Stabilization of human standing posture using functional neuromuscular stimulation

Functional neuromuscular stimulation (FNS)/functional electrical stimulation (FES) is a potential way to restore some functionality to the limbs of patients with spinal cord injury through direct/indirect stimulation of the motoneuron. One of the constraints for wider use of FNS on paraplegic patients is the lack of efficient control algorithm. Most of the published works on FNS/FES control are based on oversimplified models of human body dynamics. An innovative control strategy for stabilizing the standing posture of paraplegic patients is proposed here which is a combination of a proportional-plus-derivative controller for motions of the skeletal system and a control action prediction mechanism to produce musculotendon activation. The goal is to produce musculotendon torque which can approximate those demanded by the controller for the skeletal system. In computer simulations, using a detailed skeletal–musculotendon–muscle activation dynamics model of human body, this FNS/FES control approach can stabilize a paraplegic patient's standing posture with the minimum number of musculotendon groups. Also, it is found that this control strategy can maintain stability even in the presence of reasonable variations in the controller's musculotendon parameters.     

Variability of the fatigue response of paralyzed skeletal muscle in relation to the time after spinal cord injury: mechanical and electrophysiological characteristics

The aim of this study was to determine the effect of the time after spinal cord injury (less than and greater than 10 months) on the mechanical and electrophysiological characteristics of muscle fatigue of the paralyzed electrically stimulated quadriceps muscle. Morphologically and histochemically, a relationship was observed between muscle fatigue and the delay from injury, revealing a critical period of enzymatic turning and a maximum peak of atrophy around the 10th month after the injury, followed by a long-term stabilization. Knee-torque output and M-wave variables (amplitude, latency, duration, and root mean square, RMS) of two muscular heads of the quadriceps were recorded in 19 paraplegic patients during a 120-s isometric contraction. The fatiguing muscle contraction was elicited by supramaximal continuous 20-Hz electrical stimulation. Compared to the chronic group, the acutely paralyzed group showed a greater resistance to fatigue (amount and rate of force decline, P < or = 0.01), smaller alterations of the M-wave amplitude and RMS, and a limited decrease of the muscle fiber conduction velocity (P < 0.05). Mechanical and electrophysiological changes during fatigue provided a clear functional support of the transformation of skeletal muscle under the lesion and of the existence of a critical period of muscular turn. In conclusion, when considering the artificial restoration of motor function, the evolution of the endurance and force-generating capabilities of the muscle actuator must be taken into account, particularly when tasks require important safety conditions (e.g., standing and walking).     

Assessment of Neuromuscular Function Using Percutaneous Electrical Nerve Stimulation

Percutaneous electrical nerve stimulation is a non-invasive method commonly used to evaluate neuromuscular function from brain to muscle (supra-spinal, spinal and peripheral levels). The present protocol describes how this method can be used to stimulate the posterior tibial nerve that activates plantar flexor muscles. Percutaneous electrical nerve stimulation consists of inducing an electrical stimulus to a motor nerve to evoke a muscular response. Direct (M-wave) and/or indirect (H-reflex) electrophysiological responses can be recorded at rest using surface electromyography. Mechanical (twitch torque) responses can be quantified with a force/torque ergometer. M-wave and twitch torque reflect neuromuscular transmission and excitation-contraction coupling, whereas H-reflex provides an index of spinal excitability. EMG activity and mechanical (superimposed twitch) responses can also be recorded during maximal voluntary contractions to evaluate voluntary activation level. Percutaneous nerve stimulation provides an assessment of neuromuscular function in humans, and is highly beneficial especially for studies evaluating neuromuscular plasticity following acute (fatigue) or chronic (training/detraining) exercise.     

A myocybernetic control model of skeletal muscle

A mathematical model of skeletal muscle is presented which contains the two physiological control parameters stimulation rate and motor unit recruitment. The model is complete in the sense that it adequately describes all possible contractive states normally occurring in living muscle. The modelling procedure relies entirely on established myo-physiological facts and each assumption made is substantiated by experimental data. Extensive simulation studies reveal that the model is capable of correctly predicting practically all known phenomena of the muscular force-output. A simplified version of the model is also presented, particularly suitable for inclusion as the driving structure in complex musculoskeletal link systems. This version was successfully tested in the prediction of an optimal human motion. The present control model is believed to fill a gap in the literature on models of muscle, and may be expected to provide a sound basis for research into the optimal control aspects of muscular contraction, and to stimulate such research.     

Effects of stimulation frequency versus pulse duration modulation on muscle fatigue.

During functional electrical stimulation (FES), both the frequency and intensity can be increased to increase muscle force output and counteract the effects of muscle fatigue. Most current FES systems, however, deliver a constant frequency and only vary the stimulation intensity to control muscle force. This study compared muscle performance and fatigue produced during repetitive electrical stimulation using three different strategies: (1) constant pulse-duration and stepwise increases in frequency (frequency-modulation); (2) constant frequency and stepwise increases in pulse-duration (pulse-duration-modulation); and (3) constant frequency and pulse-duration (no-modulation). Surface electrical stimulation was delivered to the quadriceps femoris muscles of 12 healthy individuals and isometric forces were recorded. Muscle performance was assessed by measuring the percent changes in the peak forces and force-time integrals between the first and the last fatiguing trains. Muscle fatigue was assessed by measuring percent declines in peak force between the 60Hz pre- and post-fatigue testing trains. The results showed that frequency-modulation showed better performance for both peak forces and force-time integrals in response to the fatiguing trains than pulse-duration-modulation, while producing similar levels of muscle fatigue. Although frequency-modulation is not commonly used during FES, clinicians should consider this strategy to improve muscle performance.     

Failure of neuromuscular propagation during human maximal voluntary contraction

The mechanism for fatigue of the adductor pollicis was studied in normal subjects during maximal voluntary contractions (MVC) sustained for 90-100 s, by comparing the force and electrical response of this muscle to voluntary motor drive with that obtainable with artificial stimulation of the ulnar nerve. The adequacy of nerve stimulation was checked by recording simultaneously the electrical response of a nonfatiguing muscle, the abductor of the small finger. The decrease in force and in the natural electrical activity with fatigue was accompanied by a parallel decrease in the amplitude of synchronous muscle action potentials (M waves) evoked by artificial stimulation of the ulnar nerve at different frequencies. The decline in M-wave amplitude in the adductor pollicis was not due to a submaximal nerve stimulation, since the amplitudes recorded simultaneously from the nonfatiguing abductor digiti minimi remained unchanged. The force and the electrical responses from the adductor pollicis recovered in parallel with a half time of approximately 1 min. These results suggest that the loss of force of the adductor pollicis with fatigue and its subsequent recovery are largely determined by the extent of neuromuscular propagation failure. The slow recovery of the M-wave amplitude during repetitive stimulation suggests that it may be related to some aspect of muscle metabolism.     

Control of functional electrical stimulation with extended physiological proprioception

The use of functional electrical stimulation (FES) of muscle for paraplegic locomotion, or grasp augmentation in tetraplegia, is limited by the variability in muscle response to stimulation as a result of several external and internal factors. Previous approaches to this problem have used position-servo controllers, which have been shown to function satisfactorily in the laboratory. However, such systems will fail should obstacles be encountered or should the stimulation hardware develop a fault. To prevent such potentially dangerous failures some form of sensory feedback is required. This paper describes the first application of a technique known as extended physiological proprioception (EPP) to the control of FES to compensate for muscle response variability and provide proprioceptive feedback via the appropriate sensory pathways. In the experimental system described, a paraplegic subject controlled the extension of his paralysed knee by shoulder protraction. A Bowden cable linked the two joints, and a dynamometer in this cable was used to derive the control signal for a computer-controlled stimulator which delivered surface stimulation to the quadriceps muscle group. Modelling and parameter identification were performed by analysis of the step response, and the controller was designed from consideration of the root locus. The advantages of the system, in terms of improved proprioceptive feedback and reduced limb-positioning error were assessed in a test of joint positioning accuracy with vision occluded. The EPP system showed improvements over both open and closed-loop position-servo controllers.     

A predictive model of fatigue in human skeletal muscles.

Fatigue is a major limitation to the clinical application of functional electrical stimulation. The activation pattern used during electrical stimulation affects force and fatigue. Identifying the activation pattern that produces the greatest force and least fatigue for each patient is, therefore, of great importance. Mathematical models that predict muscle forces and fatigue produced by a wide range of stimulation patterns would facilitate the search for optimal patterns. Previously, we developed a mathematical isometric force model that successfully identified the stimulation patterns that produced the greatest forces from healthy subjects under nonfatigue and fatigue conditions. The present study introduces a four-parameter fatigue model, coupled with the force model that predicts the fatigue induced by different stimulation patterns on different days during isometric contractions. This fatigue model accounted for 90% of the variability in forces produced by different fatigue tests. The predicted forces at the end of fatigue testing differed from those observed by only 9%. This model demonstrates the potential for predicting muscle fatigue in response to a wide range of stimulation patterns.     

A comparison of central aspects of fatigue in submaximal and maximal voluntary contractions.

Magnetic and electrical stimulation at different levels of the neuraxis show that supraspinal and spinal factors limit force production in maximal isometric efforts ("central fatigue"). In sustained maximal contractions, motoneurons become less responsive to synaptic input and descending drive becomes suboptimal. Exercise-induced activity in group III and IV muscle afferents acts supraspinally to limit motor cortical output but does not alter motor cortical responses to transcranial magnetic stimulation. "Central" and "peripheral" fatigue develop more slowly during submaximal exercise. In sustained submaximal contractions, central fatigue occurs in brief maximal efforts even with a weak ongoing contraction (<15% maximum). The presence of central fatigue when much of the available motor pathway is not engaged suggests that afferent inputs contribute to reduce voluntary activation. Small-diameter muscle afferents are likely to be activated by local activity even in sustained weak contractions. During such contractions, it is difficult to measure central fatigue, which is best demonstrated in maximal efforts. To show central fatigue in submaximal contractions, changes in motor unit firing and force output need to be characterized simultaneously. Increasing central drive recruits new motor units, but the way this occurs is likely to depend on properties of the motoneurons and the inputs they receive in the task. It is unclear whether such factors impair force production for a set level of descending drive and thus represent central fatigue. The best indication that central fatigue is important during submaximal tasks is the disproportionate increase in subjects' perceived effort when maintaining a low target force.     

Fatigue compensation during FES using surface EMG

Muscle fatigue limits the effectiveness of FES when applied to regain functional movements in spinal cord injured (SCI) individuals. The stimulation intensity must be manually increased to provide more force output to compensate for the decreasing muscle force due to fatigue. An artificial neural network (ANN) system was designed to compensate for muscle fatigue during functional electrical stimulation (FES) by maintaining a constant joint angle. Surface electromyography signals (EMG) from electrically stimulated muscles were used to determine when to increase the stimulation intensity when the muscle’s output started to drop.

In two separate experiments on able-bodied subjects seated in hard back chairs, electrical stimulation was continuously applied to fatigue either the biceps (during elbow flexion) or the quadriceps muscle (during leg extension) while recording the surface EMG. An ANN system was created using processed surface EMG as the input, and a discrete fatigue compensation control signal, indicating when to increase the stimulation current, as the output. In order to provide training examples and test the systems’ performance, the stimulation current amplitude was manually increased to maintain constant joint angles. Manual stimulation amplitude increases were required upon observing a significant decrease in the joint angle. The goal of the ANN system was to generate fatigue compensation control signals in an attempt to maintain a constant joint angle.

On average, the systems could correctly predict 78.5% of the instances at which a stimulation increase was required to maintain the joint angle. The performance of these ANN systems demonstrates the feasibility of using surface EMG feedback in an FES control system.     

Transcutaneous FES of the paralyzed quadriceps: is knee torque affected by unintended activation of the hamstrings?

This study addresses the question whether unintended response of the knee flexors (hamstrings) accompanies transcutaneous functional electrical stimulation (FES) of the quadriceps and whether the knee torque is hereby affected. Transcutaneous FES of the right quadriceps of two paraplegic subjects was applied and measurements were made of the net torque and of the myoelectric activities of the quadriceps and hamstrings muscles of the right leg. A low correlation was obtained between the peak-to-peak amplitudes of the M-waves of the two muscles. This correlation decreased further with the development of fatigue, which indicated that the electromyography (EMG) signals from the hamstrings were not the result of cross-talk between adjacent recording sites. The force profile of each muscle was determined from a developed model incorporating EMG-based activation, muscle anthropometry as obtained from in vivo magnetic resonance imaging of the thigh, and metabolic fatigue function, based on data acquired by 31P nuclear magnetic resonance spectroscopy. A sensitivity analysis revealed that the muscle specific tension and the muscle moment arms have a major influence on the resulting muscle forces and should therefore be accurately provided. The results show that during the unfatigued phase of contraction the estimated maximal force in the hamstrings was lower than 20% of that in the quadriceps and could be considered to be practically negligible. As fatigue progressed the hamstrings-to-quadriceps force ratio increased, reaching up to 45%, and the effect of co-activation on the torque partition between the two muscles was no longer negligible.     

Symmetry of FES responses in the lower extremities of paraplegic patients

Due to natural or artificial obstacles, gait is a less automatic and periodic process than it would appear when studying normal walking on the level. Pre-programmed functional electrical stimulation (FES) sequences, therefore, do not appear to be a suitable approach to the control of multichannel electrical stimulators in the restoration of paraplegic walking. Walking in paraplegic subjects must be, to a large extent, under voluntary control. To lessen the burden of this control, the symmetry of walking can be taken into account. Symmetric motion of the legs requires symmetric FES actuation. Symmetry of FES responses was studied in a group of 10 paraplegic subjects who had all undergone the FES training program. Recruitment curve, fatigue index and twitch delay were assessed. An average 80% symmetry was found in all parameters measured, thus allowing a reduction of complexity of control approach for FES locomotor aids.     

A Brain-Machine-Muscle Interface for Restoring Hindlimb Locomotion after Complete Spinal Transection in Rats

A brain-machine interface (BMI) is a neuroprosthetic device that can restore motor function of individuals with paralysis. Although the feasibility of BMI control of upper-limb neuroprostheses has been demonstrated, a BMI for the restoration of lower-limb motor functions has not yet been developed. The objective of this study was to determine if gait-related information can be captured from neural activity recorded from the primary motor cortex of rats, and if this neural information can be used to stimulate paralysed hindlimb muscles after complete spinal cord transection. Neural activity was recorded from the hindlimb area of the primary motor cortex of six female Sprague Dawley rats during treadmill locomotion before and after mid-thoracic transection. Before spinal transection there was a strong association between neural activity and the step cycle. This association decreased after spinal transection. However, the locomotive state (standing vs. walking) could still be successfully decoded from neural recordings made after spinal transection. A novel BMI device was developed that processed this neural information in real-time and used it to control electrical stimulation of paralysed hindlimb muscles. This system was able to elicit hindlimb muscle contractions that mimicked forelimb stepping. We propose this lower-limb BMI as a future neuroprosthesis for human paraplegics.     

A musculoskeletal model of the upper extremity for use in the development of neuroprosthetic systems

Upper extremity neuroprostheses use functional electrical stimulation (FES) to restore arm motor function to individuals with cervical level spinal cord injury. For the design and testing of these systems, a biomechanical model of the shoulder and elbow has been developed, to be used as a substitute for the human arm. It can be used to design and evaluate specific implementations of FES systems, as well as FES controllers. The model can be customized to simulate a variety of pathological conditions. For example, by adjusting the maximum force the muscles can produce, the model can be used to simulate an individual with tetraplegia and to explore the effects of FES of different muscle sets. The model comprises six bones, five joints, nine degrees of freedom, and 29 shoulder and arm muscles. It was developed using commercial, graphics-based modeling and simulation packages that are easily accessible to other researchers and can be readily interfaced to other analysis packages. It can be used for both forward-dynamic (inputs: muscle activation and external load; outputs: motions) and inverse-dynamic (inputs: motions and external load; outputs: muscle activation) simulations. Our model was verified by comparing the model calculated muscle activations to electromyographic signals recorded from shoulder and arm muscles of five subjects. As an example of its application to neuroprosthesis design, the model was used to demonstrate the importance of rotator cuff muscle stimulation when aiming to restore humeral elevation. It is concluded that this model is a useful tool in the development and implementation of upper extremity neuroprosthetic systems.     

Feedback-controlled stimulation enhances human paralyzed muscle performance.

Chronically paralyzed muscle requires extensive training before it can deliver a therapeutic dose of repetitive stress to the musculoskeletal system. Neuromuscular electrical stimulation, under feedback control, may subvert the effects of fatigue, yielding more rapid and extensive adaptations to training. The purposes of this investigation were to 1) compare the effectiveness of torque feedback-controlled (FDBCK) electrical stimulation with classic open-loop constant-frequency (CONST) stimulation, and 2) ascertain which of three stimulation strategies best maintains soleus torque during repetitive stimulation. When torque declined by 10%, the FDBCK protocol modulated the base stimulation frequency in three ways: by a fixed increase, by a paired pulse (doublet) at the beginning of the stimulation train, and by a fixed decrease. The stimulation strategy that most effectively restored torque continued for successive contractions. This process repeated each time torque declined by 10%. In fresh muscle, FDBCK stimulation offered minimal advantage in maintaining peak torque or mean torque over CONST stimulation. As long-duration fatigue developed in subsequent bouts, FDBCK stimulation became most effective ( approximately 40% higher final normalized torque than CONST). The high-frequency strategy was selected approximately 90% of the time, supporting that excitation-contraction coupling compromise and not neuromuscular transmission failure contributed to fatigue of paralyzed muscle. Ideal stimulation strategies may vary according to the site of fatigue; this stimulation approach offered the advantage of online modulation of stimulation strategies in response to fatigue conditions. Based on stress-adaptation principles, FDBCK-controlled stimulation may enhance training effects in chronically paralyzed muscle.     

Effect of selective fatiguing of the shank muscles on single-leg-standing sway.

Control of standing requires the continuous activity of the leg muscles. In single leg standing the system is less redundant and muscular activity is more intensive. The objective of this study was to examine the effect of force imbalance of the shank muscles, evoked by their selective fatiguing, on postural control in single-leg standing. Five healthy subjects performed two single-leg standing trials, lasting as long as the subject could maintain steady balance, and separated by a 240s quasi-isotonic sustained effort to induce fatigue of the Tibialis Anterior and Peroneus muscles. The following were on-line monitored: sway-related parameters, e.g., ground reaction force and center of pressure in the standing trials; and electromyogram of the Tibialis Anterior, Peroneus and Gastrocnemius muscles in all experiments. Simple and multiple linear regressions served to study the fatigue effects on the relationship between muscle activity and postural sway. The results indicate that the evoked muscle imbalance leads to (a) increased postural sway; (b) increased correlation between muscle activity, and sway-related parameters. Thus, with the reduction of the level of redundancy the system becomes more synchronized. These results have potential relevance for cases of muscle impairment, in which electrical stimulation is required to augment muscle activity.     

Interaction against different environmental dynamics during a leg extension task is controlled by temporal rather than amplitude scaling of muscular activity

Force exertion against different mechanical environments can affect motor control strategies in order to account for the altered environmental dynamics and to maintain the ability to produce force. Here, we investigated the change of muscular activity of selected muscles of the lower extremities while the participants interacted with an external mechanical device of variable stability. Twenty-five healthy participants exerted force against the device by performing a unilateral ballistic leg extension task under 1 or 3 degrees of freedom (DoF). Directional force data and electromyographic responses from four leg muscles (TA, VM, GM, PL) were recorded. Muscle responses to the altered experimental conditions were analyzed by calculating time to peak electrical activity (TTP), peak electrical activity (PEA), slope of EMG-signal and muscle activity. It was found that neuromuscular system adjustments to the task are expressed mainly by temporal (TTP) rather than amplitude (PEA) scaling of muscular activity. This change was specific for the investigated muscles. Moreover, a selective increase of muscle activity occurred while increasing external DoF. This scheme was accompanied by a significant reduction of applicable force against the device in the unstable 3 DoF condition. The findings suggest that orchestration of movement control is linked to environmental dynamics also affecting the ability to produce force under dynamic conditions. The adjustments of the neuromuscular system are rather temporal in nature being consistent with the impulse timing hypothesis of motor control.     

Alterations in corticospinal excitability with imposed vs. voluntary fatigue in human hand muscles.

We aimed to determine whether postexercise depression of motor-evoked potentials (MEPs) could be demonstrated without voluntary muscle activation in humans. Voluntary fatigue was induced with a 2-min maximal voluntary contraction (MVC) of the first dorsal interosseous (FDI) muscle. On another occasion, "electrical fatigue" was induced with trains of shocks delivered for 2 min over the FDI motor point. Five of the twelve subjects also underwent "sequential fatigue" consisting of a 2-min MVC of FDI followed by 20 min of rest and then 2 min of motor point stimulation. Voluntary fatigue induced MEP depression that persisted for at least 20 min. Electrical fatigue induced a transient MEP facilitation that subsided 20 min after the stimulation and became depressed within 30 min. Thus MEP depression can be induced by both voluntary and electrical fatigue. With electrical fatigue, the initial depression is "masked" by transient MEP facilitation, reflecting cortical plasticity induced by the prolonged electrical stimulation. MEP depression probably reflects tonic afferent input from the exercising muscle that alters cortical excitability without altering spinal excitability.     

Biochemical correlates of fatigue. A brief review

Muscle fatigue, defined as a decreased force generating capacity, develops gradually during exercise and is distinct from exhaustion, which occurs when the required force or exercise intensity can no longer be maintained. We have reviewed several biochemical and ionic changes reported to occur in exercising muscle, and analysed the possible effects these changes may have on the electrical and contractile properties of the muscle. There is no evidence that substrate depletion can account for the decreased force generating capacity, but this factor may be important for the rate of energy turnover and be a major determinant for endurance. Increased concentration of inorganic phosphate and hydrogen ions will depress the force generating capacity, but since fatigue can develop gradually without accumulation of these ions they can only be important when aerobic ATP production is insufficient to support the contractions. Evidence is presented showing that a disturbed balance of K+ alone might cause depolarisation block at high stimulation frequencies, but extracellular K+ accumulation does not increase gradually during prolonged dynamic or static exercise, and is therefore not closely related to fatigue. The repeated release of Ca2+ from the sarcoplasmic reticulum (SR) during muscular activity is suggested of Ca2+ by the mitochondria, increasing with stimulation frequency and duration and possibly also deteriorating mitochondrial function. We therefore speculate that decreased Ca2+ availability for release from SR might contribute to a gradual decline in force generating capacity during all types of exercise.     

Cognitive cost of motor reorganizations associated with muscular fatigue during a repetitive pointing task

Muscular fatigue is known to impair motor performance and to catalyse the development of upper limb musculoskeletal disorders. In order to delay the deleterious effects of muscular fatigue, the central nervous system (CNS) employs compensatory strategies. The cognitive cost of such compensatory strategies was assessed in 10 male subjects who alternatively performed two dual-task protocols before and immediately after an exhaustion procedure specific to upper arm abductor musculature. The main motor tasks were an isometric force-matching and a rapid multi-joint pointing. A secondary probe reaction time (RT) task was performed during both protocols and served as an indicator of attentional demands. Overall motor task performance was maintained despite fatigue. Kinematic and electromyographic data revealed that subjects used motor reorganization during the pointing task when fatigued. The RT increased with fatigue in both dual-task protocols, but this increase was significantly higher during the pointing task than during the force-matching task.The results highlight that the motor reorganization used by the CNS under muscular fatigue states require higher attentional demands than the initial motor organization. Finally, the capacity to delay the deleterious effects of muscular fatigue seems to depend on the proportion of cognitive resources available to plan the compensatory motor strategy.