Learning to walk with a robotic ankle exoskeleton

We used a lower limb robotic exoskeleton controlled by the wearer's muscle activity to study human locomotor adaptation to disrupted muscular coordination. Ten healthy subjects walked while wearing a pneumatically powered ankle exoskeleton on one limb that effectively increased plantar flexor strength of the soleus muscle. Soleus electromyography amplitude controlled plantar flexion assistance from the exoskeleton in real time. We hypothesized that subjects' gait kinematics would be initially distorted by the added exoskeleton power, but that subjects would reduce soleus muscle recruitment with practice to return to gait kinematics more similar to normal. We also examined the ability of subjects to recall their adapted motor pattern for exoskeleton walking by testing subjects on two separate sessions, 3 days apart. The mechanical power added by the exoskeleton greatly perturbed ankle joint movements at first, causing subjects to walk with significantly increased plantar flexion during stance. With practice, subjects reduced soleus recruitment by approximately 35% and learned to use the exoskeleton to perform almost exclusively positive work about the ankle. Subjects demonstrated the ability to retain the adapted locomotor pattern between testing sessions as evidenced by similar muscle activity, kinematic and kinetic patterns between the end of the first test day and the beginning of the second. These results demonstrate that robotic exoskeletons controlled by muscle activity could be useful tools for testing neural mechanisms of human locomotor adaptation.     

Joint kinetic response during unexpectedly reduced plantar flexor torque provided by a robotic ankle exoskeleton during walking

During human walking, plantar flexor activation in late stance helps to generate a stable and economical gait pattern. Because plantar flexor activation is highly mediated by proprioceptive feedback, the nervous system must modulate reflex pathways to meet the mechanical requirements of gait. The purpose of this study was to quantify ankle joint mechanical output of the plantar flexor stretch reflex response during a novel unexpected gait perturbation. We used a robotic ankle exoskeleton to mechanically amplify the ankle torque output resulting from soleus muscle activation. We recorded lower-body kinematics, ground reaction forces, and electromyography during steady-state walking and during randomly perturbed steps when the exoskeleton assistance was unexpectedly turned off. We also measured soleus Hoffmann- (H-) reflexes at late stance during the two conditions. Subjects reacted to the unexpectedly decreased exoskeleton assistance by greatly increasing soleus muscle activity about 60 ms after ankle angle deviated from the control condition (p<0.001). There were large differences in ankle kinematic and electromyography patterns for the perturbed and control steps, but the total ankle moment was almost identical for the two conditions (p=0.13). The ratio of soleus H-reflex amplitude to background electromyography was not significantly different between the two conditions (p=0.4). This is the first study to show that the nervous system chooses reflex responses during human walking such that invariant ankle joint moment patterns are maintained during perturbations. Our findings are particularly useful for the development of neuromusculoskeletal computer simulations of human walking that need to adjust reflex gains appropriately for biomechanical analyses.     

Invariant ankle moment patterns when walking with and without a robotic ankle exoskeleton

To guide development of robotic lower limb exoskeletons, it is necessary to understand how humans adapt to powered assistance. The purposes of this study were to quantify joint moments while healthy subjects adapted to a robotic ankle exoskeleton and to determine if the period of motor adaptation is dependent on the magnitude of robotic assistance. The pneumatically powered ankle exoskeleton provided plantar flexor torque controlled by the wearer's soleus electromyography (EMG). Eleven naïve individuals completed two 30-min sessions walking on a split-belt instrumented treadmill at 1.25 m/s while wearing the ankle exoskeleton. After two sessions of practice, subjects reduced their soleus EMG activation by ～36% and walked with total ankle moment patterns similar to their unassisted gait (r²=0.98±0.02, THSD, p>0.05). They had substantially different ankle kinematic patterns compared to their unassisted gait (r²=0.79±0.12, THSD, p<0.05). Not all of the subjects reached a steady-state gait pattern within the two sessions, in contrast to a previous study using a weaker robotic ankle exoskeleton (Gordon and Ferris, 2007). Our results strongly suggest that humans aim for similar joint moment patterns when walking with robotic assistance rather than similar kinematic patterns. In addition, greater robotic assistance provided during initial use results in a longer adaptation process than lesser robotic assistance.     

Mechanical performance of artificial pneumatic muscles to power an ankle-foot orthosis

We developed a powered ankle-foot orthosis that uses artificial pneumatic muscles to produce active plantar flexor torque. The purpose of this study was to quantify the mechanical performance of the orthosis during human walking. Three subjects walked at a range of speeds wearing ankle-foot orthoses with either one or two artificial muscles working in parallel. The orthosis produced similar total peak plantar flexor torque and network across speeds independent of the number of muscles used. The orthosis generated approximately 57% of the peak ankle plantar flexor torque during stance and performed approximately 70% of the positive plantar flexor work done during normal walking. Artificial muscle bandwidth and force-length properties were the two primary factors limiting torque production. The lack of peak force and work differences between single and double muscle conditions can be explained by force-length properties. Subjects altered their ankle kinematics between conditions resulting in changes in artificial muscle length. In the double muscle condition greater plantar flexion yielded shorter artificial muscles lengths and decreased muscle forces. This finding emphasizes the importance of human testing in the design and development of robotic exoskeleton devices for assisting human movement. The results of this study outline the mechanical performance limitations of an ankle-foot orthosis powered by artificial pneumatic muscles. This orthosis could be valuable for gait rehabilitation and for studies investigating neuromechanical control of human walking.     

Invariant hip moment pattern while walking with a robotic hip exoskeleton

Robotic lower limb exoskeletons hold significant potential for gait assistance and rehabilitation; however, we have a limited understanding of how people adapt to walking with robotic devices. The purpose of this study was to test the hypothesis that people reduce net muscle moments about their joints when robotic assistance is provided. This reduction in muscle moment results in a total joint moment (muscle plus exoskeleton) that is the same as the moment without the robotic assistance despite potential differences in joint angles. To test this hypothesis, eight healthy subjects trained with the robotic hip exoskeleton while walking on a force-measuring treadmill. The exoskeleton provided hip flexion assistance from approximately 33% to 53% of the gait cycle. We calculated the root mean squared difference (RMSD) between the average of data from the last 15 min of the powered condition and the unpowered condition. After completing three 30-min training sessions, the hip exoskeleton provided 27% of the total peak hip flexion moment during gait. Despite this substantial contribution from the exoskeleton, subjects walked with a total hip moment pattern (muscle plus exoskeleton) that was almost identical and more similar to the unpowered condition than the hip angle pattern (hip moment RMSD 0.027, angle RMSD 0.134, p<0.001). The angle and moment RMSD were not different for the knee and ankle joints. These findings support the concept that people adopt walking patterns with similar joint moment patterns despite differences in hip joint angles for a given walking speed.     

Can altered muscle synergies control unimpaired gait?

Recent studies have postulated that the human motor control system recruits groups of muscles through low-dimensional motor commands, or muscle synergies. This scheme simplifies the neural control problem associated with the high-dimensional structure of the neuromuscular system. Several lines of evidence have suggested that neurological injuries, such as stroke or cerebral palsy, may reduce the dimensions that are available to the motor control system, and these altered dimensions or synergies are thought to contribute to impaired walking patterns. However, no study has investigated whether impaired low-dimensional control spaces necessarily lead to impaired walking patterns. In this study, using a two-dimensional model of walking, we developed a synergy-based control framework that can simulate the dynamics of walking. The simulation analysis showed that a synergy-based control scheme can produce well-coordinated movements of walking matching unimpaired gait. However, when the dimensions available to the controller were reduced, the simplified emergent pattern deviated from unimpaired gait. A system with two synergies, similar to those seen after neurological injury, could not produce an unimpaired walking pattern. These findings provide further evidence that altered muscle synergies can contribute to impaired gait patterns and may need to be directly addressed to improve gait after neurological injury.     

Patterns of muscle activity during different behaviors in chicks: implications for neural control

The large behavioral repertoire that spans the embryonic and postembryonic stages of development make chicks an ideal system for identifying patterns of muscle activity that are common to different behaviors and those that are behavior-specific. The main goal of this work was to identify the similar and dissimilar aspects of the recruitment patterns and the regulation of muscle activity during three distinct postembryonic behaviors: walking, swimming and airstepping. We identified two synergies that were common to each of these behaviors. The synergies were not disrupted by the absence of FT1 activity in airstepping. Within each synergy the recruitment time, recruitment order and duration of activity were not rigid, but varied according to the context-specific resistance that the leg encountered. Unlike the other muscles, FT2 activity was not recruited as part of the same synergy in each behavior. When weight-bearing contact with the substrate did not occur, as in swimming and airstepping, as well as in walking in chicks with deafferented legs, FT2 activity was not recruited as part of either synergy, but was recruited during the time between them. Although not identical, embryonic motility and hatching motor pattern both show the two synergies described for the postembryonic behaviors. Like the latter behaviors, the synergies tolerated the absence of activity from specific muscles. Thus, we suggest that the CNS produces different behaviors using many of the same muscles by organizing the patterned activity around two common synergies while permitting the different muscles that participate in a synergy to be modified in tandem or on an individual basis. Furthermore, the common synergies are established early during prenatal development in chicks.Abbreviations aIF anterior iliofibularius - CF caudilioflexorius - CNS central nervous system - EMG electromyogram - FT femorotibialis - GL gastrocnemius lateralis - P1 protraction 1 - P2 protraction 2 - pIF posterior iliofibularis - R retraction - SA sartorius - TA tibialis anterior - pIF posterior iliofibularis - ms millisecond     

Muscle demand and kinematic similarities between pediatric-modified motor-assisted elliptical training at fast speed and fast overground walking: Real-world implications for pediatric gait rehabilitation

The purpose of this research was to compare children’s lower extremity muscle activity and kinematics while walking at fast pace and training at fast speeds with and without motor-assistance on a pediatric-modified motor-assisted elliptical. Twenty-one children without disabilities were recruited and fifteen completed all three training conditions at self-selected fast pace. Repeated-measures ANOVAs identified muscle demand (peak, mean, duration) differences across device conditions and fast walking. Root mean square error compared overall kinematic profiles and statistical parametric mapping identified kinematic differences between conditions. Motor-assisted training reduced lower extremity muscle demands compared to training without the motor’s assistance (16 of 21 comparisons) and to fast walking (all but one comparison). Training without the motor’s assistance required less muscle effort than fast walking (16 of 21 comparisons). Kinematic differences between device conditions and fast walking were greater distally (thigh, knee, ankle) than proximally (trunk, pelvis, hip). In summary, transitioning from training with to without the motor’s assistance promoted progressively greater activity across the lower extremity muscles studied, with sagittal plane kinematic changes most apparent at the distal joints. Our findings highlight how motor-assistance can be manipulated to customize physiologic challenges to lower extremity muscles prior to fast overground walking.     

Changes in muscle coordination with training.

Three core concepts, activity-dependent coupling, the composition of muscle synergies, and Hebbian adaptation, are discussed with a view to illustrating the nature of the constraints imposed by the organization of the central nervous system on the changes in muscle coordination induced by training. It is argued that training invoked variations in the efficiency with which motor actions can be generated influence the stability of coordination by altering the potential for activity-dependent coupling between the cortical representations of the focal muscles recruited in a movement task and brain circuits that do not contribute directly to the required behavior. The behaviors that can be generated during training are also constrained by the composition of existing intrinsic muscle synergies. In circumstances in which attempts to produce forceful or high velocity movements would otherwise result in the generation of inappropriate actions, training designed to promote the development of control strategies specific to the desired movement outcome may be necessary to compensate for protogenic muscle recruitment patterns. Hebbian adaptation refers to processes whereby, for neurons that release action potentials at the same time, there is an increased probability that synaptic connections will be formed. Neural connectivity induced by the repetition of specific muscle recruitment patterns during training may, however, inhibit the subsequent acquisition of new skills. Consideration is given to the possibility that, in the presence of the appropriate sensory guidance, it is possible to gate Hebbian plasticity and to promote greater subsequent flexibility in the recruitment of the trained muscles in other task contexts.     

No evidence of expertise-related changes in muscle synergies during rowing

The purpose of the present study was to determine whether expertise in rowing is driven by a specific structure in muscular coordination. We compared seven experienced rowers and eight untrained (i.e., inexperienced) subjects during rowing on an ergometer. Both surface electromyography activity and mechanical patterns (forces exerted at the handle and the foot-stretcher) were recorded during a high intensity rowing exercise. A non-negative matrix factorization was applied to 23 electromyographic patterns to differentiate muscle synergies. Results showed that expertise was not associated with different dimensionality in the electromyographic data and that three muscle synergies were sufficient to explain the majority of the variance accounted for (i.e., >90% of the total variance) in the two populations. The synergies extracted were similar in the two populations, with identical functional roles. While the temporal organization of the propulsive synergies was very similar, slight differences were found in the composition of the muscle synergies (muscle synergy vectors) between the two populations. The results suggests that rowing expertise would not require the development of novel muscle synergies but would imply intrinsic synergies already used in different behaviors. Performance in rowing is more probably linked to adjustments in the mechanical output of the muscle synergies rather than to differences in the shape and timing of their activations.     

A noninvasive technique for in vivo measurement of joint torques of biarticular muscles.

The objective of this work was to develop a noninvasive method to measure the joint torques produced by biarticular muscles at two joints simultaneously. During intramuscular stimulation of the cat medial gastrocnemius (MG) muscle, torques at the ankle and knee joints were calculated from forces measured in two dimensions at the end point of the cat paw under isometric conditions. The method was verified by the known anatomical properties of cat MG muscle and the tibialis anterior (TA) muscle. The MG muscle was shown to produce a significant flexion torque at the knee, besides an extension torque at the ankle. This was in agreement with its anatomical arrangement. The TA muscle produced primarily an ankle flexion torque. The small knee torque, due to measurement errors, yielded an estimate of measurement accuracy of 3.0 +/- 2.1% (n = 52). The coupling ratio of the MG muscle, defined as T(ankle)/T(knee), varied significantly with both knee and ankle angles. The profile of MG mechanical coupling agreed qualitatively with changes in limb configuration. The method can be used to measure recruitment properties of electrically stimulated biarticular muscles, and may potentially be used to study the biomechanics of biarticular coupling.     

Muscle activation of patients suffering from asymmetric ankle osteoarthritis during isometric contractions and level walking – A time–frequency analysis

Asymmetric osteoarthritis (OA) is a common type of OA in the ankle joint. OA also influences the muscles surrounding a joint, however, little is known about the muscle activation in asymmetric ankle OA. Therefore, the aim of this study was to characterize the patients’ muscle activation during isometric ankle torque measurements and level walking. Surface electromyography (EMG) was measured of gastrocnemius medialis (GM) and lateralis (GL), soleus (SO), tibialis anterior (TA), and peroneus longus (PL) in 12 healthy subjects and 12 ankle OA patients. To obtain time and frequency components of the EMG power a wavelet transformation was performed. Furthermore, entropy was introduced to characterize the homogeneity of the wavelet patterns.Patients produced lower plantar- and dorsiflexion torques and their TA wavelet spectrum was shifted towards lower frequencies. While walking, the patients’ muscles were active with a lower intensity and over a broader time–frequency region. In contrast to controls and varus OA patients, maximal GM activity of valgus OA patients lagged behind the activity of GL and SO. In both tasks, PL of the valgus patients contained more low frequency power. The results of this study will help to assess whether surgical interventions of ankle OA can reestablish the muscle activation patterns.     

Pregnant women exaggerate cautious gait patterns during the transition between level and hill surfaces

Falls are the leading cause of nonfatal injury across all age groups and a common incident for pregnant women. Thus, there is a critical demand for research to evaluate if walking strategies in pregnant women change throughout pregnancy in order to effectively intervene and minimize the incidence rate. The aim of the present study was to analyze modifications in temporal–spatial parameters as well as muscle activity during hill walking transitions in pregnant women between gestational week 20 and 32. Based upon previous literature, we hypothesized that in comparison to level walking, the transition strides of pregnant women would be distinct between trimesters in order to accommodate the physical changes within twelve weeks. Thirteen pregnant women completed a series of randomly assigned walking conditions on level and hill surfaces during gestational week 20 and 32. Our results demonstrated that pregnant women modulated their gait patterns throughout pregnancy with additional joint flexion as well as muscle activity at the ankle, knee and hip. In summary, pregnant women exaggerate cautious gait patterns by walking slower and wider with greater joint flexion and muscle activity in order to safely transition between level and hill surfaces.     

Walking with increased ankle pushoff decreases hip muscle moments

In a simple bipedal walking model, an impulsive push along the trailing limb (similar to ankle plantar flexion) or a torque at the hip can power level walking. This suggests a tradeoff between ankle and hip muscle requirements during human gait. People with anterior hip pain may benefit from walking with increased ankle pushoff if it reduces hip muscle forces. The purpose of our study was to determine if simple instructions to alter ankle pushoff can modify gait dynamics and if resulting changes in ankle pushoff have an effect on hip muscle requirements during gait. We hypothesized that changes in ankle kinetics would be inversely related to hip muscle kinetics. Ten healthy subjects walked on a custom split-belt force-measuring treadmill at 1.25m/s. We recorded ground reaction forces and lower extremity kinematic data to calculate joint angles and internal muscle moments, powers and angular impulses. Subjects walked under three conditions: natural pushoff, decreased pushoff and increased pushoff. For the decreased pushoff condition, subjects were instructed to push less with their feet as they walked. Conversely, for the increased pushoff condition, subjects were instructed to push more with their feet. As predicted, walking with increased ankle pushoff resulted in lower peak hip flexion moment, power and angular impulse as well as lower peak hip extension moment and angular impulse (p<0.05). Our results emphasize the interchange between hip and ankle kinetics in human walking and suggest that increased ankle pushoff during gait may help to compensate for hip muscle weakness or injury and reduce hip joint forces.     

Muscle contributions to support and progression during single-limb stance in crouch gait

Pathological movement patterns like crouch gait are characterized by abnormal kinematics and muscle activations that alter how muscles support the body weight during walking. Individual muscles are often the target of interventions to improve crouch gait, yet the roles of individual muscles during crouch gait remain unknown. The goal of this study was to examine how muscles contribute to mass center accelerations and joint angular accelerations during single-limb stance in crouch gait, and compare these contributions to unimpaired gait. Subject-specific dynamic simulations were created for ten children who walked in a mild crouch gait and had no previous surgeries. The simulations were analyzed to determine the acceleration of the mass center and angular accelerations of the hip, knee, and ankle generated by individual muscles. The results of this analysis indicate that children walking in crouch gait have less passive skeletal support of body weight and utilize substantially higher muscle forces to walk than unimpaired individuals. Crouch gait relies on the same muscles as unimpaired gait to accelerate the mass center upward, including the soleus, vasti, gastrocnemius, gluteus medius, rectus femoris, and gluteus maximus. However, during crouch gait, these muscles are active throughout single-limb stance, in contrast to the modulation of muscle forces seen during single-limb stance in an unimpaired gait. Subjects walking in crouch gait rely more on proximal muscles, including the gluteus medius and hamstrings, to accelerate the mass center forward during single-limb stance than subjects with an unimpaired gait.     

Impact of ankle foot orthosis stiffness on Achilles tendon and gastrocnemius function during unimpaired gait

Ankle foot orthoses (AFOs) are designed to improve gait for individuals with neuromuscular conditions and have also been used to reduce energy costs of walking for unimpaired individuals. AFOs influence joint motion and metabolic cost, but how they impact muscle function remains unclear. This study investigated the impact of different stiffness AFOs on medial gastrocnemius muscle (MG) and Achilles tendon (AT) function during two walking speeds. We performed gait analyses for eight unimpaired individuals. Each individual walked at slow and very slow speeds with a 3D printed AFO with no resistance (free hinge condition) and four levels of ankle dorsiflexion stiffness: 0.25 Nm/°, 1 Nm/°, 2 Nm/°, and 3.7 Nm/°. Motion capture, ultrasound, and musculoskeletal modeling were used to quantify MG and AT lengths with each AFO condition. Increasing AFO stiffness increased peak AFO dorsiflexion moment with decreased peak knee extension and peak ankle dorsiflexion angles. Overall musculotendon length and peak AT length decreased, while peak MG length increased with increasing AFO stiffness. Peak MG activity, length, and velocity significantly decreased with slower walking speed. This study provides experimental evidence of the impact of AFO stiffness and walking speed on joint kinematics and musculotendon function. These methods can provide insight to improve AFO designs and optimize musculotendon function for rehabilitation, performance, or other goals.     

The neuromuscular demands of toe walking: a forward dynamics simulation analysis

Toe walking is a gait deviation with multiple etiologies and often associated with premature and prolonged ankle plantar flexor electromyographic activity. The goal of this study was to use a detailed musculoskeletal model and forward dynamical simulations that emulate able-bodied toe and heel-toe walking to understand why, despite an increase in muscle activity in the ankle plantar flexors during toe walking, the internal ankle joint moment decreases relative to heel-toe walking. The simulations were analyzed to assess the force generating capacity of the plantar flexors by examining each muscle's contractile state (i.e., the muscle fiber length, velocity and activation). Consistent with experimental measurements, the simulation data showed that despite a 122% increase in soleus muscle activity and a 76% increase in gastrocnemius activity, the peak internal ankle moment in late stance decreased. The decrease was attributed to non-optimal contractile conditions for the plantar flexors (primarily the force-length relationship) that reduced their ability to generate force. As a result, greater muscle activity is needed during toe walking to produce a given muscle force level. In addition, toe walking requires greater sustained plantar flexor force and moment generation during stance. Thus, even though toe walking requires lower peak plantar flexor forces that might suggest a compensatory advantage for those with plantar flexor weakness, greater neuromuscular demand is placed on those muscles. Therefore, medical decisions concerning whether to reduce equinus should consider not only the impact on the ankle moment, but also the expected change to the plantar flexor's force generating capacity.     

Muscle synergies underlying sit-to-stand tasks in elderly people and their relationship with kinetic characteristics

BackgroundPhysiological evidence suggests that the nervous system controls motion by using a low-dimensional synergy organization for muscle activation. Because the muscle activation produces joint torques, kinetic changes accompanying aging can be related to changes in muscle synergies.ObjectivesWe explored the effects of aging on muscle synergies underlying sit-to-stand tasks, and examined their relationships with kinetic characteristics.MethodsFour younger and three older adults performed the sit-to-stand task at two speeds. Subsequently, we extracted the muscle synergies used to perform these tasks. Hierarchical cluster analysis was used to classify these synergies. We also calculated kinetic variables to compare the groups.ResultsThree independent muscle synergies generally appeared in each subject. The spatial structure of these synergies was similar across age groups. The change in motion speed affected only the temporal structure of these synergies. However, subject-specific muscle synergies and kinetic variables existed.ConclusionsOur results suggest common muscle synergies underlying the sit-to-stand task in both young and elderly adults. People may actively change only the temporal structure of each muscle synergy. The precise subject-specific structuring of each muscle synergy may incorporate knowledge of the musculoskeletal kinetics.     

Neuromechanical adaptation to hopping with an elastic ankle-foot orthosis.

When humans hop or run on different surfaces, they adjust their effective leg stiffness to offset changes in surface stiffness. As a result, the overall stiffness of the leg-surface series combination remains independent of surface stiffness. The purpose of this study was to determine whether humans make a similar adjustment when springs are placed in parallel with the leg via a lower limb orthosis. We studied seven human subjects hopping in place on one leg while wearing an ankle-foot orthosis. We used an ankle-foot orthosis because the ankle joint is primarily responsible for leg stiffness during hopping. A spring was added to the ankle-foot orthosis so that it increased orthosis stiffness by providing plantar flexor torque during ankle dorsiflexion. We hypothesized that subjects would decrease their biological ankle stiffness when the spring was added to the orthosis, keeping total ankle stiffness constant. We collected kinematic, kinetic, and electromyographic data during hopping with and without the spring on the orthosis. We found that total ankle stiffness and leg stiffness did not change across the two orthosis conditions (ANOVA, P > 0.05). This was possible because subjects decreased their biological ankle stiffness to offset the orthosis spring stiffness (P < 0.0001). The reduction in biological ankle stiffness was accompanied by decreases in soleus, medial gastrocnemius, and lateral gastrocnemius muscle activation (P < 0.0002). These results suggest that an elastic exoskeleton might improve human running performance by reducing muscle recruitment.