William Z. Rymer

Simultaneous and nonlinear identification of mechanical and reflex properties of human elbow joint muscles

The naturally coexisting intrinsic mechanical and reflex properties of the human elbow joint were identified simultaneously using nonlinear, time-delay, continuous-time, and dynamic models. Angular random perturbations of small amplitude and low bandwidth were applied to the joint using a computer-controlled servomotor, while the subject maintained various levels of mean background muscle torque. Joint neuromuscular dynamics were identified from the measured elbow angle and torque. Stretch reflexes were modeled nonlinearly with both dynamic and static reflex gains. A continuous-time system identification method was developed to estimate parameters of the nonlinear models directly from sampled data while retaining realistic physical or physiological interpretations. Results from six subjects showed that dynamic stretch reflex gains, joint stiffness, and viscosity generally increased with mean background muscle torque; and that dynamic stretch reflex gain was higher during muscle stretch than that during muscle shortening. More importantly, the study provided realistic simultaneous estimates of the relative contributions of intrinsic mechanical and reflex actions to net joint torque. In particular, reflexively-mediated stiffness generated a significant portion of the total joint stiffness and the percentage varied systematically with background muscle torque.

Endpoint Force Fluctuations Reveal Flexible Rather Than Synergistic Patterns of Muscle Cooperation

We developed a new approach to investigate how the nervous system activates multiple redundant muscles by studying the endpoint force fluctuations during isometric force generation at a multi-degree-of-freedom joint. We hypothesized that, due to signal-dependent muscle force noise, endpoint force fluctuations would depend on the target direction of index finger force and that this dependence could be used to distinguish flexible from synergistic activation of the musculature. We made high-gain measurements of isometric forces generated to different target magnitudes and directions, in the plane of index finger metacarpophalangeal joint abduction-adduction/flexion-extension. Force fluctuations from each target were used to calculate a covariance ellipse, the shape of which varied as a function of target direction. Directions with narrow ellipses were approximately aligned with the estimated mechanical actions of key muscles. For example, targets directed along the mechanical action of the first dorsal interosseous (FDI) yielded narrow ellipses, with 88% of the variance directed along those target directions. It follows the FDI is likely a prime mover in this target direction and that, at most, 12% of the force variance could be explained by synergistic coupling with other muscles. In contrast, other target directions exhibited broader covariance ellipses with as little as 30% of force variance directed along those target directions. This is the result of cooperation among multiple muscles, based on independent electromyographic recordings. However, the pattern of cooperation across target directions indicates that muscles are recruited flexibly in accordance with their mechanical action, rather than in fixed groupings.

In vivo human knee joint dynamic properties as functions of muscle contraction and joint position

Information on the dynamic properties (joint stiffness, viscosity and limb inertia) of the human knee joint is scarce in the literature, especially for actively contracting knee musculature. A joint driving device was developed to apply small-amplitude random perturbations to the human knee at several flexion angles with the subject maintaining various levels of muscle contraction. It was found that joint stiffness and viscosity increased with muscle contraction substantially, while limb inertia was constant. Stiffness produced by the quadriceps was highest at 30 degrees flexion and decreased with increasing or decreasing flexion angle, while knee flexors produced highest stiffness at 90 degree flexion. When knee flexion was < 60 degrees, stiffness produced by the quadriceps was higher than that of the hamstrings and gastrocnemius at the same level of background muscle torque, while knee flexor muscles produced higher stiffnesses than the quadriceps at 90 degree flexion. Similar but less obvious trends were observed for joint viscosity. Passive joint stiffness at full knee extension was significantly higher than in more flexed positions. Surprisingly, as the knee joint musculature changed from relaxed to contracting at 50% MVC, system damping ratio remained at about 0.2. This outcome potentially simplifies neuromuscular control of the knee joint. In contrast, the natural undamped frequency increased more than twofold, potentially making the knee joint respond more quickly to the central nervous system commands. The approach described here provides us with a potentially valuable tool to quantify in vivo dynamic properties of normal and pathological human knee joints.

Alterations in upper limb muscle synergy structure in chronic stroke survivors

Previous studies in neurologically intact subjects have shown that motor coordination can be described by task-dependent combinations of a few muscle synergies, defined here as a fixed pattern of activation across a set of muscles. Arm function in severely impaired stroke survivors is characterized by stereotypical postural and movement patterns involving the shoulder and elbow. Accordingly, we hypothesized that muscle synergy composition is altered in severely impaired stroke survivors. Using an isometric force matching protocol, we examined the spatial activation patterns of elbow and shoulder muscles in the affected arm of 10 stroke survivors (Fugl-Meyer <25/66) and in both arms of six age-matched controls. Underlying muscle synergies were identified using non-negative matrix factorization. In both groups, muscle activation patterns could be reconstructed by combinations of a few muscle synergies (typically 4). We did not find abnormal coupling of shoulder and elbow muscles within individual muscle synergies. In stroke survivors, as in controls, two of the synergies were comprised of isolated activation of the elbow flexors and extensors. However, muscle synergies involving proximal muscles exhibited consistent alterations following stroke. Unlike controls, the anterior deltoid was coactivated with medial and posterior deltoids within the shoulder abductor/extensor synergy and the shoulder adductor/flexor synergy in stroke was dominated by activation of pectoralis major, with limited anterior deltoid activation. Recruitment of the altered shoulder muscle synergies was strongly associated with abnormal task performance. Overall, our results suggest that an impaired control of the individual deltoid heads may contribute to poststroke deficits in arm function.

The relation between Ashworth scores and neuromechanical measurements of spasticity following stroke

BackgroundSpasticity is a common impairment that follows stroke, and it results typically in functional loss. For this reason, accurate quantification of spasticity has both diagnostic and therapeutic significance. The most widely used clinical assessment of spasticity is the modified Ashworth scale (MAS), an ordinal scale, but its validity, reliability and sensitivity have often been challenged. The present study addresses this deficit by examining whether quantitative measures of neural and muscular components of spasticity are valid, and whether they are strongly correlated with the MAS.MethodsWe applied abrupt small amplitude joint stretches and Pseudorandom Binary Sequence (PRBS) perturbations to both paretic and non-paretic elbow and ankle joints of stroke survivors. Using advanced system identification techniques, we quantified the dynamic stiffness of these joints, and separated its muscular (intrinsic) and reflex components. The correlations between these quantitative measures and the MAS were investigated.ResultsWe showed that our system identification technique is valid in characterizing the intrinsic and reflex stiffness and predicting the overall net torque. Conversely, our results reveal that there is no significant correlation between muscular and reflex torque/stiffness and the MAS magnitude. We also demonstrate that the slope and intercept of reflex and intrinsic stiffnesses plotted against the joint angle are not correlated with the MAS.ConclusionLack of significant correlation between our quantitative measures of stroke effects on spastic joints and the clinical assessment of muscle tone, as reflected in the MAS suggests that the MAS does not provide reliable information about the origins of the torque change associated with spasticity, or about its contributing components.

Exposure to Acute Intermittent Hypoxia Augments Somatic Motor Function in Humans With Incomplete Spinal Cord Injury

Background. Neural plasticity may contribute to motor recovery following spinal cord injury (SCI). In rat models of SCI with respiratory impairment, acute intermittent hypoxia (AIH) strengthens synaptic inputs to phrenic motor neurons, thereby improving respiratory function by a mechanism known as respiratory long-term facilitation. Similar intermittent hypoxia-induced facilitation may be feasible in somatic motor pathways in humans. Objective. Using a randomized crossover design, the authors tested the hypothesis that AIH increases ankle strength in people with incomplete SCI. Methods. Ankle strength was measured in 13 individuals with chronic, incomplete SCI before and after AIH. Voluntary ankle strength was estimated using changes in maximum isometric ankle plantar flexion torque generation and plantar flexor electromyogram activity following 15 low oxygen exposures (Fio2 = 0.09, 1-minute intervals). Results were compared with trials where subjects received sham exposure to room air. Results. AIH increased plantar flexion torque by 82 ± 33% (P < .003) immediately following AIH and was sustained above baseline for more than 90 minutes (P < .007). Increased ankle plantar flexor electromyogram activity (P = .01) correlated with increased torque (r2 = .5; P < .001). No differences in plantar flexion strength or electromyogram activity were observed in sham experiments. Conclusions. AIH elicits sustained increases in volitional somatic motor output in persons with chronic SCI. Thus, AIH has promise as a therapeutic tool to induce plasticity and enhance motor function in SCI patients.

Daily intermittent hypoxia enhances walking after chronic spinal cord injury A randomized trial

Objectives: To test the hypothesis that daily acute intermittent hypoxia (dAIH) and dAIH combined with overground walking improve walking speed and endurance in persons with chronic incomplete spinal cord injury (iSCI). Methods: Nineteen subjects completed the randomized, double-blind, placebo-controlled, crossover study. Participants received 15, 90-second hypoxic exposures (dAIH, fraction of inspired oxygen [Fio2] = 0.09) or daily normoxia (dSHAM, Fio2 = 0.21) at 60-second normoxic intervals on 5 consecutive days; dAIH was given alone or combined with 30 minutes of overground walking 1 hour later. Walking speed and endurance were quantified using 10-Meter and 6-Minute Walk Tests. The trial is registered at ClinicalTrials.gov (NCT01272349). Results: dAIH improved walking speed and endurance. Ten-Meter Walk time improved with dAIH vs dSHAM after 1 day (mean difference [MD] 3.8 seconds, 95% confidence interval [CI] 1.1–6.5 seconds, p = 0.006) and 2 weeks (MD 3.8 seconds, 95% CI 0.9–6.7 seconds, p = 0.010). Six-Minute Walk distance increased with combined dAIH + walking vs dSHAM + walking after 5 days (MD 94.4 m, 95% CI 17.5–171.3 m, p = 0.017) and 1-week follow-up (MD 97.0 m, 95% CI 20.1–173.9 m, p = 0.014). dAIH + walking increased walking distance more than dAIH after 1 day (MD 67.7 m, 95% CI 1.3–134.1 m, p = 0.046), 5 days (MD 107.0 m, 95% CI 40.6–173.4 m, p = 0.002), and 1-week follow-up (MD 136.0 m, 95% CI 65.3–206.6 m, p < 0.001). Conclusions: dAIH ± walking improved walking speed and distance in persons with chronic iSCI. The impact of dAIH is enhanced by combination with walking, demonstrating that combinatorial therapies may promote greater functional benefits in persons with iSCI. Classification of evidence: This study provides Class I evidence that transient hypoxia (through measured breathing treatments), along with overground walking training, improves walking speed and endurance after iSCI.

Assessing dexterity function: A comparison of two alternatives for the NIH toolbox

STUDY DESIGN Clinical measurement. INTRODUCTION Manual dexterity is an important aspect of motor function across the age span. PURPOSE OF THE STUDY To identify a single measure of manual dexterity for inclusion in the National Institutes of Health (NIH) Toolbox Assessment of Neurological and Behavioral Function. METHODS A total of 340 subjects participated in our study. Two alternatives, Rolyan® 9-Hole Peg Test (9-HPT) and Grooved Pegboard test, were compared by assessing their score range across age groups (3-85 yr) and their test-retest reliability, concurrent, and known groups validity. RESULTS The 9-HPT was a simple, efficient, and low-cost measure of manual dexterity appropriate for administration across the age range. Test-retest reliability coefficients were 0.95 and 0.92 for right and left hands, respectively. The 9-HPT correlated with Bruininks-Oseretsky Test (BOT) of Motor Proficiency, dexterity subscale, at -0.87 to -0.89 and with Purdue Pegboard at -0.74 to -0.75. The Grooved Pegboard had good test-retest reliability (0.91 and 0.85 for right and left hands, respectively). The Grooved Pegboard correlated with BOT at -0.50 to -0.63 and with Purdue Pegboard at -0.73 to -0.78. However, the Grooved Pegboard required longer administration time and was challenging for the youngest children and oldest adults. CONCLUSIONS Based on its feasibility and measurement properties, the 9-HPT was recommended for inclusion in the motor battery of the NIH Toolbox. LEVEL OF EVIDENCE NA.

Development of the MACARM - a novel cable robot for upper limb neurorehabilitation

This paper describes the design and operation of the multi-axis cartesian-based arm rehabilitation machine (MACARM), a new cable (wire) robot for upper limb rehabilitation. The prototype configuration is comprised of an array of 8 motors mounted at the corners of a cubic support frame that provides, via cables, 6 degree of freedom (DOF) control of a centrally located end-effector. A 6 DOF load cell mounted on the end-effector provides force measurement. Given its relatively simple architecture, the MACARM may provide an attractive alternative to serial robots for use in neurorehabilitation.

Robustness of muscle synergies underlying three-dimensional force generation at the hand in healthy humans

Previous studies using advanced matrix factorization techniques have shown that the coordination of human voluntary limb movements may be accomplished using combinations of a small number of intermuscular coordination patterns, or muscle synergies. However, the potential use of muscle synergies for isometric force generation has been evaluated mostly using correlational methods. The results of such studies suggest that fixed relationships between the activations of pairs of muscles are relatively rare. There is also emerging evidence that the nervous system uses independent strategies to control movement and force generation, which suggests that one cannot conclude a priori that isometric force generation is accomplished by combining muscle synergies, as shown in movement control. In this study, we used non-negative matrix factorization to evaluate the ability of a few muscle synergies to reconstruct the activation patterns of human arm muscles underlying the generation of three-dimensional (3-D) isometric forces at the hand. Surface electromyographic (EMG) data were recorded from eight key elbow and shoulder muscles during 3-D force target-matching protocols performed across a range of load levels and hand positions. Four synergies were sufficient to explain, on average, 95% of the variance in EMG datasets. Furthermore, we found that muscle synergy composition was conserved across biomechanical task conditions, experimental protocols, and subjects. Our findings are consistent with the view that the nervous system can generate isometric forces by assembling a combination of a small number of muscle synergies, differentially weighted according to task constraints.