A computational framework to study neural-structural interactions in human walking

Thesis (S.M.)--Massachusetts Institute of Technology, Dept. of Electrical Engineering and Computer Science, 2010.This electronic version was submitted by the student author. The certified thesis is available in the Institute Archives and Special Collections.Cataloged from student submitted PDF version of thesis.Includes bibliographical references (p. 91-94).Neuroscientists researching locomotion take a top-down approach by elucidating high- level cortical control circuits. In contrast, biomechanists prefer to focus on structural and mechanical aspects of the legged movement apparatus. We posit that studying interplay between neural co-ordination and legged biomechanics can yield crucial insight into (a) motor control and (b) human leg morphology. Physiological facts indicate that muscle actuator state (activation, length and velocity) is key to this neural-structural interplay. Here we present a novel model-based framework to resolve individual muscle state and describe neural-structural interactions in normal gait. We solve the inverse problem of using kinematic, kinetic and electro-myographic data recorded on healthy humans during level-ground,self-selected speed walking to estimate state of three major ankle muscles. Our approach comprises of two steps. First, we estimate neurally-controlled muscle activity from EMG data by building on statistical and mechanistic methods in the literature. Second, we perform a system ID on a mechanistic (Hill-type) model of the three muscles to nd tendon morpho- logical parameters governing evolution of muscle length and velocity. We implement the parameter identication as an optimization based on the hypothesis that neural control and lower limb morphology have co-evolved for optimal metabolic economy of natural walking.(cont.) We cross-validate our framework against independent datasets, and nd good model-empirical ankle torque agreement (R 2 = 0.96). The resulting muscle length and velocity predictions are consistent with in vivo ultra- sound scan measures. Further, model predictions reveal how leg structure and neural control come together to (a) dene roles of individual plantar exor muscles and (b) boost their joint performance. We nd that the Soleus operates as a steady ecient force source, while the Gastrocnemius functions as a burst mechanical power source. An analysis of the estimated states and optimized parameters reveals that the plantar exors operate jointly at a net mechanical eciency of 0.69 ±0.12. This is roughly three times higher than the maximal eciency of skeletal muscle performing positive work. Our results suggest that neural control may be tuned to exploit the elasticity of tendinous structures in the leg and achieve the high walking economy of humans.by Pavitra Krishnaswamy.S.M

USING MUSCULOSKELETAL MODELING TO ASSESS MUSCLE FUNCTION AND GAIT ASYMMETRY AFTER A STRAYER PROCEDURE APPLIED TO A CHILD WITH CEREBRAL PALSY

Cerebral palsy (CP) is a common group of neuromotor disorders with symptoms appearing during childhood. Children with CP often undergo orthopedic surgeries and treatment plans depending on the gait pattern and its severity. Jump gait is a gait pattern present in bilateral spastic CP and is characterized by a combination of ankle equinus, accentuated hip and knee flexion, lumbar lordosis, and anterior pelvis tilt. The modified Strayer procedure is a surgical intervention to treat equinus in ambulatory children with CP and is often accompanied by botulinum toxin type A (BTX) injections to aid in spasticity reduction. Musculoskeletal modeling is a promising approach to indirectly estimatemuscle function, includingmuscle force, andmuscle induced accelerations. Gait asymmetry is often studied as it is associated with pathological gait. This study aimed to analyze the improvements in gait function in one child with CP following corrective surgery for jump gait. Gait asymmetry, muscle forces and contributions to the center of mass accelerations during walking were assessed before, one and two years after surgery. Furthermore, comparison with typically developed children was also performed. Threedimensional marker coordinates and ground reaction forces (GRF) during walking were recorded and used as input for musculoskeletal simulations using OpenSim. Two years post-surgery, gait asymmetry reduced to levels similar to or lower than unimpaired gait. Overall joint kinematics improved, although the increase in dorsiflexion was not enough to achieve heel strike at first contact in the lower limb submitted to surgery. Estimates of muscle forces showed the child with CP relied more on proximal muscles to walk, mainly the vasti and hamstrings, before and after surgery. Soleus muscle forces increased following surgery, becoming the primary contributor to vertical support from the plantarflexors. Suggestions were made for treatment plans and for maintaining surgical improvements, such as strengthening of weakened muscles.Paralisia cerebral (PC) é um grupo de perturbações neuromotoras cujos sintomas aparecem durante a infância. Crianças com PC são regularmente submetidas a cirurgias ortopédicas e planos de tratamento de acordo com o padrão de marcha e grau de severidade. Marcha em salto é um padrão de marcha presente em PC espástica bilateral caracterizada por pé equino, flexão acentuada do joelho e anca, lordose lombar, e inclinação pélvica anterior. O procedimento modificado de Strayer é uma cirurgia comum para tratar pé equino em crianças com PC em contexto ambulatório e é normalmente acompanhada por injeções de toxina botulínica. Modelação musculoesquelética é uma abordagem que permite estimar, indiretamente, as forças e acelerações induzidas musculares. Assimetria na marcha é frequentemente estudada por estar associada a uma marcha patológica. O objetivo deste trabalho consiste em estudar as melhorias na marcha de uma criança com PC após cirurgia. Assimetria da marcha, forças e contribuições musculares para a aceleração do centro de massa foram avaliadas antes, um e dois anos após cirurgia. Além disso, foi feita a comparação com marcha saudável. Foram gravadas as coordenadas tridimensionais dos marcadores e forças de reação do solo para as simulações musculoesqueléticas através do OpenSim. Dois anos após cirurgia, a assimetria melhorou para níveis semelhantes ou inferiores aos da marcha saudável. Em termo gerais, a cinemática melhorou, porém, apesar da capacidade de dorsiflexão ter aumentado, o calcanhar não estabelece o primeiro contacto no membro inferior submetido a cirurgia. Resultados das forças musculares mostram uma maior dependência em músculos proximais na criança com PC, principalmente o vasto e os isquiotibiais, antes e após cirurgia. As forças musculares do solear aumentaram após cirurgia, tornando-se o principal plantarflexor a contribuir para o suporte. Fortalecimento de músculos enfraquecidos foi um dos planos de tratamento sugeridos para preservação das melhorias obtidas pela cirurgia

Stretch hyperreflexia in children with cerebral palsy:Assessment - Contextualization - Modulation

Cerebral palsy (CP) is a neurological disorder and the most frequent cause of motor impairment in children in Europe. Around 85% of children with CP experience stretch hyperreflexia, also known as “spasticity”. Stretch hyperreflexia is an excessive response to muscle stretch, leading to increased joint resistance. The joint hyper-resistance causes limitations in activities such as walking. Multiple methods have been developed to measure stretch hyperreflexia, but evidence supporting the use of these methods for diagnostics and treatment evaluation in children with CP is insufficient. Furthermore, most methods are designed to assess stretch reflexes in passive conditions, which might not translate to the limitations encountered due to stretch reflexes during activities. Furthermore, while a broad range of stretch hyperreflexia treatments is available, many are invasive, non-specific, or temporary and might have adverse side effects. Training methods to reduce stretch reflexes using biofeedback are promising non-invasive methods with potential long-term sustained effects. Still, clinical feasibility needs to be improved before implementation in clinical rehabilitation of children with CP. This thesis aimed to develop methods to assess stretch hyperreflexia of the calf muscles during passive conditions, as well as in the context of walking. Additionally, this thesis aimed to develop clinically feasible methods to modulate stretch hyperreflexia in the calf muscle of children with CP. The outcomes are described in eight different studies presented in this thesis. All in all, the work presented in this thesis shows that sagittal plane clinical gait analysis can be performed using the human body model and can be complemented with ultrasound imaging of the calf muscle. Motorized methods to assess stretch hyperreflexia in passive conditions might be useful for evaluation in adults after SCI/Stroke. Still, limitations regarding feasibility and validity limit clinical application for children with CP. Furthermore, this thesis provides additional evidence that the deviating muscle activation patterns during walking, particularly the increased activation around initial contact, are caused by stretch hyper-reflexes in children with CP. The deviating muscle activation patterns, with increased activation during early stance and reduced activation around push-off, can be modulated within one session by several children with CP. Therefore, the next step is to develop a training program to modulate the activation pattern and potentially decrease stretch hyper-reflexes in children with CP to improve the gait patter

Quantification of knee extensor muscle forces: a multimodality approach

Given the growing interest of using musculoskeletal (MSK) models in a large number of clinical applications for quantifying the internal loading of the human MSK system, verification and validation of the model’s predictions, especially at the knee joint, have remained as one of the biggest challenges in the use of the models as clinical tools. This thesis proposes a methodology for more accurate quantification of knee extensor forces by exploring different experimental and modelling techniques that can be used to enhance the process of verification and validation of the knee joint model within the MSK models for transforming the models to a viable clinical tool. In this methodology, an experimental protocol was developed for simultaneous measurement of the knee joint motion, torques, external forces and muscular activation during an isolated knee extension exercise. This experimental protocol was tested on a cohort of 11 male subjects and the measurements were used to quantify knee extensor forces using two different MSK models representing a simplified model of the knee extensor mechanism and a previously-developed three-dimensional MSK model of the lower limb. The quantified knee extensor forces from the MSK models were then compared to evaluate the performance of the models for quantifying knee extensor forces. The MSK models were also used to investigate the sensitivity of the calculated knee extensor forces to key modelling parameters of the knee including the method of quantifying the knee centre of rotation and the effect of joint translation during motion. In addition, the feasibility of an emerging ultrasound-based imaging technique (shear wave elastography) for direct quantification of the physiologically-relevant musculotendon forces was investigated. The results in this thesis showed that a simplified model of the knee can be reliably used during a controlled planar activity as a computationally-fast and effective tool for hierarchical verification of the knee joint model in optimisation-based large-scale MSK models to provide more confidence in the outputs of the models. Furthermore, the calculation of knee extensor muscle forces has been found to be sensitive to knee joint translation (moving centre of rotation of the knee), highlighting the importance of this modelling parameter for quantifying physiologically-realistic knee muscle forces in the MSK models. It was also demonstrated how the movement of the knee axis of rotation during motion can be used as an intuitive tool for understanding the functional anatomy of the knee joint. Moreover, the findings in this thesis indicated that the shear wave elastography technique can be potentially used as a novel method for direct quantification of the physiologically-relevant musculotendon forces for independent validation of the predictions of musculotendon forces from the MSK models.Open Acces

Automated and Standardized Tools for Realistic, Generic Musculoskeletal Model Development

Human movement is an instinctive yet challenging task that involves complex interactions between the neuromusculoskeletal system and its interaction with the surrounding environment. One key obstacle in the understanding of human locomotion is the availability and validity of experimental data or computational models. Corresponding measurements describing the relationships of the nervous and musculoskeletal systems and their dynamics are highly variable. Likewise, computational models and musculoskeletal models in particular are vitally dependent on these measurements to define model behavior and mechanics. These measurements are often sparse and disparate due to unsystematic data collection containing variable methodologies and reporting conventions. To date, there is not a framework to concatenate and manage musculoskeletal data (muscle moment arms and lengths). These morphological measurements need to be assembled to manage, compare, and analyze these data to develop comprehensive musculoskeletal models. Such a framework would enable researchers to select and update the posture-dependent relationships necessary to describe musculoskeletal dynamics, which are essential for simulation of muscle and joint torques in movement. Analogous to all simulations, these models require rigorous validation to ensure their accuracy. This is particularly important for musculoskeletal models that represent high-dimensional, posture-dependent relationships developed from limited and variable datasets. Here, I developed a computational workflow to collect and manage moment arm datasets from available published literature for the development of a human lower-limb musculoskeletal model. The moment arm relationships from multiple datasets were then used to create complete moment arm descriptions for all major leg muscles and were validated within a generic musculoskeletal model. These developments are crucial in advancing musculoskeletal modeling by providing standardized software and workflows for managing high-dimensional and posture-dependent morphological data to creating realistic and robust musculoskeletal models

On the role of stability in animal morphology and neural control

Mechanical stability is vital for the fitness and survival of animals and is a crucial aspect of robot design and control. Stability depends on multiple factors, including the body\u27s intrinsic mechanical response and feedback control. But feedback control is more fragile than the body\u27s innate mechanical response or open-loop control strategies because of sensory noise and time-delays in feedback. This thesis examines the overarching hypothesis that stability demands have played a crucial role in how animal form and function arise through natural selection and motor learning. In two examples, finger contact and overall body stability, we investigated the relationship between morphology, open-loop control, and stability. By studying the stability of the internal degrees of freedom of a finger when pushing on a hard surface, we find that stability limits the force that we can produce and is a dominant aspect of the neural control of the finger\u27s muscles. In our study on whole body lateral stability during locomotion in terrestrial animals, we find that the overall body aspect ratio has evolved to ensure passive lateral stability on the uneven terrain of natural environments. Precisely gripping an object with the fingertips is a hallmark of human hand dexterity. In Chapter 2, we show how human fingers are intrinsically prone to a buckling-type postural instability and how humans use careful neural orchestration of our muscles so that the elastic response of our muscles can suppress the intrinsic instability. In Chapter 3, we extend these findings further to examine the nature of neuromuscular variability and how the nervous system deals with the need for muscle-induced stability. We find that there is structure to neuromuscular variability so that most of the variability lies within the subspace that does not affect stability. Inspired by the open-loop stable control of our index fingers, in Chapter 4, we derive open-loop stability conditions for a general mechanical linkage with arbitrary joint torques subjected to holonomic constraints. The solution that we derive is physically realizable as cable-driven active mechanical linkages. With a user-prescribed cable layout, we pose the problem of actuating the system to maintain stability while subject to goals like energy minimization as a convex optimization problem. We are thus able to use efficient optimization methods available for convex problems and demonstrate numerical solutions in examples inspired by the finger. Chapter 5 presents a general formulation of the stability criteria for active mechanical linkages subject to Pfaffian holonomic and non-holonomic constraints. Active mechanical linkages subject to multiple constraints represent the mechanics of systems spanning many domains and length scales, such as limbs and digits in animals and robots, and elastic networks like actin meshes in microscopic systems. We show that a constrained mechanical linkage with regular stiffness and damping, and circulation-free feedback, can only destabilize by static buckling when subject to holonomic constraints. In contrast, the same mechanical linkage, subject to a non-holonomic constraint, such as a skate contact, can exhibit either static buckling or flutter instability. Chapter 6 moves away from neural control and studies the shape of animal bodies and their relationship to stability in locomotion. We investigate why small land animals tend to have a crouched or sprawled posture, whereas larger animals are generally more upright. We propose a new hypothesis that the scaling of body aspect ratio with size is driven by the scale-dependent unevenness of natural terrain. We show that the scaling law arising from the need for stability on rough natural terrain correctly predicts the frontal aspect ratio scaling law across 335 terrestrial vertebrates and invertebrates, spanning eight orders of magnitude in mass so that smaller animals have a wider aspect ratio. We also carry out statistical analyses that consider the phylogenetic relationship among the species in our dataset to show that the scaling is not due to gradual changes of the traits over time. Thus, stability demands on natural terrain may have driven the macroevolution of body aspect ratio across terrestrial animals. Interrogating unstable and marginally stable behaviors has helped us identify the morphological and control features that allow animals to perform robustly in noisy environments where perfect sensory feedback cannot be assumed. Although the thesis identifies the `what\u27 and `why,\u27 further studies are needed to understand `how\u27 mechanics and development intertwine to give rise to control and form in growing and adapting biological organisms