Neuromuscular Mechanisms of Movement Variability: Implications for Rehabilitation and Augmentation

Although speed-accuracy trade-offs and planning and execution of rapid goaldirected movements have garnered significant research interest, far fewer studies have reported results on the lower end of the movement speed spectrum. Not only do very interesting observations exist that are unique to slow movements, but an explanation of these observations is highly relevant to motor function recovery and motor skill learning, where movements are typically slow at the initiation of therapy or learning, and movement speed increases through practice, exercise or therapy. In the first part of this thesis, based on data from nine stroke patients who underwent a month-long hybrid traditional and robotic therapy protocol, a correlation analysis shows that measures of movement quality based on minimum jerk theory for movement planning correlates significantly and strongly with clinical measures of motor impairment. In contrast, measures of movement speed lack statistical significance and show only weak to moderate correlations with clinical measures. These results constitute an important step towards establishing a much-needed bridge between clinical and robotic rehabilitation research communities. In the second part, the origins of movement intermittency or variability in slow movements are explored. A study with five healthy subjects who completed a manual circular tracking task shows that movement intermittency increases in distal direction along the arm during multi-joint movements. This result suggests that a neuromuscular noise option is favored against a submovement-based central planning alternative, as the source of variability in slow movements. An additional experimental study with eight healthy subjects who completed slow elbow flexion movements at a constant slow speed target under varying resistive torque levels demonstrates that resistive torques can significantly decrease movement speed variability. The relationship between resistive torque levels and speed variability, however, is not monotonic. This finding may constitute a basis for proper design of novel human skill augmentation methods for delicate tasks and improve motor rehabilitation and learning protocols. Finally, a neuro-musculoskeletal model of the elbow suggests that movement speed variability in slow movements cannot be solely attributed to variability in the mechanics of muscle force generation. Together, these analyses, simulations, and experiments shed light on variability in slow movements, and will inform the development of novel paradigms for robotic rehabilitation, motor skill learning and augmentation

Physical demand but not dexterity is associated with motor flexibility during rapid reaching in healthy young adults

Healthy humans are able to place light and heavy objects in small and large target locations with remarkable accuracy. Here we examine how dexterity demand and physical demand affect flexibility in joint coordination and end-effector kinematics when healthy young adults perform an upper extremity reaching task. We manipulated dexterity demand by changing target size and physical demand by increasing external resistance to reaching. Uncontrolled manifold analysis was used to decompose variability in joint coordination patterns into variability stabilizing the end-effector and variability de-stabilizing the end-effector during reaching. Our results demonstrate a proportional increase in stabilizing and de-stabilizing variability without a change in the ratio of the two variability components as physical demands increase. We interpret this finding in the context of previous studies showing that sensorimotor noise increases with increasing physical demands. We propose that the larger de-stabilizing variability as a function of physical demand originated from larger sensorimotor noise in the neuromuscular system. The larger stabilizing variability with larger physical demands is a strategy employed by the neuromuscular system to counter the de-stabilizing variability so that performance stability is maintained. Our findings have practical implications for improving the effectiveness of movement therapy in a wide range of patient groups, maintaining upper extremity function in old adults, and for maximizing athletic performance

Task-Dependent Properties of the Human Anconeus Muscle

Recording motor unit (MU) action potentials during fast muscle contractions, specifically during movement, presents unique challenges that constrain the investigation of the upper limits of human MU performance. The anconeus muscle exhibits many advantageous characteristics that suggest it is an appealing model for the study of MU behaviour in challenging experiment paradigms. Thus, the purpose was to determine the MU recruitment and discharge properties associated with the generation of movement up to maximal angular velocities of elbow extension and to determine the effect of submaximal fatiguing movements on these MU properties. Due to the synergistic nature of the anconeus in the elbow extensor muscle group, a secondary purpose was to determine whether MUs of the muscles comprising the elbow extensor group behave differently during the production of high forces. Discharge rates and recruitment thresholds were tracked in 24 and 17 MUs, respectively. It was revealed that anconeus MUs increase discharge rates over two distinct linear ranges possessing different input-output gain relationships relative to elbow extension velocity. Anconeus MUs exhibited variable responses to increased resultant velocity when recruitment thresholds were considered. These variable responses, that were more common in higher threshold MUs, indicated that a compression of the MU recruitment range of the anconeus occurred as elbow extension velocity increased. Using the same recording techniques, fatigue-related changes in discharge rates and recruitment thresholds of 12 MUs were determined throughout a protocol comprised of fast, maximal, static muscle contractions, and submaximal and periodic maximal movements. Results of this study demonstrated that MU properties are graded differently in response to submaximal fatiguing movements depending on the intensity of the movement, but that contraction type did not affect the relative changes in these MU properties. Lastly, MUs in three elbow extensors including the anconeus were tracked during constant joint angle force production to near maximal intensities. Differences between the elbow extensors were observed for MU discharge rates and recruitment thresholds with increasing force. These findings support an integrated model of earlier established MU control strategies for the elbow extensors and show anconeus MU recruitment occurs over a greater range than previously believed

New control strategies for neuroprosthetic systems

The availability of techniques to artificially excite paralyzed muscles opens enormous potential for restoring both upper and lower extremity movements with\ud neuroprostheses. Neuroprostheses must stimulate muscle, and control and regulate the artificial movements produced. Control methods to accomplish these tasks include feedforward (open-loop), feedback, and adaptive control. Feedforward control requires a great deal of information about the biomechanical behavior of the limb. For the upper extremity, an artificial motor program was developed to provide such movement program input to a neuroprosthesis. In lower extremity control, one group achieved their best results by attempting to meet naturally perceived gait objectives rather than to follow an exact joint angle trajectory. Adaptive feedforward control, as implemented in the cycleto-cycle controller, gave good compensation for the gradual decrease in performance observed with open-loop control. A neural network controller was able to control its system to customize stimulation parameters in order to generate a desired output trajectory in a given individual and to maintain tracking performance in the presence of muscle fatigue. The authors believe that practical FNS control systems must\ud exhibit many of these features of neurophysiological systems

Modeling of equilibrium point trajectory control in human arm movements

The underlying concept of the Equilibrium Point Hypothesis (EPH) is that the CNS provides a virtual trajectory of joint motion, representing spacing and timing, with actual movement dynamics being produced by interactions of limb inertia, muscle viscosity and speed/position feedback from muscle spindles. To counter criticisms of the EPH, investigators have proposed the use of complex virtual trajectories, non-linear damping, stiffness and time varying stiffness to the EPH model. While these features allow the EPH to adequately produce human joint velocities, they conflict with the EPH’s premise of simple pre-planned monotonic control of movement trajectory. As a result, this study proposed an EPH based method, which provides a simpler mechanism in motor control without conflict with the core advantages of the original approach. This work has proposed relative damping as an addition to the EPH model to predict the single and two joint arm movements. This addition results in simulated data that not only closely match experimental angle data, but also match the experimental joint torques. In addition, it is suggested that this modified model can be used to predict the multi-joint angular trajectories with fast and normal velocities, without the need for time varying or non-linear stiffness and damping, but with simple monotonic virtual trajectories. In the following study, this relative damping model has been further enhanced with an EMG-based determination of the virtual trajectory and with physiologically realistic neuromuscular delays. The results of unobstructed voluntary movement studies suggest that the EPH models use realistic impedance values and produce desired joint trajectories and joint torques in unperturbed voluntary arm movement. A subsequent study of obstructed voluntary arm movement extended the relative damping concept, and incorporated the influential factors of the mechanical behavior of the neural, muscular and skeletal system in the control and coordination of arm posture and movement. A significant problem of the study is how this information should be used to modify control signals to achieve desired performance. This study used an EPH model to examine changes of controlling signals for arm movements in the context of adding perturbation/load in the form of forces/torques. The mechanical properties and reflex actions of muscles of the elbow joint were examined. Brief unexpected torque/force pulses of identical magnitude and time duration were introduced at different stages of the movement in a random order by a pre-programmed 3 degree of freedom (DOF) robotic arm (MOOG FCS HapticMaster). The results show that the subjects may maintain the same control parameters (virtual trajectory, stiffness and damping) regardless of added perturbations that cause substantial changes in EMG activity and kinematics

The Aging Neuromuscular System and Motor Performance

Age-related changes in the basic functional unit of the neuromuscular system, the motor unit, and its neural inputs have a profound effect on motor function, especially among the expanding number of old (older than ∼60 yr) and very old (older than ∼80 yr) adults. This review presents evidence that age-related changes in motor unit morphology and properties lead to impaired motor performance that includes 1) reduced maximal strength and power, slower contractile velocity, and increased fatigability; and 2) increased variability during and between motor tasks, including decreased force steadiness and increased variability of contraction velocity and torque over repeat contractions. The age-related increase in variability of motor performance with aging appears to involve reduced and more variable synaptic inputs that drive motor neuron activation, fewer and larger motor units, less stable neuromuscular junctions, lower and more variable motor unit action potential discharge rates, and smaller and slower skeletal muscle fibers that coexpress different myosin heavy chain isoforms in the muscle of older adults. Physical activity may modify motor unit properties and function in old men and women, although the effects on variability of motor performance are largely unknown. Many studies are of cross-sectional design, so there is a tremendous opportunity to perform high-impact and longitudinal studies along the continuum of aging that determine 1) the influence and cause of the increased variability with aging on functional performance tasks, and 2) whether lifestyle factors such as physical exercise can minimize this age-related variability in motor performance in the rapidly expanding numbers of very old adults

Rate Modulation of the Human Anconeus Muscle During High-Intensity Dynamic Fatigue of the Elbow Extensor Muscle Group

PURPOSE: To evaluate anconeus motor unit firing rate (MUFR) as a function of time to task failure (TTF) during maximal velocity elbow extensions at a moderately heavy load. METHODS: Two fine-wire intramuscular electrode pairs were inserted into the anconeus to record MUFR in twelve male participants (25±3y). Individual MUs were tracked throughout a three-stage dynamic elbow extension fatigue protocol. Mean MUFR were calculated for the following time ranges: 0-15%, 45-60%, and 85-100% TTF. RESULTS: Following the fatigue task, with a mean TTF of 83s, peak power decreased 64% compared to baseline. Data from 20 anconeus MUs showed changes in MUFR from ~36 Hz (0-15% TTF) to ~28 Hz (45-60% TTF) to ~23 Hz (85-100% TTF). CONCLUSION: During high-intensity maximal velocity dynamic contractions, anconeus firing rates decreased substantially. The relative decrease in MUFR after this task is in accordance with that reported for sustained high-intensity isometric tasks in other muscles

Muscle Coordination Contributes to Function after Stroke; Proprioception Contributes to Control of Posture, Movement

More than half of stroke survivors experience persistent upper extremity motor impairments that can negatively impact quality of life and independence. Effective use of the upper extremity requires coordination of agonist/antagonist muscle pairs, as well as coordination of multiple control actions for stabilizing and moving the arm. In this dissertation, I present three studies in which I recorded isometric torque production, single joint movement and stabilization, and clinical measures of function and impairments after stroke to evaluate the extent to which changes in coordination of agonist/antagonist muscles and of sequential control actions contribute to deficits after stroke. In Aim 1, I quantified the extent to which stroke-related deficits in the coordination of agonist/antagonist muscle pairs degraded the ability to generate, maintain, and relax cued torques about the elbow. Participants who survived stroke (SP) and neurologically intact participants (NI) performed pursuit tracking of step-changes in isomeric torque targets to investigate coordination of activation magnitude in elbow agonist/antagonist muscle pairs. SP had marked hypertonia of the primary flexor muscles, which led to increased compensatory activity in the primary extensor muscles. These stroke-related deficits of muscle coordination degraded ability to generate, maintain, and relax cued torque production. In Aim 2, SP and NI performed sequential combinations of elbow stabilization and movements to investigate impairments in execution and coordination of these fundamental control actions. Impaired proprioception in SP was associated with increased impairments in stabilizing the arm against a perturbation compared with SP with intact proprioception. Surprisingly, SP with intact proprioception had greater impairments when moving than did SP with impaired proprioception. These results support the supposition that deficits of somatosensation can differentially impact neural control of limb stabilization and movement. Aim 3 used correlation and forward regression to compare deficits of muscle coordination (Aim 1) and control (Aim 2) to one another in order to quantify the extent to which each could explain deficits of motor function after stroke. Taken together, the three studies revealed that stroke-related deficits in coordination timing and magnitude of muscle activation impact clinically-measured function, and that somatosensory deficits can differentially impair neuromotor stabilization and movement control

Dynamic primitives of motor behavior

We present in outline a theory of sensorimotor control based on dynamic primitives, which we define as attractors. To account for the broad class of human interactive behaviors—especially tool use—we propose three distinct primitives: submovements, oscillations, and mechanical impedances, the latter necessary for interaction with objects. Owing to the fundamental features of the neuromuscular system—most notably, its slow response—we argue that encoding in terms of parameterized primitives may be an essential simplification required for learning, performance, and retention of complex skills. Primitives may simultaneously and sequentially be combined to produce observable forces and motions. This may be achieved by defining a virtual trajectory composed of submovements and/or oscillations interacting with impedances. Identifying primitives requires care: in principle, overlapping submovements would be sufficient to compose all observed movements but biological evidence shows that oscillations are a distinct primitive. Conversely, we suggest that kinematic synergies, frequently discussed as primitives of complex actions, may be an emergent consequence of neuromuscular impedance. To illustrate how these dynamic primitives may account for complex actions, we brieflyreviewthree typesof interactivebehaviors: constrained motion, impact tasks, and manipulation of dynamic objects.United States. National Institutes of Health (T32GM008334)American Heart Association (11SDG7270001)National Science Foundation (U.S.) (NSF DMS-0928587