Intraspinal microstimulation generates functional movements after spinal-cord injury

Restoring locomotion after spinal-cord injury has been a difficult problem to solve with traditional functional electrical stimulation (FES) systems. Intraspinal microstimulation (ISMS) is a novel approach to FES that takes advantage of spinal-cord locomotor circuits by stimulating in the spinal cord directly. Previous studies in spinal-cord intact cats showed near normal recruitment order, reduced fatigue, and functional, synergistic movements induced by stimulation through a few microwires implanted over a 3-cm region in the lumbosacral cord. The present study sought to test the feasibility of ISMS for restoring locomotion after complete spinal-cord transection. In four adult male cats, the spinal cord was severed at T10, T11, or T12. Two to four weeks later, 30 wires (30 microm, stainless steel) were implanted, under anesthesia, in both sides of the lumbosacral cord. The cats were then decerebrated. Stimulus pulses (40-50 Hz, 200 micros, biphasic) with amplitudes ranging from 1-4x threshold (threshold = 32 +/- 19 microA) were delivered through each unipolar electrode. Kinetics, kinematics, and electromyographic (EMG) measurements were obtained with the cats suspended over a stationary treadmill with embedded force platforms for the hindlimbs. Phasic, interleaved stimulation through electrodes generating flexor or extensor movements produced bilateral weight-bearing stepping of the hindlimbs with ample foot clearance during swing. Minimal changes in kinematics and little fatigue were seen during episodes of 40 consecutive steps. The results indicate that ISMS is a promising technique for restoring locomotion after injury.     

Intraspinal micro stimulation generates locomotor-like and feedback-controlled movements

Intraspinal microstimulation (ISMS) may provide a means for improving motor function in people suffering from spinal cord injuries, head trauma, or stroke. The goal of this study was to determine whether microstimulation of the mammalian spinal cord could generate locomotor-like stepping and feedback-controlled movements of the hindlimbs. Under pentobarbital anesthesia, 24 insulated microwires were implanted in the lumbosacral cord of three adult cats. The cats were placed in a sling leaving all limbs pendent. Bilateral alternating stepping of the hindlimbs was achieved by stimulating through as few as two electrodes in each side of the spinal cord. Typical stride lengths were 23.5 cm, and ample foot clearance was achieved during swing. Mean ground reaction force during stance was 36.4 N, sufficient for load-bearing. Feedback-controlled movements of the cat's foot were achieved by reciprocally modulating the amplitude of stimuli delivered through two intraspinal electrodes generating ankle flexion and extension such that the distance between a sensor on the cat's foot and a free sensor moved back and forth by the investigators was minimized.. The foot tracked the displacements of the target sensor through its normal range of motion. Stimulation through electrodes with tips in or near lamina IX elicited movements most suitable for locomotion. In chronically implanted awake cats, stimulation through dorsally located electrodes generated paw shakes and flexion-withdrawals consistent with sensory perception but no weight-bearing extensor movements. These locations would not be suitable for ISMS in incomplete spinal cord injuries. Despite the complexity of the spinal neuronal networks, our results demonstrate that by stimulating through a few intraspinal microwires, near-normal bipedal locomotor-like stepping and feedback-controlled movements could be achieved.     

Could cortical signals control intraspinal stimulators? A theoretical evaluation.

In this paper, we examine the control signals that are required to generate stepping using two different intraspinal microstimulation (ISMS) paradigms and discuss the theoretical feasibility of controlling ISMS-evoked stepping using a brain computer interface. Tonic (constant amplitude) and phasic (modulated amplitude) ISMS protocols were used to produce stepping in the hind limbs of paralyzed cats. Low-amplitude tonic ISMS activated a spinal locomotor-like network that resulted in bilateral stepping of the hind limbs. Phasic ISMS generated coordinated stepping by simultaneously activating flexor synergies in one limb coupled with extensor synergies in the other. Using these ISMS paradigms, we propose that one or two independent cortical signals will be adequate for controlling ISMS-induced stepping after SCI.     

A pilot study of myoelectrically controlled FES of upper extremity

Functional electrical stimulation (FES) of upper limbs can be used for the recovery of some hand functions on patients with CNS lesions. This study deals with the control of FES by means of myoelectrical activity detected from voluntarily activated paretic muscles. The specific aim of this paper is to evaluate the accuracy of myoelectrical control in terms of produced force and movement. For this purpose, a specific device called myoelectrical controlled functional electrical stimulator (MeCFES) has been developed and applied to six tetraplegic patients with a spinal cord lesion and one stroke hemiplegic patient. Residual myoelectric signals from the paretic wrist extensor (m. extensor carpi radialis, ECR) have been used to control stimulation of either the wrist extension (i.e., the same muscle) or thumb flexion. A tracking test based on a visual feedback of the produced force or movement compared to a reference target trajectory was used to quantify control accuracy. A comparison was made between the tracking performances of each subject with and without the MeCFES and the learning process for two of the subjects were observed during consecutive sessions. Results showed that the wrist extension was improved in three out of five C5 SCI patients and the thumb flexion was largely increased in one incomplete C3 SCI patient. The hemiplegic patient showed limited thumb control with the MeCFES but indicated the possibility of a carry over effect. It was found that a low residual natural force resulted in a less accurate movement but also with a large increase (up to ten times) of the muscle output. On the contrary, persons with a medium residual force obtained a smaller amplification of muscle force with a higher tracking accuracy     

Restoration of use of paralyzed limb muscles using sensory nerve signals for state control of FES-assisted walking.

A real-time functional electrical stimulation (FES) state controller was designed that utilized sensory nerve cuff signals from the cat forelimb to control the timing of stimulation of the Palmaris Longus (PalL) muscle during walking on the treadmill. Sensory nerve signals from the median and superficial radial nerves provided accurate, reliable feedback related to foot contact and lift-off which, when analyzed with single threshold Schmitt triggers, produced valuable state information about the step cycle. The study involved three experiments: prediction of the timing of muscle activity in an open-loop configuration with no stimulation, prediction of the timing of muscle activity in a closed-loop configuration that included stimulation of the muscle over natural PaIL electromyogram (EMG), and temporary paralysis of selected forelimb muscles coupled with the use of the state controller to stimulate the PalL in order to return partial support function to the anesthetized limb. The FES state controller was tested in a variety of walking conditions, including different treadmill speeds and slopes. The results obtained in these experiments demonstrate that nerve cuff signals can provide a useful source of feedback to FES systems for control of limb function.     

The effects of long-term FES-assisted walking on intrinsic and reflex dynamic stiffness in spastic spinal-cord-injured subjects

The effects of long-term functional electrical stimulation (FES)-assisted walking on ankle dynamic stiffness were examined in spinal cord-injured (SCI) subjects with incomplete motor function loss. A parallel-cascade system identification method was used to identify intrinsic and reflex contributions to dynamic ankle stiffness at different ankle positions while subjects remained relaxed. Intrinsic stiffness dynamics were well modeled by a linear second-order model relating intrinsic torque to joint position. Reflex stiffness dynamics were accurately described by a linear third-order model relating halfwave rectified velocity to reflex torque. We examined four SCI subjects before and after long-term FES-assisted walking (>16 mo). Another SCI subject, who used FES for only five months was examined 12 mo latter to serve as a non-FES, SCI control. Reflex stiffness decreased in FES subjects by an average of 53% following FES-assisted walking, intrinsic stiffness also dropped by 45%. In contrast, both reflex and intrinsic stiffness increased in the non-FES, SCI control. These findings suggest that FES-assisted walking may have therapeutic effects, helping to reduce abnormal joint stiffness.     

Control of limb movements by functional neuromuscular stimulation

Summary form only given. Functional neuromuscular stimulation (FNS) provides a means to restore motor functions for spinal cord injury (SCI) and stroke patients. Most FNS clinical systems operate under open-loop control methods, but closed-loop hand grasp systems are now being tested. Closed-loop control is most suitable for motor tasks requiring low speed and high accuracy, such as hand grasp. Open-loop feedforward control is desirable for high speed motor acts such as arm movement and walking. To satisfy the requirements of speed and accuracy, and to account for the biomechanics of FNS task control, a combined open-loop and closed-loop controller structure design, called the perturbation controller, is proposed. In this control system, the patient commands initiate the task by instructing the controller with movement direction, distance and speed. The feedforward controller interprets the instructions and generates the desired movement trajectory, stiffness, and feedforward input to activate muscles     

Nerve cuff recordings of muscle afferent activity from tibial and peroneal nerves in rabbit during passive ankle motion.

Activity from muscle afferents regarding ankle kinesthesia was recorded using cuff electrodes in a rabbit preparation in which tactile input from the foot was eliminated. The purpose was to determine if such activity can provide information useful in controlling functional electrical stimulation (FES) systems that restore mobility in spinal injured man. The rabbit's ankle was passively flexed and extended while the activity of the tibial and peroneal nerves was recorded. Responses to trapezoidal stimulus profiles were investigated for excursions from 10 degrees to 60 degrees using velocities from 5 degrees/s to 30 degrees/s and different initial ankle positions. The recorded signals mainly reflect activity from primary and secondary muscle afferents. Dorsiflexion stretched the ankle extensors and produced velocity dependent activity in the tibial nerve, and this diminished to a tonic level during the stimulus plateau. The peroneal nerve was silent during dorsiflexion, but was activated by stretch of the peroneal muscles during ankle extension. The responses of the two nerves behaved in a reciprocal manner, but exhibited considerable hysteresis, since motion that relaxed the stretch to the driving muscle produced an immediate cessation of the prior stretch induced activity. A noted difference between the tibial and peroneal nerve responses is that the range of joint position change that activated the flexor afferents was greater then for the extensor afferents. Ankle rotation at higher velocities increased the dynamic stretch evoked responses during the stimulus ramp but showed no effect on the tonic activity during the stimulus plateau. Prestretching the muscles by altering the initial position increased the response to the ramp movement, however, for the peroneal nerve, when the prestretch brought the flexor muscles near to their maximal lengths, the response to additional stretch provided by the ramp movement was diminished. The results indicate that the whole nerve recorded muscle afferent activity may be useful for control of FES assisted standing, because it can indicate the direction of rotation of the passively moved ankle joint, along with coarse information regarding the rate of movement and static joint position.     

Paraplegic standing supported by FES-controlled ankle stiffness

The objective of this paper was to investigate whether a paraplegic subject is able to maintain balance during standing by means of voluntary and reflex activity of the upper body while being supported by closed loop controlled ankle stiffness using FES. The knees and hips of the subject were held in extended positions by a mechanical apparatus, which restricted movement to the sagittal plane. The subject underwent several training sessions where the appropriate level of stiffness around the ankles was maintained by the mechanical apparatus. This enabled the subject to learn how to use the upper body for balancing. After the subject gained adequate skills closed-loop FES was employed to regulate ankle stiffness, replacing the stiffness provided by the apparatus. A method to control antagonist muscle moment was implemented. In subsequent standing sessions, the subject had no difficulties in maintaining balance. When the FES support was withheld, the ability to balance was lost.     

Locomotor-related networks in the lumbosacral enlargement of the adult spinal cat: activation through intraspinal microstimulation.

It is commonly accepted that locomotor-related neuronal circuitry resides in the lumbosacral spinal cord. Pharmacological agents, epidural electrical stimulation, and sensory stimulation can be used to activate these instrinsic networks in in vitro neonatal rat and in vivo cat preparations. In this study, we investigated the use of low-level tonic intraspinal microstimulation (ISMS) as a means of activating spinal locomotor networks in adult cats with complete spinal transections. Trains of low-amplitude electrical pulses were delivered to the spinal cord via groups of fine microwires implanted in the ventral horns of the lumbosacral enlargement. In contrast to published reports, tonic ISMS applied through microwires in the caudal regions of the lumbosacral enlargement (L7-S1) was more effective in eliciting alternating movements in the hindlimbs than stimulation in the rostral regions. Possible mechanisms of action of tonic ISMS include depolarization of locally oscillating networks in the lumbosacral cord, backfiring of primary afferents, or activation of propriospinal neurons.     

Feasibility of EMG-Based Neural Network Controller for an Upper Extremity Neuroprosthesis

The overarching goal of this project is to provide shoulder and elbow function to individuals with C5/C6 spinal cord injury (SCI) using functional electrical stimulation (FES), increasing the functional outcomes currently provided by a hand neuroprosthesis. The specific goal of this study was to design a controller based on an artificial neural network (ANN) that extracts information from the activity of muscles that remain under voluntary control sufficient to predict appropriate stimulation levels for several paralyzed muscles in the upper extremity. The ANN was trained with activation data obtained from simulations using a musculoskeletal model of the arm that was modified to reflect C5 SCI and FES capabilities. Several arm movements were recorded from able-bodied subjects and these kinematics served as the inputs to inverse dynamic simulations that predicted muscle activation patterns corresponding to the movements recorded. A system identification procedure was used to identify an optimal reduced set of voluntary input muscles from the larger set that are typically under voluntary control in C5 SCI. These voluntary activations were used as the inputs to the ANN and muscles that are typically paralyzed in C5 SCI were the outputs to be predicted. The neural network controller was able to predict the needed FES paralyzed muscle activations from “voluntary” activations with less than a 3.6% RMS prediction error.      

Musculoskeletal Model-Guided, Customizable Selection of Shoulder and Elbow Muscles for a C5 SCI Neuroprosthesis

Individuals with C5/C6 spinal cord injury (SCI) have a number of paralyzed muscles in their upper extremities that can be electrically activated in a coordinated manner to restore function. The selection of a practical subset of paralyzed muscles for stimulation depends on the specific condition of the individual, the functions targeted for restoration, and surgical considerations. This paper presents a musculoskeletal model-based approach for optimizing the muscle set used for functional electrical stimulation (FES) of the shoulder and elbow in this population. Experimentally recorded kinematics from able-bodied subjects served as inputs to a musculoskeletal model of the shoulder and elbow, which was modified to reflect the reduced muscle force capacities of an individual with C5 SCI but also the potential of using FES to activate paralyzed muscles. A large number of inverse dynamic simulations mimicking typical activities of daily living were performed that included (1) muscles with retained voluntary control and (2) many different combinations of stimulated paralyzed muscles. These results indicate that a muscle set consisting of the serratus anterior, infraspinatus and triceps would enable the greatest range of relevant movements. This set will become the initial target in a C5SCI neuroprosthesis to restore shoulder and elbow function.     

Functional restoration of elbow extension after spinal-cord injury using a neural network-based synergistic FES controller.

Individuals with a C5/C6 spinal-cord injury (SCI) have paralyzed elbow extensors, yet retain weak to strong voluntary control of elbow flexion and some shoulder movements. They lack elbow extension, which is critical during activities of daily living. This research focuses on the functional evaluation of a developed synergistic controller employing remaining voluntary elbow flexor and shoulder electromyography (EMG) to control elbow extension with functional electrical stimulation (FES). Remaining voluntarily controlled upper extremity muscles were used to train an artificial neural network (ANN) to control stimulation of the paralyzed triceps. Surface EMG was collected from SCI subjects while they produced isometric endpoint force vectors of varying magnitude and direction using triceps stimulation levels predicted by a biomechanical model. ANNs were trained with the collected EMG and stimulation levels. We hypothesized that once trained and implemented in real-time, the synergistic controller would provide several functional benefits. We anticipated the synergistic controller would provide a larger range of endpoint force vectors, the ability to grade and maintain forces, the ability to complete a functional overhead reach task, and use less overall stimulation than a constant stimulation scheme.     

Control of the Lower Leg During Walking: A Versatile Model of the Foot

An improved biomechanical model has been implemented for use in gait simulations and functional electrical stimulation (FES). The novelty includes longitudinal bending of the foot which implements geometrical changes that appear “healthy-like” during the stance phase of gait. The simulation uses optimal control which minimizes the activation of flexor and extensor muscles, as well as the tracking error. Correspondingly, the results of the bending foot model, contrasted against a rigid foot biomechanical model, show that torques in the knee during foot contact were as much as 36.9 Nm (46.1%) lower, while muscle excitation was on average 6.1% lower. The simulation also shows that the shank angle of the bending foot model was virtually identical to that of the rigid foot model. However, this model's worth is most prevalent in its use for stance phase control in individuals who use multichannel FES. Notably, it can also be used for simulating the gait of individuals who lack ankle articulation and use an active transfemoral prosthesis.      

Functional electrical stimulation of abdominal muscles to augment tidal volume in spinal cord injury.

Functional electrical stimulation (FES) of abdominal muscles as a method of enhancing ventilation was explored in six neurologically intact subjects and five subjects with spinal cord injury (SCI) who had levels of injury between C4 and C7. Pulmonary ventilation was augmented in both groups predominantly due to an increase in tidal volume. The average increase in tidal volume during FES for the neurologically intact group was 350 ml, while in the SCI group it was 220 ml. The FES caused active volume decreases in both the lower thorax and upper abdomen, which together appear to be the mechanism behind the increases seen in tidal volume. Therefore, the proposed method might be useful in future clinical practice. The results indicate that FES of abdominal muscles should be more thoroughly explored as a potential technique of ventilatory support in SCI. The results also point to the necessity for further studies of maintaining the condition of the chest wall in the pulmonary rehabilitation of individuals with tetraplegia.     

Model-based control of FES-induced single joint movements

A crucial issue of functional electrical stimulation (FES) is the control of motor function by the artificial activation of paralyzed muscles. Major problems that limit the success of current FES systems are the nonlinearity of the target system and the rapid change of muscle properties due to fatigue. In this study, four different strategies, including an adaptive algorithm, to control the movement of the freely swinging shank were developed on the basis of computer simulations and experimentally evaluated on two subjects with paraplegia due to a complete thoracic spinal cord injury. After developing a nonlinear, physiologically based model describing the dynamic behavior of the knee joint and muscles, an open-loop approach, a closed-loop approach, and a combination of both were tested. In order to automate the individual adjustments cited, we further evaluated the performance of an adaptive feedforward controller. The two parameters chosen for the adaptation were the threshold pulse width and the scaling factor for adjusting the active moment produced by the stimulated muscle to the fitness of the muscle. These parameters have been chosen because of their significant time variability. The first three controllers with fixed parameters yielded satisfactory result. An additional improvement was achieved by applying the adaptive algorithm that could cope with problems due to muscle fatigue, thus permitting on-line identification of critical parameters of the plant. Although the present study is limited to a simplified experimental setup, its applicability to more complex and functional movements can be expected     

The effect of random modulation of functional electrical stimulation parameters on muscle fatigue.

Muscle contractions induced by functional electrical stimulation (FES) tend to result in rapid muscle fatigue, which greatly limits activities such as FES-assisted standing and walking. It was hypothesized that muscle fatigue caused by FES could be reduced by randomly modulating parameters of the electrical stimulus. Seven paraplegic subjects participated in this study. While subjects were seated, FES was applied to quadriceps and tibialis anterior muscles bilaterally using surface electrodes. The isometric force was measured, and the time for the force to drop by 3 dB (fatigue time) and the normalized force-time integral (FTI) were determined. Four different modes of FES were applied in random order: constant stimulation, randomized frequency (mean 40 Hz), randomized current amplitude, and randomized pulsewidth (mean 250 micros). In randomized trials, stimulation parameters were stochastically modulated every 100 ms in a range of +/-15% using a uniform probability distribution. There was no significant difference between the fatigue time measurements for the four modes of stimulation. There was also no significant difference in the FTI measurements. Therefore, our particular method of stochastic modulation of the stimulation parameters, which involved moderate (15%) variations updated every 100 ms and centered around 40 Hz, appeared to have no effect on muscle fatigue. There was a strong correlation between maximum force measurements and stimulation order, which was not apparent in the fatigue time or FTI measurements. It was concluded that a 10-min rest period between stimulation trials was insufficient to allow full recovery of muscle strength.     

New results in feedback control of unsupported standing in paraplegia

The aim of this study was to implement a new approach to feedback control of unsupported standing and to evaluate it in tests with an intact and a paraplegic subject. In our setup, all joints above the ankles are braced and stabilizing torque at the ankle is generated by electrical stimulation of the plantarflexor muscles. A previous study showed that short periods of unsupported standing with a paraplegic subject could be achieved. In order to improve consistency and reliability and to prolong the duration of standing, we have implemented several modifications to the control strategy. These include a simplified control structure and a different controller design method. While the reliability of standing is mainly limited by the muscle characteristics such as reduced strength and progressive fatigue, the results presented here show that the new strategy allows much longer periods (up to several minutes) of unsupported standing in paraplegia.     

Interleaved, multisite electrical stimulation of cat sciatic nerve produces fatigue-resistant, ripple-free motor responses

We studied the use of physiologically based, multisite, intrafascicular electrical stimulation of the sciatic nerve to achieve ripple-free contractions and sustained, fatigue-resistant forces over a physiological range of forces in cat gastrocnemius muscle. Electrode arrays containing 100, 0.5-1.5-mm-long penetrating microelectrodes were inserted into the sciatic nerves of cats, and forces generated by gastrocnemius muscles in response to stimulation of the nerves were monitored via a force transducer attached to the tendons. In single-electrode stimulation, responses evoked by low-frequency [15 pulses/second, (p/s)] stimulation exhibited greater fatigue resistance than did responses evoked by higher frequency stimulation (30 and 60 p/s), but showed far more ripple within each response. We compared interleaved 15 p/s stimulation of four electrodes (100 micros biphasic pulses, 750-ms pulse trains) that produced a net stimulation frequency of 60 p/s with multielectrode 60 p/s quasi-simultaneous stimulation protocols. Across a broad range of forces (10% to 80% of maximum), responses evoked by multielectrode 15 p/s interleaved stimulation exhibited substantially less fatigue than did responses evoked by 60 p/s quasi-simultaneous stimulation, and less ripple than responses evoked by single-electrode 15 p/s stimulation. The effectiveness of this physiologically based stimulation paradigm encourages its application in the field of motor neuroprosthetics.     

BIONic WalkAide for correcting foot drop.

The goal of this study was to test the feasibility and efficacy of using microstimulators (BIONs) to correct foot drop, the first human application of BIONs in functional electrical stimulation (FES). A prototype BIONic foot drop stimulator was developed by modifying a WalkAide2 stimulator to control BION stimulation of the ankle dorsiflexor muscles. BION stimulation was compared with surface stimulation of the common peroneal nerve provided by a normal WalkAide2 foot drop stimulator. Compared to surface stimulation, we found that BION stimulation of the deep peroneal nerve produces a more balanced ankle flexion movement without everting the foot. A three-dimensional motion analysis was performed to measure the ankle and foot kinematics with and without stimulation. Without stimulation, the toe on the affected leg drags across the ground. The BIONic WalkAide elevates the foot such that the toe clears the ground by 3 cm, which is equivalent to the toe clearance in the unaffected leg. The physiological cost index (PCI) was used to measure effort during walking. The PCI is high without stimulation (2.29 +/- 0.37; mean +/- S.D.) and greatly reduced with surface (1.29 +/- 0.10) and BION stimulation (1.46 +/- 0.24). Also, walking speed is increased from 9.4 +/- 0.4 m/min without stimulation to 19.6 +/- 2.0 m/min with surface and 17.8 +/- 0.7 m/min with BION stimulation. We conclude that functional electrical stimulation with BIONs is a practical alternative to surface stimulation and provides more selective control of muscle activation.