows that postural responses in cats can be robustly reproduced by the activation of a few muscle synergies. We now investigate whether a similar neural strategy is used for human postural control. We hypothesized that a few muscle synergies could account for the intertrial variability in automatic postural responses from different perturbation directions, as well as different postural strategies. Postural responses to multidirectional support-surface translations in 16 muscles of the lower back and leg were analyzed in nine healthy subjects. Six or fewer muscle synergies were required to reproduce the postural responses of each subject. The composition and temporal activation of several muscle synergies identified across all subjects were consistent with the previously identified "ankle" and "hip" strategies in human postural responses. Moreover, intertrial variability in muscle activation patterns was successfully reproduced by modulating the activity of the various muscle synergies. This suggests that trial-to-trial variations in the activation of individual muscles are correlated and, moreover, represent variations in the amplitude of descending neural commands that activate individual muscle synergies. Finally, composition and temporal activation of most of the muscle synergies were similar across subjects. These results suggest that muscle synergies represent a general neural strategy underlying muscle coordination in postural tasks.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                15 April 2019
                30 April 2019
                Mar-Apr 2019
                : 6
                : 2
                : ENEURO.0358-18.2019
                Affiliations
                [1 ]Department of Bioengineering, Swanson School of Engineering, University of Pittsburgh , Pittsburgh, PA 15260
                [2 ]Center for the Neural Basis of Cognition, University of Pittsburgh , Pittsburgh, PA 15260
                Author notes

                The authors declare no competing financial interests.

                Author contributions: P.A.I. and G.T.-O. designed research; P.A.I. performed research; P.A.I. and G.T.-O. analyzed data; P.A.I. and G.T.-O. wrote the paper.

                This work was supported by the National Science Foundation (NSF) Broadening Participation Research Initiation Grants in Engineering Grant 1342183 and the NSF Grant 1535036.

                Correspondence should be addressed to Gelsy Torres-Oviedo at gelsyto@ 123456pitt.edu
                Author information
                http://orcid.org/0000-0001-6074-9070
                http://orcid.org/0000-0003-2415-1033
                Article
                eN-NWR-0358-18
                10.1523/ENEURO.0358-18.2019
                6497908
                31043463
                3f9b85e2-ef14-4956-9293-3537f2ecc984
                Copyright © 2019 Iturralde and Torres-Oviedo

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 5 September 2018
                : 5 March 2019
                : 22 March 2019
                Page count
                Figures: 5, Tables: 3, Equations: 89, References: 60, Pages: 15, Words: 12888
                Funding
                Funded by: http://doi.org/10.13039/100000001National Science Foundation (NSF)
                Award ID: BRIGE 1342183
                Award ID: 1535036
                Categories
                8
                8.1
                New Research
                Sensory and Motor Systems
                Custom metadata
                March/April 2019

                emg,locomotion,motor learning,split-belt walking
                emg, locomotion, motor learning, split-belt walking

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