Control Of Human Locomotion Research Articles

Recent Updates on Investigation of Neural Control of Human Locomotion by Non-invasive Neural Recording Techniques

本稿では，脳波や筋電図など非侵襲神経機能計測を使用したヒト二足歩行の神経制御に関する研究の近況について概説する．歩行の神経制御研究は1800年代から脈々と続いている長い歴史を持つ研究分野であり，従来はネコなどの四足動物を対象とした脳の部分破壊術を用いた研究が主流であった．しかしながら，近年の計測技術・解析技術のめざましい進歩により，ヒトにおいても対象とできる神経領域が拡大してきている．四足動物では四肢の左右・屈筋伸筋の交代性活動の生成を司る脊髄や脳幹による制御が中心であり定常歩行時では大脳皮質の関与は少ない．一方，二足直立歩行を行うヒトでは定常歩行時でさえ大脳皮質が顕著に活動する．このような違いを考慮すると，ヒト二足直立歩行の神経制御機序の理解のためには，実際にヒトが歩行中の神経活動を計測することが重要である．高密度脳波や高密度筋電図を使用した健常者・神経疾患患者の歩行実験により，ヒト二足歩行制御における大脳皮質から脳深部，脊髄の役割が徐々に明らかになりつつある．本稿ではそのようなヒト二足歩行制御の神経制御に関する近年の研究についてまとめる．

Changes in Key Biomechanical Parameters According to the Expertise Level in Runners at Different Running Speeds

Running has become increasingly popular worldwide. Among runners, there exists a wide range of expertise levels. Investigating the differences between runners at two extreme levels, that is novices and experts, is crucial to understand the changes that occur as a result of multiple years of training. Vertical oscillation of center of mass (CoM), stride frequency normalized to the leg length, and duty factor, which describes the step time relative to the flight time, are key biomechanical parameters that have been shown to be closely related to the running economy and are used to characterize the running style. The variability characteristics of these parameters may reveal valuable information concerning the control of human locomotion. However, how the expertise level and running speed affect the variability of these key biomechanical parameters has not yet been investigated. The aim of this study was to analyze the effects of expertise level (novice vs. expert) and running speed (10 km/h vs. 15 km/h) on these parameters and their variability. It was hypothesized that expert runners would have lower vertical oscillation of CoM, normalized stride frequency, and duty factor and show less variability in these parameters. The parameters' variability was operationalized by the coefficient of variation. The mean values and variability of these key biomechanical parameters according to expertise level and running speed were compared with rmANOVAs. The results showed that the experts had a lower duty factor and less variable vertical oscillation of CoM and normalized stride frequency, independently of the running speed. At a higher running speed, the variability of vertical oscillation of CoM was higher, whereas that of normalized stride frequency and duty factor did not change significantly. To the best of our knowledge, this is the first study analyzing the effects of expertise level and running speed on the variability of key biomechanical parameters.

Modelling and analysis of orthoses generated whole-body vertical vibrations impact on limb stability and compliant dynamics in a ramp gait

Whole-body vibrations provide important proprioceptive feedback for the control of human locomotion. However, these vibrations are also reported to have a detrimental effect on several existing musculoskeletal disorders. Studies have to date reported on the limits of these centre-of-mass (CoM) vibrations mainly for the level walk. However, their impact remains unquantified for other walking situations such as ramp ascent and descent (A/D). Orthotic devices have also been reported as improving limb mobility, but their contribution to whole-body vertical dynamics has not yet been investigated in ramp walking studies. This study presents methods for evaluating normal limits of CoM-vibrations on a ramp, with and without the effect of an ankle–foot orthosis (AFO). Experiments are performed on a force plate and CoM-vibrations data is recorded as a function of impact forces for both normal and AFO walking conditions. These CoM-vibrations are then modelled using a regression technique and analysed in the frequency domain. The normal limits of CoM-vibrations are quantified as limb compliance properties and stability margins for both A/D. A comparison between normal and AFO walking conditions identified significant variations (Friedman-test, p < 0.05) in lower limb compliance dynamics and stability margins. Results also showed the significant impact of AFO adjustments on musculoskeletal dynamics. This preliminary study defines the normal limits of impact forces and their efficiency associated with the wearing of an AFO. Clinically, these outcomes are important in evaluating the deleterious effects of impact forces in patients and on the effectiveness of measures taken to overcome impact forces using assistive devices.

Manual stabilization reveals a transient role for balance control during locomotor adaptation.

A fundamental feature of human locomotor control is the need to adapt walking patterns in response to changes in the environment. For example, when people walk on a split-belt treadmill, which has belts that move at different speeds, they adapt to the asymmetric speed constraints by reducing spatiotemporal asymmetry. Here, we aim to understand the role of balance control as a potential factor driving this adaptation process. We recruited 24 healthy, young adults to adapt to walking on a split-belt treadmill while either holding on to a handrail or walking with free arm swing. We measured whole body angular momentum and step length asymmetry as measures of dynamic balance and spatiotemporal asymmetry, respectively. To understand how changes in intersegmental coordination influenced whole body angular momentum, we also measured segmental angular momenta and the coefficient of cancellation. When participants were initially exposed to the asymmetry in belt speeds, we observed an increase in whole body angular momentum that was due to both an increase in the momentum of individual segments and a reduction in the coefficient of cancellation. Holding on to a handrail reduced the perturbation to asymmetry during the early phase of adaptation and resulted in a smaller aftereffect during early postadaptation. In addition, the stabilization provided by holding on to a handrail led to reductions in the coupling between angular momentum and asymmetry. These results suggest that regulation of dynamic balance is most important during the initial, transient phase of adaptation to walking on a split-belt treadmill.NEW & NOTEWORTHY We investigated the role of dynamic balance during adaptation to a split-belt treadmill by measuring whole body angular momentum with or without holding on to a handrail. The initial step length asymmetry and associations between balance and asymmetry reduced when holding on to a handrail during early adaptation. These findings indicate that dynamic balance mostly contributes to the initial phase of adaptation when people are exposed to an asymmetric walking constraint.

Bioinspired Legged Robot Design via Blended Physical and Virtual Impedance Control

In order to approach the performance of biological locomotion in legged robots, better integration between body design and control is required. In that respect, understanding the mechanics and control of human locomotion will help us build legged robots with comparable efficient performance. From another perspective, developing bioinspired robots can also improve our understanding of human locomotion. In this work, we create a bioinspired robot with a blended physical and virtual impedance control to configure the robot’s mechatronic setup. We consider human neural control and musculoskeletal system a blueprint for a hopping robot. The hybrid electric-pneumatic actuator (EPA) presents an artificial copy of this biological system to implement the blended control. By defining efficacy as a metric that encompasses both performance and efficiency, we demonstrate that incorporating a simple force-based control besides constant pressure pneumatic artificial muscles (PAM) alone can increase the efficiency up to 21% in simulations and 7% in experiments with the 2-segmented EPA-hopper robot. Also, we show that with proper adjustment of the force-based controller and the PAMs, efficacy can be further increased to 41%. Finally, experimental results with the 3-segmented EPA-hopper robot and comparisons with human hopping confirm the extendability of the proposed methods to more complex robots.

Comparison of Spatiotemporal Parameters between Athletes and Non-Athletes at Upslope Running

Upslope locomotion is challenging in our day to day life for which neuromuscular system have to work extraordinarily [1]. Despite increasing popularity of trail running, trekking, hiking that include various slope inclination, the majority of running biomechanics studies have only considered level running [2]. To understand the control of human locomotion better, physiological and biomechanical variables related to incremental slopes running during the gait cycle is imperative. Several studies have examined upslope running but the results are inconclusive [2-6]. Running at higher upslope inclination showed higher step frequency [2] and reduced stride length [6]. Conversely some studies examining various parameters did not observe any difference between level and uphill running at constant speed [4,7]. Previous studies comparing spatiotemporal characteristics in varying level of trained runners [5,8-10] indicated longer flight time and better adaptation in elite runners compared to amateur runners with increased inclination [5]. Conversely, a study showed no difference in adaptation of spatiotemporal characteristics between amateur and highly trained athletes while running upslope at given speed [2]. This leaves questions whether non-athletes adapt to different slopes gradient in the same way as trained athletes. We aimed to determine the effect of different slope gradients on spatiotemporal gait parameters between athletes and non-athletes during running on an instrumented treadmill.

Mobile Electroencephalography for Studying Neural Control of Human Locomotion.

Walking or running in real-world environments requires dynamic multisensory processing within the brain. Studying supraspinal neural pathways during human locomotion provides opportunities to better understand complex neural circuity that may become compromised due to aging, neurological disorder, or disease. Knowledge gained from studies examining human electrical brain dynamics during gait can also lay foundations for developing locomotor neurotechnologies for rehabilitation or human performance. Technical barriers have largely prohibited neuroimaging during gait, but the portability and precise temporal resolution of non-invasive electroencephalography (EEG) have expanded human neuromotor research into increasingly dynamic tasks. In this narrative mini-review, we provide a (1) brief introduction and overview of modern neuroimaging technologies and then identify considerations for (2) mobile EEG hardware, (3) and data processing, (4) including technical challenges and possible solutions. Finally, we summarize (5) knowledge gained from human locomotor control studies that have used mobile EEG, and (6) discuss future directions for real-world neuroimaging research.

Moving forward: methodological considerations for assessing corticospinal excitability during rhythmic motor output in humans.

The use of transcranial magnetic stimulation to assess the excitability of the central nervous system to further understand the neural control of human movement is expansive. The majority of the work performed to-date has assessed corticospinal excitability either at rest or during relatively simple isometric contractions. The results from this work are not easily extrapolated to rhythmic, dynamic motor outputs, given that corticospinal excitability is task-, phase-, intensity-, direction-, and muscle-dependent (Power KE, Lockyer EJ, Forman DA, Button DC. Appl Physiol Nutr Metab 43: 1176-1185, 2018). Assessing corticospinal excitability during rhythmic motor output, however, involves technical challenges that are to be overcome, or at the minimum considered, when attempting to design experiments and interpret the physiological relevance of the results. The purpose of this narrative review is to highlight the research examining corticospinal excitability during a rhythmic motor output and, importantly, to provide recommendations regarding the many factors that must be considered when designing and interpreting findings from studies that involve limb movement. To do so, the majority of work described herein refers to work performed using arm cycling (arm pedaling or arm cranking) as a model of a rhythmic motor output used to examine the neural control of human locomotion.

Functional MRI Reveals Locomotion-Control Neural Circuits in Human Brainstem.

The cuneiform nucleus (CN) and the pedunculopontine nucleus (PPN) in the midbrain control coordinated locomotion in vertebrates, but whether similar mechanisms exist in humans remain to be elucidated. Using functional magnetic resonance imaging, we found that simulated gait evoked activations in the CN, PPN, and other brainstem regions in humans. Brain networks were constructed for each condition using functional connectivity. Bilateral CN–PPN and the four pons–medulla regions constituted two separate modules under all motor conditions, presenting two brainstem functional units for locomotion control. Outside- and inside-brainstem nodes were connected more densely although the links between the two groups were sparse. Functional connectivity and network analysis revealed the role of brainstem circuits in dual-task walking and walking automaticity. Together, our findings indicate that the CN, PPN, and other brainstem regions participate in locomotion control in humans.

A model for the transfer of control from the brain to the spinal cord through synaptic learning.

The spinal cord is essential to the control of locomotion in legged animals and humans. However, the actual circuitry of the spinal controller remains only vaguely understood. Here we approach this problem from the viewpoint of learning. More precisely, we assume the circuitry evolves through the transfer of control from the brain to the spinal cord, propose a specific learning mechanism for this transfer based on the error between the cord and brain contributions to muscle control, and study the resulting structure of the spinal controller in a simplified neuromuscular model of human locomotion. The model focuses on the leg rebound behavior in stance and represents the spinal circuitry with 150 muscle reflexes. We find that after learning a spinal controller has evolved that produces leg rebound motions in the absence of a central brain input with only three structural reflex groups. These groups contain individual reflexes well known from physiological experiments but thought to serve separate purposes in the control of human locomotion. Our results suggest a more holistic interpretation of the role of individual sensory projections in spinal networks than is common. In addition, we discuss potential neural correlates for the proposed learning mechanism that may be probed in experiments. Together with such experiments, neuromuscular models of spinal learning likely will become effective tools for uncovering the structure and development of the spinal control circuitry.

Corticospinal Control of Human Locomotion as a New Determinant of Age-Related Sarcopenia: An Exploratory Study

Sarcopenia is a muscle disease listed within the ICD-10 classification. Several operational definitions have been created for sarcopenia screening; however, an international consensus is lacking. The Centers for Disease Control and Prevention have recently recognized that sarcopenia detection requires improved diagnosis and screening measures. Mounting evidence hints towards changes in the corticospinal communication system where corticomuscular coherence (CMC) reflects an effective mechanism of corticospinal interaction. CMC can be assessed during locomotion by means of simultaneously measuring Electroencephalography (EEG) and Electromyography (EMG). The aim of this study was to perform sarcopenia screening in community-dwelling older adults and explore the possibility of using CMC assessed during gait to discriminate between sarcopenic and non-sarcopenic older adults. Receiver Operating Characteristic (ROC) curves showed high sensitivity, precision and accuracy of CMC assessed from EEG Cz sensor and EMG sensors located over Musculus Vastus Medialis [Cz-VM; AUC (95.0%CI): 0.98 (0.92–1.04), sensitivity: 1.00, 1-specificity: 0.89, p < 0.001] and with Musculus Biceps Femoris [Cz-BF; AUC (95.0%CI): 0.86 (0.68–1.03), sensitivity: 1.00, 1-specificity: 0.70, p < 0.001]. These muscles showed significant differences with large magnitude of effect between sarcopenic and non-sarcopenic older adults [Hedge’s g (95.0%CI): 2.2 (1.3–3.1), p = 0.005 and Hedge’s g (95.0%CI): 1.5 (0.7–2.2), p = 0.010; respectively]. The novelty of this exploratory investigation is the hint toward a novel possible determinant of age-related sarcopenia, derived from corticospinal control of locomotion and shown by the observed large differences in CMC when sarcopenic and non-sarcopenic older adults are compared. This, in turn, might represent in future a potential treatment target to counteract sarcopenia as well as a parameter to monitor the progression of the disease and/or the potential recovery following other treatment interventions.

The Benefit of Combining Neuronal Feedback and Feed-Forward Control for Robustness in Step Down Perturbations of Simulated Human Walking Depends on the Muscle Function.

It is often assumed that the spinal control of human locomotion combines feed-forward central pattern generation with sensory feedback via muscle reflexes. However, the actual contribution of each component to the generation and stabilization of gait is not well understood, as direct experimental evidence for either is difficult to obtain. We here investigate the relative contribution of the two components to gait stability in a simulation model of human walking. Specifically, we hypothesize that a simple linear combination of feedback and feed-forward control at the level of the spinal cord improves the reaction to unexpected step down perturbations. In previous work, we found preliminary evidence supporting this hypothesis when studying a very reduced model of rebounding behaviors. In the present work, we investigate if the evidence extends to a more realistic model of human walking. We revisit a model that has previously been published and relies on spinal feedback control to generate walking. We extend the control of this model with a feed-forward muscle activation pattern. The feed-forward pattern is recorded from the unperturbed feedback control output. We find that the improvement in the robustness of the walking model with respect to step down perturbations depends on the ratio between the two strategies and on the muscle to which they are applied. The results suggest that combining feed-forward and feedback control is not guaranteed to improve locomotion, as the beneficial effects are dependent on the muscle and its function during walking.

Evidence of a "Clock" Determining Human Locomotion.

The motor control of human locomotion is still an open issue, and it may be the leading cause of the low effectiveness of lower limbs rehabilitation therapies. Locomotion motor control has proved to be fundamentally different from the upper limbs reaching task strategies, which have been used for the development of current motor control computational models used to define rehabilitation protocols. The main difference between these two tasks is the relevance of the environmental dynamics in task planning and execution. Reaching movements are dominated by the intrinsic impedance of the human body. On the other hand, locomotion is determined by the interaction between the human body and Earth's gravity. The dynamic primitives have been recently proposed to explain how humans account for the environmental dynamics during motor control; however, it is not yet possible to explain how the nervous system combines the information. This paper proposes and validates with human data that the brain controls locomotion to have the centre of mass moving between the two legs as a harmonic oscillator. This finding has enabled us to propose a control architecture that can explain how the motor primitives can be described as a special type of dynamics primitives.

Motor module activation sequence and topography in the spinal cord during air‐stepping in human: Insights into the traveling wave in spinal locomotor circuits

Coordinated locomotor muscle activity is generated by the spinal central pattern generators (CPGs), which are modulated by peripheral and supraspinal inputs. The CPGs would consist of multiple motor modules generating basic muscle activity, which are distributed rostrocaudally along the spinal cord. To activate the motor modules in proper sequence, rostrocaudally traveling waves of activation in the spinal cord are important mechanisms in the CPGs. The traveling waves of activation have been observed in nonhuman vertebrates. However, they have not yet been confirmed during human locomotion. Although, rostrocaudal wave‐like activations in the spinal cord were observed during walking in humans in a previous study, the propagation shifted rostrally toward the upper lumbar segments at foot contact. Here, using an air stepping task to remove the foot‐contact interactions, we examined whether the traveling wave mechanism exists in the human spinal circuits based on the activation sequence of motor modules and their topography. We measured electromyographic activity of lower leg muscles during the air‐stepping task. Then, we extracted motor modules (i.e., basic patterns of sets of muscle activations: muscle synergies) from the measured muscle activities using nonnegative matrix factorization method. Next, we reconstructed motoneuron (MN) activity from each module activity based on myotomal charts. We identified four types of motor modules from muscle activities during the air‐stepping task. Each motor module represented different sets of synergistic muscle activations. MN clusters innervating each motor module were sequentially activated from the rostral to caudal region in the spinal cord, from the initial flexion to the last extension phase during air‐stepping. The rostrocaudally sequential activation of MN clusters suggests the possibility that rostrocaudally traveling waves exist in human locomotor spinal circuits. The present results advance the understanding of human locomotor control mechanisms, and provide important insights into the evolution of locomotor networks in vertebrates.

Evaluation of a Neuromechanical Walking Control Model Using Disturbance Experiments.

Neuromechanical simulations have been used to study the spinal control of human locomotion which involves complex mechanical dynamics. So far, most neuromechanical simulation studies have focused on demonstrating the capability of a proposed control model in generating normal walking. As many of these models with competing control hypotheses can generate human-like normal walking behaviors, a more in-depth evaluation is required. Here, we conduct the more in-depth evaluation on a spinal-reflex-based control model using five representative gait disturbances, ranging from electrical stimulation to mechanical perturbation at individual leg joints and at the whole body. The immediate changes in muscle activations of the model are compared to those of humans across different gait phases and disturbance magnitudes. Remarkably similar response trends for the majority of investigated muscles and experimental conditions reinforce the plausibility of the reflex circuits of the model. However, the model's responses lack in amplitude for two experiments with whole body disturbances suggesting that in these cases the proposed reflex circuits need to be amplified by additional control structures such as location-specific cutaneous reflexes. A model that captures these selective amplifications would be able to explain both steady and reactive spinal control of human locomotion. Neuromechanical simulations that investigate hypothesized control models are complementary to gait experiments in better understanding the control of human locomotion.

Modular neuromuscular control of human locomotion by central pattern generator

The central pattern generators (CPG) in the spinal cord are thought to be responsible for producing the rhythmic motor patterns during rhythmic activities. For locomotor tasks, this involves much complexity, due to a redundant system of muscle actuators with a large number of highly nonlinear muscles. This study proposes a reduced neural control strategy for the CPG, based on modular organization of the co-active muscles, i.e., muscle synergies. Four synergies were extracted from the EMG data of the major leg muscles of two subjects, during two gait trials each, using non-negative matrix factorization algorithm. A Matsuoka׳s four-neuron CPG model with mutual inhibition, was utilized to generate the rhythmic activation patterns of the muscle synergies, using the hip flexion angle and foot contact force information from the sensory afferents as inputs. The model parameters were tuned using the experimental data of one gait trial, which resulted in a good fitting accuracy (RMSEs between 0.0491 and 0.1399) between the simulation and experimental synergy activations. The model׳s performance was then assessed by comparing its predictions for the activation patterns of the individual leg muscles during locomotion with the relevant EMG data. Results indicated that the characteristic features of the complex activation patterns of the muscles were well reproduced by the model for different gait trials and subjects. In general, the CPG- and muscle synergy-based model was promising in view of its simple architecture, yet extensive potentials for neuromuscular control, e.g., resolving redundancies, distributed and fast control, and modulation of locomotion by simple control signals.

Neural Control of Walking in People with Parkinsonism.

People with Parkinson's disease exhibit debilitating gait impairments, including gait slowness, increased step variability, and poor postural control. A widespread supraspinal locomotor network including the cortex, cerebellum, basal ganglia, and brain stem contributes to the control of human locomotion, and altered activity of these structures underlies gait dysfunction due to Parkinson's disease.

Muscle Spindles and Locomotor Control-An Unrecognized Falls Determinant?

BACKGROUND: Historically, evidence muscle spindles might be involved in locomotion was provided by their presence in tetrapod antigravity muscles associated with posture and locomotion. Later, Brodal (1962) noted muscle spindles in all muscles of locomotion. To unravel the complexity of the muscle spindle and its role in human locomotor control many investigators have since conducted lesion and/or anaesthesia studies in subhuman species and human contexts. QUESTIONS: How strong is the evidence linking muscle spindles to normal human locomotion and its control? Can a case be made for an association between muscle spindle dysfunction and falls injuries? METHODS: All relevant publications in the leading electronic databases were searched using the key terms muscle afferents, falls, gait, locomotion, muscle spindles. There were numerous related listings, but here only selected reports are examined and discussed because the articles had to be linked in some way to the key question driving the research. RESULTS: Evidence supports a key role for muscle spindles in the control of human locomotion, and by analogy to falls related injuries. CONCLUSION: Future work to explore the role of muscle spindles in the context of falls that occur when walking is warranted.

A neural circuitry that emphasizes spinal feedback generates diverse behaviours of human locomotion

It is often assumed that central pattern generators, which generate rhythmic patterns without rhythmic inputs, play a key role in the spinal control of human locomotion. We propose a neural control model in which the spinal control generates muscle stimulations mainly through integrated reflex pathways with no central pattern generator. Using a physics-based neuromuscular human model, we show that this control network is sufficient to compose steady and transitional 3-D locomotion behaviours, including walking and running, acceleration and deceleration, slope and stair negotiation, turning, and deliberate obstacle avoidance. The results suggest feedback integration to be functionally more important than central pattern generation in human locomotion across behaviours. In addition, the proposed control architecture may serve as a guide in the search for the neurophysiological origin and circuitry of spinal control in humans. Neural networks along the spinal cord contribute substantially to generating locomotion behaviours in humans and other legged animals. However, the neural circuitry involved in this spinal control remains unclear. We here propose a specific circuitry that emphasizes feedback integration over central pattern generation. The circuitry is based on neurophysiologically plausible muscle-reflex pathways that are organized in 10 spinal modules realizing limb functions essential to legged systems in stance and swing. These modules are combined with a supraspinal control layer that adjusts the desired foot placements and selects the leg that is to transition into swing control during double support. Using physics-based simulation, we test the proposed circuitry in a neuromuscular human model that includes neural transmission delays, musculotendon dynamics and compliant foot-ground contacts. We find that the control network is sufficient to compose steady and transitional 3-D locomotion behaviours including walking and running, acceleration and deceleration, slope and stair negotiation, turning, and deliberate obstacle avoidance. The results suggest feedback integration to be functionally more important than central pattern generation in human locomotion across behaviours. In addition, the proposed control architecture may serve as a guide in the search for the neurophysiological origin and circuitry of spinal control in humans.

ヒトの適応的な歩行を生み出す低次元構造と感覚－運動協調：運動学・筋シナジーと位相リセットの機能と応用

ヒトの適応的な歩行を生み出す低次元構造と感覚－運動協調：運動学・筋シナジーと位相リセットの機能と応用