Effects of spinal cord injury-induced changes in muscle activation on foot drag in a computational rat ankle model.

Spinal cord injury (SCI) can lead to changes in muscle activation patterns and atrophy of affected muscles. Moderate levels of SCI are typically associated with foot drag during the swing phase of locomotion. Foot drag is often used to assess locomotor recovery, but the causes remain unclear. We hypothesized that foot drag results from inappropriate muscle coordination preventing flexion at the stance-to-swing transition. To test this hypothesis and to assess the relative contributions of neural and muscular changes on foot drag, we developed a two-dimensional, one degree of freedom ankle musculoskeletal model with gastrocnemius and tibialis anterior muscles. Anatomical data collected from sham-injured and incomplete SCI (iSCI) female Long-Evans rats as well as physiological data from the literature were used to implement an open-loop muscle dynamics model. Muscle insertion point motion was calculated with imposed ankle trajectories from kinematic analysis of treadmill walking in sham-injured and iSCI animals. Relative gastrocnemius deactivation and tibialis anterior activation onset times were varied within physiologically relevant ranges based on simplified locomotor electromyogram profiles. No-atrophy and moderate muscle atrophy as well as normal and injured muscle activation profiles were also simulated. Positive moments coinciding with the transition from stance to swing phase were defined as foot swing and negative moments as foot drag. Whereas decreases in activation delay caused by delayed gastrocnemius deactivation promote foot drag, all other changes associated with iSCI facilitate foot swing. Our results suggest that even small changes in the ability to precisely deactivate the gastrocnemius could result in foot drag after iSCI.

Compensations for increased rotational inertia during human cutting turns.

Locomotion in a complex environment is often not steady state, but unsteady locomotion (stability and maneuverability) is not well understood. We investigated the strategies used by humans to perform sidestep cutting turns when running. Previous studies have argued that because humans have small yaw rotational moments of inertia relative to body mass, deceleratory forces in the initial velocity direction that occur during the turning step, or 'braking' forces, could function to prevent body over-rotation during turns. We tested this hypothesis by increasing body rotational inertia and testing whether braking forces during stance decreased. We recorded ground reaction force and body kinematics from seven participants performing 45 deg sidestep cutting turns and straight running at five levels of body rotational inertia, with increases up to fourfold. Contrary to our prediction, braking forces remained consistent at different rotational inertias, facilitated by anticipatory changes to body rotational speed. Increasing inertia revealed that the opposing effects of several turning parameters, including rotation due to symmetrical anterior-posterior forces, result in a system that can compensate for fourfold changes in rotational inertia with less than 50% changes to rotational velocity. These results suggest that in submaximal effort turning, legged systems may be robust to changes in morphological parameters, and that compensations can involve relatively minor adjustments between steps to change initial stance conditions.

Axon regeneration can facilitate or suppress hindlimb function after olfactory ensheathing glia transplantation.

Reports based primarily on anatomical evidence suggest that olfactory ensheathing glia (OEG) transplantation promotes axon regeneration across a complete spinal cord transection in adult rats. Based on functional, electrophysiological, and anatomical assessments, we found that OEG promoted axon regeneration across a complete spinal cord transection and that this regeneration altered motor responses over time. At 7 months after transection, 70% of OEG-treated rats showed motor-evoked potentials in hindlimb muscles after transcranial electric stimulation. Furthermore, a complete spinal cord retransection performed 8 months after injury demonstrated that this axon regeneration suppressed locomotor performance and decreased the hypersensitive hindlimb withdrawal response to mechanical stimulation. OEG transplantation alone promoted reorganization of lumbosacral locomotor networks and, when combined with long-term training, enhanced some stepping measures. These novel findings demonstrate that OEG promote regeneration of mature axons across a complete transection and reorganization of spinal circuitry, both of which contribute to sensorimotor function.

Correction: Finger Muscle Attachments for an OpenSim Upper-Extremity Model.

[This corrects the article DOI: 10.1371/journal.pone.0121712.].

Unconstrained three-dimensional reaching in rhesus monkeys.

To better understand normative behavior for quantitative evaluation of motor recovery after injury, we studied arm movements by non-injured rhesus monkeys during a food-retrieval task. While seated, monkeys reached, grasped, and retrieved food items. We recorded three-dimensional kinematics and muscle activity, and used inverse dynamics to calculate joint moments due to gravity, segmental interactions, and to the muscles and tissues of the arm. Endpoint paths showed curvature in three dimensions, suggesting that maintaining straight paths was not an important constraint. Joint moments were dominated by gravity. Generalized muscle and interaction moments were less than half of the gravitational moments. The relationships between shoulder and elbow resultant moments were linear during both reach and retrieval. Although both reach and retrieval required elbow flexor moments, an elbow extensor (triceps brachii) was active during both phases. Antagonistic muscles of both the elbow and hand were co-activated during reach and retrieval. Joint behavior could be described by lumped-parameter models analogous to torsional springs at the joints. Minor alterations to joint quasi-stiffness properties, aided by interaction moments, result in reciprocal movements that evolve under the influence of gravity. The strategies identified in monkeys to reach, grasp, and retrieve items will allow the quantification of prehension during recovery after a spinal cord injury and the effectiveness of therapeutic interventions.

OEG implantation and step training enhance hindlimb-stepping ability in adult spinal transected rats.

Numerous treatment strategies for spinal cord injury seek to maximize recovery of function and two strategies that show substantial promise are olfactory bulb-derived olfactory ensheathing glia (OEG) transplantation and treadmill step training. In this study we re-examined the issue of the effectiveness of OEG implantation but used objective, quantitative measures of motor performance to test if there is a complementary effect of long-term step training and olfactory bulb-derived OEG implantation. We studied complete mid-thoracic spinal cord transected adult female rats and compared four experimental groups: media-untrained, media-trained, OEG-untrained and OEG-trained. To assess the extent of hindlimb locomotor recovery at 4 and 7 months post-transection we used three quantitative measures of stepping ability: plantar stepping performance until failure, joint movement shape and movement frequency compared to sham controls. OEG transplantation alone significantly increased the number of plantar steps performed at 7 months post-transection, while training alone had no effect at either time point. Only OEG-injected rats plantar placed their hindpaws for more than two steps by the 7-month endpoint of the study. OEG transplantation combined with training resulted in the highest percentage of spinal rats per group that plantar stepped, and was the only group to significantly improve its stepping abilities between the 4- and 7-month evaluations. Additionally, OEG transplantation promoted tissue sparing at the transection site, regeneration of noradrenergic axons and serotonergic axons spanning the injury site. Interestingly, the caudal stump of media- and OEG-injected rats contained a similar density of serotonergic axons and occasional serotonin-labelled interneurons. These data demonstrate that olfactory bulb-derived OEG transplantation improves hindlimb stepping in paraplegic rats and further suggest that task-specific training may enhance this OEG effect.

Maneuvers during legged locomotion.

Maneuverability is essential for locomotion. For animals in the environment, maneuverability is directly related to survival. For humans, maneuvers such as turning are associated with increased risk for injury, either directly through tissue loading or indirectly through destabilization. Consequently, understanding the mechanics and motor control of maneuverability is a critical part of locomotion research. We briefly review the literature on maneuvering during locomotion with a focus on turning in bipeds. Walking turns can use one of several different strategies. Anticipation can be important to adjust kinematics and dynamics for smooth and stable maneuvers. During running, turns may be substantially constrained by the requirement for body orientation to match movement direction at the end of a turn. A simple mathematical model based on the requirement for rotation to match direction can describe leg forces used by bipeds (humans and ostriches). During running turns, both humans and ostriches control body rotation by generating fore-aft forces. However, whereas humans must generate large braking forces to prevent body over-rotation, ostriches do not. For ostriches, generating the lateral forces necessary to change movement direction results in appropriate body rotation. Although ostriches required smaller braking forces due in part to increased rotational inertia relative to body mass, other movement parameters also played a role. Turning performance resulted from the coordinated behavior of an integrated biomechanical system. Results from preliminary experiments on horizontal-plane stabilization support the hypothesis that controlling body rotation is an important aspect of stable maneuvers. In humans, body orientation relative to movement direction is rapidly stabilized during running turns within the minimum of two steps theoretically required to complete analogous maneuvers. During straight running and cutting turns, humans exhibit spring-mass behavior in the horizontal plane. Changes in the horizontal projection of leg length were linearly related to changes in horizontal-plane leg forces. Consequently, the passive dynamic stabilization associated with spring-mass behavior may contribute to stability during maneuvers in bipeds. Understanding the mechanics of maneuverability will be important for understanding the motor control of maneuvers and also potentially be useful for understanding stability.

Changes in motoneuron properties and synaptic inputs related to step training after spinal cord transection in rats.

Although recovery from spinal cord injury is generally meager, evidence suggests that step training can improve stepping performance, particularly after neonatal spinal injury. The location and nature of the changes in neural substrates underlying the behavioral improvements are not well understood. We examined the kinematics of stepping performance and cellular and synaptic electrophysiological parameters in ankle extensor motoneurons in nontrained and treadmill-trained rats, all receiving a complete spinal transection as neonates. For comparison, electrophysiological experiments included animals injured as young adults, which are far less responsive to training. Recovery of treadmill stepping was associated with significant changes in the cellular properties of motoneurons and their synaptic input from spinal white matter [ipsilateral ventrolateral funiculus (VLF)] and muscle spindle afferents. A strong correlation was found between the effectiveness of step training and the amplitude of both the action potential afterhyperpolarization and synaptic inputs to motoneurons (from peripheral nerve and VLF). These changes were absent if step training was unsuccessful, but other spinal projections, apparently inhibitory to step training, became evident. Greater plasticity of axonal projections after neonatal than after adult injury was suggested by anatomical demonstration of denser VLF projections to hindlimb motoneurons after neonatal injury. This finding confirmed electrophysiological measurements and provides a possible mechanism underlying the greater training susceptibility of animals injured as neonates. Thus, we have demonstrated an "age-at-injury"-related difference that may influence training effectiveness, that successful treadmill step training can alter electrophysiological parameters in the transected spinal cord, and that activation of different pathways may prevent functional improvement.

Dose dependence of the 5-HT agonist quipazine in facilitating spinal stepping in the rat with epidural stimulation.

Epidural electrical stimulation (ES) at spinal cord segment L2 can produce coordinated step-like movements in completely spinalized adult rats [R.M. Ichiyama, Y.P. Gerasimenko, H. Zhong, R.R. Roy, V.R. Edgerton, Hindlimb stepping movements in complete spinal rats induced by epidural spinal cord stimulation, Neurosci. Lett. 383 (2005) 339-344]. Plantar placement of the paws, however, was rarely observed. Here, we sought to determine the dose dependence of a 5-HT agonist (quipazine) on stepping kinematics when administered in combination with ES. Six adult female Sprague-Dawley rats received a complete mid-thoracic spinal cord transection and were implanted with epidural electrodes at the L2 spinal cord level. Quipazine (i.p.) was tested at doses of 0.1, 0.2, 0.3, 0.4, and 0.5 mg/kg. Rats were placed in a body weight support system, allowing them to walk bipedally on a moving treadmill belt (7 cm/s). 3D step kinematics analysis revealed that coordinated alternating bilateral stepping was induced by L2 stimulation (50 Hz) alone and by quipazine alone. Furthermore, the combination treatment produced significantly greater numbers of plantar steps and improved quality of stepping compared to either intervention alone. Both number and quality of stepping peaked at the intermediate dose of 0.3-0.4 mg/kg. The results indicate that quipazine and ES can have complementary effects on spinal circuits and that quipazine dosage is an important factor in differentially modulating these circuitries to improve the quality of the bipedal stepping on a treadmill belt.

A three-dimensional model of the rat hindlimb: musculoskeletal geometry and muscle moment arms.

As a first step towards developing a dynamic model of the rat hindlimb, we measured muscle attachment and joint center coordinates relative to bony landmarks using stereophotogrammetry. Using these measurements, we analyzed muscle moment arms as functions of joint angle for most hindlimb muscles, and tested the hypothesis that postural change alone is sufficient to alter the function of selected muscles of the leg. We described muscle attachment sites as second-order curves. The length of the fit parabola and residual errors in the orthogonal directions give an estimate of muscle attachment sizes, which are consistent with observations made during dissection. We modeled each joint as a moving point dependent on joint angle; relative endpoint errors less than 7% indicate this method as accurate. Most muscles have moment arms with a large range across the physiological domain of joint angles, but their moment arms peak and vary little within the locomotion domain. The small variation in moment arms during locomotion potentially simplifies the neural control requirements during this phase. The moment arms of a number of muscles cross zero as angle varies within the quadrupedal locomotion domain, indicating they are intrinsically stabilizing. However, in the bipedal locomotion domain, the moment arms of these muscles do not cross zero and thus are no longer intrinsically stabilizing. We found that muscle function is largely determined by the change in moment arm with joint angle, particularly the transition from quadrupedal to bipedal posture, which may alter an intrinsically stabilizing arrangement or change the control burden.

Index finger and thumb kinematics and performance measurements for common touchscreen gestures.

This study aimed to quantify differences in 7 touchscreen gestures. Eighteen participants performed index finger tapping, sliding in 4 orthogonal directions, and index finger and thumb pinch and stretch gestures on a touchscreen tablet computer. We hypothesized that two finger gestures would require longer task completion time and greater finger joint excursions than sliding gestures using only the index finger. We measured task completion times and finger joint kinematics. Tapping showed the fastest average (±SD) task completion time, 567(190) ms, of all gestures (p < 0.001). Pinch had faster task completion time, 765(277) ms, than all single-finger sliding gestures (p < 0.001). Stretch was faster to complete at 843(317) ms (p < 0.001) than all sliding gestures except slide right. Stretch demonstrated greater mean index finger metacarpophalangeal flexion/extension joint excursions, 63(16)°, compared to sliding gestures, 34(10)°, and tapping, 27(13)° (p < 0.01). Overall, two-finger gestures were faster to complete and showed greater joint excursions than single-finger sliding gestures.

A model for differential leg joint function during human running.

Locomotion requires coordination of leg joints to maintain stability and to maneuver. We studied leg joint function during constant-average-velocity running and the sagittal-plane maneuvers of step ascent and descent. We tested two hypotheses: (1) that leg joints perform distinct functions during locomotion; and (2) that humans select functional parameters to maximize intrinsic dynamic stability. We recorded whole-body kinematics and forces when participants stepped up or down a single vertical step, and found that leg joints show functional differences during both constant-average-velocity locomotion and maneuvers. The hip, knee and ankle function as a motor, damper, and spring, respectively. We therefore constructed a simplified computational model of a human leg with a motor, damper, and spring in series (MDS). The intrinsic dynamics of the model resulted in sustained locomotion on level ground within narrow parameter ranges. However, using parameters experimentally derived from humans, the model showed only short-term stability. Humans may not optimize intrinsic dynamic stability alone, but may instead choose mechanical and behavioral parameters appropriate for both constant-average-velocity locomotion and maneuvers. Understanding joint-level mechanical function during unsteady locomotion helps to understand how differential joint function contributes to whole-body performance, and could lead to improvements in rehabilitation, prosthetic and robotic design.

Fingertip forces and completion time for index finger and thumb touchscreen gestures.

Users actuate touchscreen computers by applying forces with their fingers to the touchscreen, although the amount and direction of the force is unknown. Our aim was to characterize the magnitude, direction and impulse of the force applied during single finger (tapping and sliding in four directions) and two finger gestures (stretch and pinch). Thirteen subjects performed repeated trials of each gesture. Mean(±SD) resultant force was 0.50(0.09)N for tap, 0.79(0.32)N to 1.18(0.47)N for sliding gestures, 1.47(0.63)N for pinch and 2.05(1.13)N for stretch. Mean resultant force was significantly less (p<0.04) for tap than for all gestures except slide right. The direction of force application was more vertical for the two-finger gestures as compared to the single- finger gestures. Tap was the fastest gesture to complete at 133(83)ms, followed by slide right at 421(181)ms. On average, participants took the longest to complete the stretch gesture at 920(398)ms. Overall, there are differences in forces, force direction, and completion times among touchscreen gestures that could be used to estimate musculoskeletal exposure and help forge guidelines to reduce risk of musculoskeletal injury.

A hypothesis for the function of braking forces during running turns.

We examined the functional role of braking forces observed when humans execute turning maneuvers. Deceleration caused by braking forces contributes to changing the movement direction of the center of mass (COM) and maintaining constant velocity. We argue that braking forces also prevent over-rotation of the body about the vertical axis during maneuvers. We analyzed data from sidestep and crossover cuts at average initial running velocities of 3 m s(-1). Absent braking, lateral forces would result in body rotations 1.4-3 times the change in COM movement direction, causing the orientation of the body to be substantially mis-aligned with the direction of movement at the end of the step. A simple model based on the hypothesis that body rotation should match COM deflection can explain 70% of the variance in braking forces employed during running turns.

Finger joint coordination during tapping.

We investigated finger joint coordination during tapping by characterizing joint kinematics and torques in terms of muscle activation patterns and energy profiles. Six subjects tapped with their index finger on a computer keyswitch as if they were typing on the middle row of a keyboard. Fingertip force, keyswitch position, kinematics of the metacarpophalangeal (MCP) and the proximal and distal interphalangeal (IP) joints, and intramuscular electromyography of intrinsic and extrinsic finger muscles were measured simultaneously. Finger joint torques were calculated based on a closed-form Newton-Euler inverse dynamic model of the finger. During the keystroke, the MCP joint flexed and the IP joints extended before and throughout the loading phase of the contact period, creating a closing reciprocal motion of the finger joints. As the finger lifted, the MCP joint extended and the interphalangeal (IP) joints flexed, creating an opening reciprocal motion. Intrinsic finger muscle and extrinsic flexor activities both began after the initiation of the downward finger movement. The intrinsic finger muscle activity preceded both the IP joint extension and the onset of extrinsic muscle activity. Only extrinsic extensor activity was present as the finger was lifted. While both potential energy and kinetic energy are present and large enough to overcome the work necessary to press the keyswitch, the motor control strategies utilize the muscle forces and joint torques to ensure a successful keystroke.

Leg joint function during walking acceleration and deceleration.

Although constant-average-velocity walking has been extensively studied, less is known about walking maneuvers that change speed. We investigated the function of individual leg joints when humans walked at a constant speed, accelerated or decelerated. We hypothesized that leg joints make different functional contributions to maneuvers. Specifically, we hypothesized that the hip generates positive mechanical work (acting like a "motor"), the knee generates little mechanical work (acting like a "strut"), and the ankle absorbs energy during the first half of stance and generates energy during the second half (consistent with "spring"-like function). We recorded full body kinematics and kinetics, used inverse dynamics to estimate net joint moments, and decomposed joint function into strut-, motor-, damper-, and spring-like components using indices based on net joint work. Although overall leg mechanics were primarily strut-like, individual joints did not act as struts during stance. The hip functioned as a power generating "motor," and ankle function was consistent with spring-like behavior. Even though net knee work was small, the knee did not behave solely as a strut but also showed motor-, and damper-like function. Acceleration involved increased motor-like function of the hip and ankle. Deceleration involved decreased hip motor-like function and ankle spring-like function and increased damping at the knee and ankle. Changes to joint mechanical work were primarily due to changes in joint angular displacements and not net moments. Overall, joints maintain different functional roles during unsteady locomotion.

Two-handed grip on a mobile phone affords greater thumb motor performance, decreased variability, and a more extended thumb posture than a one-handed grip.

Holding a mobile computing device with two hands may affect thumb motor performance, joint postures, and device stability compared to holding the device and tapping the touchscreen with the thumb of the holding hand. We tested the hypotheses that holding a touchscreen mobile phone with two hands lead to increased thumb motor performance, different thumb postures, and decreased device movement relative to using one hand. Ten right-handed participants completed reciprocal thumb tapping tasks between emulated keys on a smartphone in either a one- (portrait) or two-handed (landscape) grip configuration. Effective index of performance measured from Fitts' Law was 9% greater (p < 0.001), movement time 7% faster (p < 0.001), and taps were 4% more precise (p < 0.016) for the two-handed grip. Tapping with a two-handed grip involved significantly different wrist and thumb postures than a one-handed grip. Variability of the computing device's movement was 36-63% lower for the two-handed grip compared to the one-handed grip condition (p < 0.001). The support for our hypotheses suggests that a two-handed grip results in increased performance and more extended wrist and thumb postures than a single-handed grip. Device designs that allow two-handed grips may afford increased performance relative to a one-handed grip.

Extrinsic and intrinsic index finger muscle attachments in an OpenSim upper-extremity model.

Musculoskeletal models allow estimation of muscle function during complex tasks. We used objective methods to determine possible attachment locations for index finger muscles in an OpenSim upper-extremity model. Data-driven optimization algorithms, Simulated Annealing and Hook-Jeeves, estimated tendon locations crossing the metacarpophalangeal (MCP), proximal interphalangeal (PIP) and distal interphalangeal (DIP) joints by minimizing the difference between model-estimated and experimentally-measured moment arms. Sensitivity analysis revealed that multiple sets of muscle attachments with similar optimized moment arms are possible, requiring additional assumptions or data to select a single set of values. The most smooth muscle paths were assumed to be biologically reasonable. Estimated tendon attachments resulted in variance accounted for (VAF) between calculated moment arms and measured values of 78% for flex/extension and 81% for ab/adduction at the MCP joint. VAF averaged 67% at the PIP joint and 54% at the DIP joint. VAF values at PIP and DIP joints partially reflected the constant moment arms reported for muscles about these joints. However, all moment arm values found through optimization were non-linear and non-constant. Relationships between moment arms and joint angles were best described with quadratic equations for tendons at the PIP and DIP joints.

Finger muscle attachments for an OpenSim upper-extremity model.

We determined muscle attachment points for the index, middle, ring and little fingers in an OpenSim upper-extremity model. Attachment points were selected to match both experimentally measured locations and mechanical function (moment arms). Although experimental measurements of finger muscle attachments have been made, models differ from specimens in many respects such as bone segment ratio, joint kinematics and coordinate system. Likewise, moment arms are not available for all intrinsic finger muscles. Therefore, it was necessary to scale and translate muscle attachments from one experimental or model environment to another while preserving mechanical function. We used a two-step process. First, we estimated muscle function by calculating moment arms for all intrinsic and extrinsic muscles using the partial velocity method. Second, optimization using Simulated Annealing and Hooke-Jeeves algorithms found muscle-tendon paths that minimized root mean square (RMS) differences between experimental and modeled moment arms. The partial velocity method resulted in variance accounted for (VAF) between measured and calculated moment arms of 75.5% on average (range from 48.5% to 99.5%) for intrinsic and extrinsic index finger muscles where measured data were available. RMS error between experimental and optimized values was within one standard deviation (S.D) of measured moment arm (mean RMS error = 1.5 mm < measured S.D = 2.5 mm). Validation of both steps of the technique allowed for estimation of muscle attachment points for muscles whose moment arms have not been measured. Differences between modeled and experimentally measured muscle attachments, averaged over all finger joints, were less than 4.9 mm (within 7.1% of the average length of the muscle-tendon paths). The resulting non-proprietary musculoskeletal model of the human fingers could be useful for many applications, including better understanding of complex multi-touch and gestural movements.

Non-linear viscoelastic models predict fingertip pulp force-displacement characteristics during voluntary tapping.

We evaluated whether lumped-parameter non-linear viscoelastic models of human fingertip tissue can describe fingertip force-displacement characteristics during a range of rapid, dynamic tapping tasks. Eight human subjects tapped with their index finger on the surface of a rigid load cell while an optical system tracked fingertip position using an infra-red LED attached to the fingernail. Four different tapping conditions were tested: normal and high-speed taps with a relaxed hand, and normal and high-speed taps with the other fingers co-contracted. A non-linear viscoelastic model comprised of an instantaneous stiffness function and viscous relaxation function was capable of predicting fingertip tissue force response due to measured pulp compression under these four different loading conditions. The model could successfully reconstruct very rapid (less than 5 ms) force transients, and forces occurring over time periods greater than 100 ms, with errors of 10%. Model parameters varied by less than 20% over the four conditions, despite almost 3-fold differences in average forces and 38% differences in fingertip velocities. Energy dissipation by the fingertip averaged 81%, and varied little (<3%) across conditions, despite a 1. 5-fold range of energy input. The ability of a lumped-parameter model to describe fingertip force-displacement characteristics during a range of conditions contributes both to understanding the transmission of force through the fingertip to the musculoskeletal system and to predicting the stimulation of mechano-receptors located within the fingertip.