Functional electrical stimulation using microstimulators to correct foot drop: a case study.

This paper presents a case study that tested the feasibility and efficacy of using injectable microstimulators (BIONs) in a functional electrical stimulation (FES) device to correct foot drop. Compared with surface stimulation of the common peroneal nerve, stimulation with BIONs provides more selective activation of specific muscles. For example, stimulation of the tibialis anterior (TA) and extensor digitorum longus (EDL) muscles with BIONs produces ankle flexion without excessive inversion or eversion of the foot (i.e., balanced flexion). Efficacy was assessed using a 3-dimensional motion analysis of the ankle and foot trajectories during walking with and without stimulation. Without stimulation, the toe on the affected leg drags across the ground. BION stimulation of the TA muscle and deep peroneal nerve (which innervates TA and EDL) elevates the foot such that the toe clears the ground by 3 cm, which is equivalent to the toe clearance in the less affected leg. The physiological cost index (PCI) measured effort during walking. The PCI equals the change in heart rate (from rest to activity) divided by the walking speed; units are beats per metre. The PCI is high without stimulation (2.29 +/- 0.37, mean +/- SD) and greatly reduced with surface (1.29 +/- 0.10) and BIONic stimulation (1.46 +/- 0.24). Also, walking speed 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 BIONic stimulation. These results suggest that FES delivered by a BION is an alternative to surface stimulation and provides selective control of muscle activation.

RF-powered BIONs for stimulation and sensing.

Virtually all bodily functions are controlled by electrical signals in nerves and muscles. Electrical stimulation can restore missing signals but this has been difficult to achieve practically because of limitations in the bioelectric interfaces. Wireless, injectable microdevices are versatile, robust and relatively inexpensive to implant in a variety of sites and applications. Several variants are now in clinical use or under development to perform stimulation and/or sensing functions and to operate autonomously or with continuous coordination and feedback control.

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 3-D 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.

Mesencephalic projections to the first cervical segment in the cat.

Mesencephalic neurons projecting to the upper cervical spinal cord were examined by mapping the distributions of labeled cells after injecting fluorescent tracers or wheat-germ agglutinin conjugated to horseradish peroxidase (WGA-HRP) into the C1 segment. Injections into the central or deep regions of the ventral horn produced retrograde labeling in cells of several mesencephalic regions. The majority of cells were found contralaterally in the superior colliculus and red nucleus, and ipsilaterally in and around the interstitial nucleus of Cajal (INC), in the cuneiform region, and in the fields of Forel. Smaller numbers of cells were located in the periaqueductal gray matter, nucleus annularis, and magnocellular nucleus of the posterior commissure. Dorsomedial injections in the ventral horn near the ventral commissure labeled only a subset of these projections, including cells in the mesencephalic reticular formation adjacent to the INC and in the nucleus annularis. Dorsolateral injections labeled some cells in the superior colliculus and were particularly effective at labeling cells in the red nucleus. These results suggest that at least ten different cell groups project to the ventral horn of the first cervical segment. Most, but not all, groups originate from regions implicated previously in the control of eye or head movements.

Neck muscles in the rhesus monkey. I. Muscle morphometry and histochemistry.

Morphometric methods were used to describe the musculotendinous lengths, fascicle lengths, pennation angles, and cross-sectional areas of neck muscles in adult Macaca mulatta monkeys. Additionally, muscles were frozen, sectioned, and stained for ATPase activity to determine fiber-type composition. Individual rhesus muscles were found to vary widely in their degree of similarity to feline and human muscles studied previously. Suboccipital muscles and muscles supplied by the spinal accessory nerve were most similar to human homologs, whereas most other muscles exhibited architectural specializations. Many neck muscles were architecturally complex, with multiple attachments and internal aponeuroses or tendinous inscriptions that affected the determination of their cross-sectional areas. All muscles were composed of a mixture of type I, IIa, and IIb fiber types the relative proportions of which varied. Typically, head-turning muscles had lower proportions of type II (fast) fibers than homologous feline muscles, whereas extensor muscles contained higher proportions of type II fibers. The physical and histochemical specializations described here are known to have a direct bearing on functional properties, such as force-developing capacity and fatigue-resistance. These specializations must be recognized if muscles are to be modeled accurately or studied electrophysiologically.

Neck muscles in the rhesus monkey. II. Electromyographic patterns of activation underlying postures and movements.

Electromyographic (EMG) activity was recorded in < or = 12 neck muscles in four alert monkeys whose heads were unrestrained to describe the spatial and temporal patterns of neck muscle activation accompanying a large range of head postures and movements. Some head postures and movements were elicited by training animals to generate gaze shifts to visual targets. Other spontaneous head movements were made during orienting, tracking, feeding, expressive, and head-shaking behaviors. These latter movements exhibited a wider range of kinematic patterns. Stable postures and small head movements of only a few degrees were associated with activation of a small number of muscles in a reproducible synergy. Additional muscles were recruited for more eccentric postures and larger movements. For head movements during trained gaze shifts, movement amplitude, velocity, and acceleration were correlated linearly and agonist muscles were recruited without antagonist muscles. Complex sequences of reciprocal bursts in agonist and antagonist muscles were observed during very brisk movements. Turning movements of similar amplitudes that began from different initial head positions were associated with systematic variations in the activities of different muscles and in the relative timings of these activities. Unique recruitment synergies were observed during feeding and head-shaking behaviors. Our results emphasize that the recruitment of a given muscle was generally ordered and consistent but that strategies for coordination among various neck muscles were often complex and appeared to depend on the specifics of musculoskeletal architecture, posture, and movement kinematics that differ substantially among species.

Real-time sonography to estimate muscle thickness: comparison with MRI and CT.

PURPOSE: We investigated the feasibility of using real-time sonography to measure muscle thickness. Clinically, this technique would be used to measure the thickness of human muscles in which intramuscular microstimulators have been implanted to treat or prevent disuse atrophy. METHODS: Porcine muscles were implanted with microstimulators and imaged with sonography, MRI, and CT to assess image artifacts created by the microstimulators and to design protocols for image alignment between methods. Sonography and MRI were then used to image the deltoid and supraspinatus muscles of 6 healthy human subjects. RESULTS: Microstimulators could be imaged with all 3 methods, producing only small imaging artifacts. Muscle-thickness measurements agreed well between methods, particularly when external markers were used to precisely align the imaging planes. The correlation coefficients for sonographic and MRI measurements were 0.96 for the supraspinatus and 0.97 for the deltoid muscle. Repeated sonographic measurements had a low coefficient of variation: 2.3% for the supraspinatus and 3.1% for the deltoid muscle. CONCLUSIONS: Real-time sonography is a relatively simple and inexpensive method of accurately measuring muscle thickness as long as the operator adheres to a strict imaging protocol and avoids excessive pressure with the transducer.

Recruitment properties of intramuscular and nerve-trunk stimulating electrodes.

Functionally useful reanimation of paralyzed limbs generally requires reliable, finely graded control of muscle recruitment and force with minimal fatigue. We used force and electromyographic (EMG) recordings in combination with myofibrillar adenosine triphosphatase activity and glycogen depletion analysis to investigate the recruitment properties of intramuscular (IM) and nerve cuff (NC) stimulating electrodes implanted acutely or chronically in cat hindlimbs. Overall, 32 muscles were submaximally stimulated with current intensities producing approximately 20% of maximal twitch force using 330 ms trains of pulses at 20 and 40 pps. Both the glycogen-depletion and fatigue-test results were found to be difficult to interpret because NC stimulation resulted in surprisingly unstable recruitment during such trains. Fluctuations of force and M-waves within trains of identical stimuli were significantly greater for NC than for IM stimulation. NC stimulation produced much steeper recruitment curves and a reduced tetanus/twitch ratio compared to IM stimulation. IM stimulation produced more reliable and less fatigable recruitment of a mix of motor unit types that tended to be localized in neuromuscular compartments containing, or adjacent to, the IM electrode. We hypothesize that trains of submaximal stimulation applied through NC electrodes resulted in fluctuating recruitment because this electrode configuration magnifies the effects of refractoriness and small changes in axonal excitability during pulse trains.

Marked non-uniformity of fiber-type composition in the primate suboccipital muscle obliquus capitis inferior.

Obliquus capitis inferior (OCI) is a monoarticular suboccipital muscle linking the transverse process of the atlas (C1) to the spinous process of the axis (C2). Histochemical analysis of fiber-type composition showed that the muscle has a marked gradient of fiber-type distribution in which type I fibers comprise 95-100% of fibers in the deepest region but less than 10% of fibers in the superficial layer. Step-like changes in fiber-type proportions occurred between groups of fascicles. In most instances the boundaries between these fascicles did not exhibit different perimysial features from those fascicles with similar fiber-type proportions. OCI contained large numbers of muscle spindles, which were concentrated in deep regions rich in type I fibers. The degree of nonuniformity in fiber-type distribution seen in OCI is unusually large when compared with patterns described in other primate muscles, and has implications for the way that the muscle is studied anatomically and physiologically.

Morphometry, histochemistry, and innervation of cervical shoulder muscles in the cat.

Morphometric and histochemical methods were used to estimate the force-developing capabilities and fiber-type contents of four muscle complexes (rhomboideus, levator scapulae, trapezius, and sternomastoideus) that link the shoulder girdle to the skull and cervical vertebrae. Each complex contained at least two member muscles that were distinctive architecturally and often had specialized innervation patterns. Trapezius and sternocleidomastoideus were innervated by both cranial nerve XI and cervical spinal nerves. Glycogen depletion of trapezius suggested that the nerves derived from cervical roots might be entirely sensory. Muscles within each complex varied in physiological cross-sectional area from less than 0.1 cm2 to greater than 1 cm2. They showed differences in fiber-type composition that suggested specialized roles for different behaviors. The morphometric features of the cervical shoulder muscles suggest that they have considerable potential to produce head movements and should be incorporated into feline head-movement models.

Feline caudofemoralis muscle. Muscle fibre properties, architecture, and motor innervation.

Feline caudofemoralis (CF) is a promising preparation in which to study the properties of mammalian fast-twitch skeletal muscle, but little is known about its muscle fiber properties, architecture, and motor innervation. We used histochemical techniques to confirm that it contained predominantly type IIB fibers (95+/-2%, n=8, with six of eight muscles composed exclusively of type IIA and IIB fibers), but physiological experiments showed less fatiguability than for the type IIB component of medial gastrocnemius. This may be related to the surprisingly strong and regular recruitment of CF during repetitive tasks such as walking and trotting, which we demonstrated electromyographically. We measured muscle length over the anatomical range of motion for CF (approximately 0.6-1.2 L0) and estimated working length during walking and trotting (approximately 0.95-1.15 L0). The specific tension was similar to that of the exclusively slow-twitch soleus muscle (31.2+/-4.7 N/cm2 compared with 31.8+/-4.1 N/cm2; P>0.8). Single fiber dissections of CF revealed a series-fibered architecture with a mean of 2.3 fibers, each 2.5 cm long, required to span the fascicle length. We identified two neuromuscular compartments in CF by cutting one of the two nerve branches innervating CF and depleting the glycogen stores in the intact motor units. These compartments were in parallel and extended the length of the muscle; their electromyographic activity was similar during various natural behaviors. CF and gluteus maximus motoneurons were labeled concurrently with a combination of fluorescent, retrograde tracers including Fluororuby, Fluorogold and Fast Blue. The CF motor nucleus was located in L7-S1, overlapping and intermingling extensively with the nucleus of the adjacent gluteus maximus muscle. Distributions of CF motoneuron diameter revealed one large peak around 50-55 microm, with relatively few small-diameter (less than 35 microm) cells. Using estimates of the total number of fibers in three muscles and the estimated number of alpha-motoneurons for those same muscles, we calculated a mean innervation ratio of approximately 270, which is at the low end of the innervation ratios for type IIB motor units from other feline muscles and more similar to type IIA motor units. In general, CF appears to be a useful preparation in which to study the properties of fast-twitch muscle, but these properties may vary somewhat from type IIB fibers from different muscles.

Long-term biocompatibility of a miniature stimulator implanted in feline hind limb muscles.

Chronic foreign-body responses and muscular changes were examined following the implantation of active miniature stimulators into the hind limb muscles of cats for periods of up to three months. The radio-frequency (RF)-powered stimulators were injected into muscles through a 12-gauge hypodermic needle. The tissue responses around the active stimulators were compared histologically to those provoked by passive devices, broken glass, silicone tubing, polyester suture material coated with polybutylate, and two of the internal components of the stimulator (ferrite, integrated circuit chip). Active and passive stimulators produced similar, benign foreign-body reactions that resulted in an essentially identical fibrous capsule over time. The responses were similar to those produced by the internal components and the suture material, and were more modest than those produced by the broken glass. The capsule did not appear to interfere with the functionality of active devices because thresholds measured during the post-implantation survival period did not change significantly over time. Unexpectedly, the severity of the reaction differed significantly amongst the various target muscles. Medial gastrocnemius exhibited the most severe response, whereas tibialis anterior had the least reaction.

Effects of regional stimulation using a miniature stimulator implanted in feline posterior biceps femoris.

The effects of placement of a miniature implantable stimulator on motor unit recruitment were examined in the posterior head of cat biceps femoris. The implantable stimulator (13-mm long x 2-mm diameter) was injected either proximally near the main nerve branch, or distally near the muscle insertion, through a 12-gauge hypodermic needle. Glycogen-depletion methods were used to map the distribution of fibers activated by electrical stimulation. Muscle fibers were found to be depleted at most or all proximodistal levels of the muscle, but the density of depleted fibers varied transversely according to the stimulus strength and proximity of the device to the nerve-entry site. Thus, muscle cross sections often had a "patchy" appearance produced because different proportions of depleted fibers intermingled with undepleted fibers in different parts of the cross section. In other preparations, the force of muscle contraction was measured when stimuli of varying strengths were delivered by the stimulator positioned at the same proximal or distal sites within the muscle. Devices placed close to the nerve-entry site produced the greatest forces. Those placed more distally produced less force. As stimulus current and/or pulse width increased, muscle force increased, often in steps, until a maximum was reached, which was usually limited by the compliance voltage of the device to less than the force produced by whole nerve stimulation.

Morphometry of human neck muscles.

STUDY DESIGN: Cadaveric dissections were used to study muscle morphometry. OBJECTIVE: To describe systematically the musculotendinous lengths, fascicle lengths, pennation angles, and physiologic cross-sectional areas of neck and shoulder muscles implicated in head movement. SUMMARY OF BACKGROUND DATA: In previous studies of neck-muscle anatomy, researchers described only a subset of muscle features, often using crude or indirect methods. None used microdissected muscles to correct measured parameters for the presence of multiple fiber compartments, internal aponeuroses, or variations in fiber or sarcomere length required for qualitative models of force-generating capabilities. METHODS: Muscle mass, pennation angle, fascicle length, and sarcomere length were measured in 14 neck muscles from 10 human cadavers. Architecturally complex muscles with multiple attachments were divided into subvolumes, and each subvolume was examined from both the superficial and deep surfaces, Internal aponeuroses were microdissected within muscles to characterize architectural specializations. Physiologic cross-sectional areas were calculated from the morphometric data. RESULTS: The neck musculature was architecturally complex. Many muscles crossed two or more joints and had multiple attachments to different bones. In some, the presence of tendons and aponeuroses was associated with specializations in fascicle organization. Considerable interindividual variation was found in the number and location of tendinous insertions of the scalenes and longissimus capitis muscles. In addition, rhomboideus showed significant variations in its size and shape. The cross-sectional areas of neck muscles from large and small subjects did not scale proportionately with body height and weight, nor did individual muscles with widely varying cross-sectional areas (0.3-15.3cm2) scale from on subject to another. CONCLUSIONS: The accuracy of morphometry can be improved by incorporating measurements made by microdissecting neck muscles. The presence of aponeurotic attachments can greatly shorten fascicle length; failure to identify such attachments can lead to underestimates of cross-sectional areas. Accuracy of a generalized model of the neck is also improved by normalizing sarcomere lengths in all muscles.

Shoulder and forelimb orientations and loading in sitting cats: implications for head and shoulder movement.

A three-dimensional static analysis was carried out to characterize the effects of ground reaction forces propagated through different joints in the forelimb and shoulder of quietly sitting cats. Stereofluoroscopy, used to identify the orientations of bones, showed that the scapula is held in a parasagittal plane, with its vertebral border located dorsally to the spines of thoracic vertebrae. The forelimb is held with the elbow flexed. Loading on the elbow tended to flex and adduct the ulna, whereas loading on the glenohumeral joint tended to extend, adduct and internally rotate the humerus. Loading on the scapula was confined primarily to the sagittal plane and tended to rotate the vertebral border of the scapula caudally around the head of the humerus. This caudally-directed moment suggests that the static equilibrium of the feline scapula depends upon muscular forces directed cranially, presumably by way of attachments on the skull and cervical column. The differing arrangement of the shoulder-to-neck transition in cats and humans suggests caution in the use of feline models to represent some aspects of human head movement.

How to construct and move a cat's neck.

Extensive information has been accumulated over the past several years about the head-neck sensory-motor system, in particular that relating to cats. Using still x-ray and cineradiographic analysis, the skeletal geometry of head-neck posture in three dimensions--when an animal is resting, actively orienting, or locomoting--is described. From these descriptions, cervical, vertebral, and craniocervical joint biomechanics for all three rotational dimensions are quantified. These behavioral data on muscle and skeletal movements have been incorporated in a biomechanical, functional anatomical model of the head-neck movement system. Individual as well as groups of neck muscles have been measured in detail and their kinematics determined. The role of a number of these muscles will be described for several reflex and voluntary behavioral contexts, including muscle co-contractions. Having established how each movement is accomplished, the neuronal sensory-motor reflex basis of head-neck system stabilization in space is addressed. The vestibular system is largely responsible for acquisition and maintenance of upright posture. The bilateral semicircular canals (horizontal, anterior, posterior) and otoliths (sacculus, utriculus) feed information differentially to specific neck muscles: these connections are reviewed with regard to the origin of the reflex are from each receptor to its destination of specific muscles. Behavioral data from normal animals, and from animals whose vestibular receptor systems are selectively lesioned, will be reviewed to complement the functional interpretation of the sensory-motor transformations. Finally, the requirements for space-time coordinated cat head-neck movements will be synthesized, based on biomechanics, muscle kinematics, canal/otolith connectivity, and selective lesion experiments.

Distribution of motoneurons supplying feline neck muscles taking origin from the shoulder girdle.

A combination of fluorescent retrograde tracers and horseradish peroxidase (HRP) was used to compare the spinal distributions of motoneurons supplying shoulder muscles with attachments to the skull and cervical spinal cord that suggest a significant role in head movement. Two muscles, the rhomboideus and the levator scapulae, were innervated by multiple segmental nerve bundles that entered the muscles at different rostrocaudal locations. Motoneurons that were labelled retrogradely from rhomboideus nerve bundles formed a single, long column in the ventral horn from C4 to C6, lateral to previously studied motor nuclei supplying deep neck muscles. When different tracers were used to differentiate motoneurons supplying specific nerve bundles, discrete subnuclei could be identified that were organized in a rostrocaudal sequence corresponding to the rostrocaudal order of the nerve bundles. Levator scapulae motoneurons formed a second elongate column immediately lateral to the rhomboidues motor nucleus. Three other muscles, that trapezius, sternomastoideus, and cleidomastoideus, were supplied by cranial nerve XI. Labelled motoneurons from these muscles formed a single column from the spinomedullary junction to middle C6. Within this column, the three motor nuclei supplying the sternomastoideus, cleidomastoideus, and trapezius were laminated mediolaterally. Sternomastoideus and cleidomastoideus motoneurons were confined to upper cervical segments, whereas trapezius motoneurons were found from C1 to C6. In C1 and C6, the motoneuron column was located centrally in the gray matter, but, between C2 and C5, the column lay on the lateral wall of the ventral horn in a position dorsolateral to motor nuclei supplying the rhomboideus and the deeper neck muscles. The findings in this study suggest that descending and propriospinal systems responsible for coordinating head movement may have to descend as far caudally as C6 if they are to project onto muscles controlling the mobility of the lower neck.

Effect of neck posture on patterns of activation of feline neck muscles during horizontal rotation.

The electromyographic (EMG) patterns of neck muscles were recorded during whole-body horizontal rotation in head-free, alert cats and head-restrained, decerebrate cats. In some trials the cervical column of the animal was oriented vertically, whereas in others it was oriented more horizontally. In alert cats making head movements that compensated for the motion of the platform, neck muscles with modulated patterns of activity could be divided into a subset whose individual EMG patterns changed significantly when the neck posture was altered (including longissimus capitis, obliquus capitis superior and scalenus anterior) and a subset whose individual EMG patterns were invariant regardless of neck posture (including obliquus capitis inferior, levator scapulae and complexus). In head-restrained, decerebrate cats, electromyograms from all implanted muscles were modulated similarly in phase with the platform position. Changing the orientation of the neck had little effect upon these EMG patterns evoked by the horizontal vestibulocollic reflex. One decerebrate cat with strong extensor tone was tested further under head-free conditions. There was very little compensatory head movement, but individual neck muscles displayed patterns of activity that were more similar to those observed in alert, head-free animals.

A novel method to identify migration of small implantable devices.

A histologic method has been developed to assess the migration of chronically-implanted intramuscular devices. Bullet-shaped glass devices with varying tip configurations and glass-encapsulated microstimulators of a similar size were loaded with the fluorescent tracer Procion Yellow dissolved in molten glucose. Dissolution of the hardened glucose soon after contact with body fluids released the Procion Yellow, which binds irreversibly to local tissues, thereby marking the initial site of implantation with a localized fluorescent spot. After survival times of 2-7 weeks, histologic analysis usually showed a close physical relationship between the fluorescent spot and the connective-tissue capsule from which the device was extracted. In one case, migration of a sharply pointed device from the deep surface of an implanted muscle was recognized by differences in the location of the dye spot and the site of explantation from nearby fascia. Results suggested that this method could measure migratory distances as small as 5-10 mm.