Contribution of stretch reflexes to locomotor control: a modeling study

It is known that the springlike properties of muscles provide automatic load compensation during weight bearing. How crucial is sensory control of the motor output given these basic properties of the locomotor system? To address this question, a neuromuscular model was used to test two hypotheses. (1) Stretch reflexes are too weak and too delayed to contribute significantly to weight-bearing. (2) The important contributions of sensory input involve state-dependent processing. We constructed a two-legged planar locomotor model with 9 segments, driven by 12 musculotendon actuators with Hill-type force-velocity and monotonic force-length properties. Electromyographic (EMG) profiles of the simulated muscle groups during slow level walking served as actuator activation functions. Spindle Ia and tendon organ Ib sensory inputs were represented by transfer functions with a latency of 35 ms, contributing 30% to the net EMG profile and gated to be active only when the receptor-bearing muscles were contracting. Locomotor stability was assessed by parametric variations of actuator maximum forces during locomotion in open-loop ("deafferented") trials and in trials with feedback control based on either sensory-evoked stretch reflexes or finite-state rules. We arrived at the following conclusions. (1) In the absence of sensory control, the intrinsic stiffness of limb muscles driven by a stereotyped rhythmical pattern can produce surprisingly stable gait. (2) When the level of central activity is low, the contribution of stretch reflexes to load compensation can be crucial. However, when central activity provides adequate load compensation, the contribution of stretch reflexes is less significant. (3) Finite-state control can greatly extend the adaptive capability of the locomotor system.     

Paraspinal muscle reflex dynamics

Neuromuscular control of spinal stability may be represented as a control system wherein the paraspinal muscle reflex acts as feedback response to kinetic and kinematic disturbances of the trunk. The influence of preparatory muscle recruitment for the control of spinal stability has been previously examined, but there are few reported studies that characterize paraspinal reflex gain as feedback response. In the current study, the input-output dynamics of paraspinal reflexes were quantified by means of the impulse response function (IRF), with trunk perturbation force representing the input signal and EMG the output signal. Surface EMGs were collected from the trunk muscles in response to a brief anteriorly directed impact force applied to the trunk of healthy participants. Reflex behavior was measured in response to three levels of force impulse, 6.1, 9.2 and 12.0 Ns, and two different levels of external trunk flexion preload, 0 and 110 N anterior force. Reflex EMG was quantifiable in response to 91% of the perturbations. Mean reflex onset latency was 30.7+/-21.3 ms and reflex amplitude increased with perturbation amplitude. Impulse response function gain, G(IRF), was defined as the peak amplitude of the measured IRF and provided a consistent measure of response behavior. EMG reflex amplitude and G(IRF) increased with force impulse. Mean G(IRF) was 2.27+/-1.31% MVC/Ns and demonstrated declining trend with flexion preload. Results agree with a simple systems model of the neuromechanical feedback behavior. The relative contribution of the reflex dynamics to spinal stability must be investigated in future research.     

Ankle extensor proprioceptors contribute to the enhancement of the soleus EMG during the stance phase of human walking

A rapid plantar flexion perturbation applied to the ankle during the stance phase of the step cycle during human walking unloads the ankle extensors and produces a marked decline in the soleus EMG. This demonstrates that sensory activity contributes importantly to the enhancement of the ankle extensor muscle activation during human walking. On average, the EMG begins to decline approximately 52 ms after the perturbation. In contrast, a rapid dorsi flex ion perturbation produces a group Ia mediated short-latency stretch reflex burst with an onset latency of approximately 36 ms. The transmission of sensory traffic from the foot and ankle was suppressed in 10 subjects by an anaesthetic nerve block produced with local injections of lidocaine hydrochloride. The anaesthetic block had no effect on the stance phase soleus EMG, the latencies of the EMG responses, or the magnitude of the EMG decline following the plantar flexion perturbation. Therefore, it is more likely that proprioceptive afferents, rather than cutaneous afferents, contribute to the background soleus EMG during the late stance phase of the step cycle. The large difference in onset latencies between the short-latency reflex and unload responses suggests that the largest of the active group Ia afferents might not contribute strongly to the background soleus EMG, although it remains to be determined which of the proprioceptive pathways provide the more important contributions.     

Dynamical simulation of speech cooperative articulation by muscle linkages

Different kinds of articulators, such as the upper and lower lips, jaw, and tongue, are precisely coordinated in speech production. Based on a perturbation study of the production of a fricative consonant using the upper and lower lips, it has been suggested that increasing the stiffness in the muscle linkage between the upper lip and jaw is beneficial for maintaining the constriction area between the lips (Gomi et al. 2002). This hypothesis is crucial for examining the mechanism of speech motor control, that is, whether mechanical impedance is controlled for the speech motor coordination. To test this hypothesis, in the current study we performed a dynamical simulation of lip compensatory movements based on a muscle linkage model and then evaluated the performance of compensatory movements. The temporal pattern of stiffness of muscle linkage was obtained from the electromyogram (EMG) of the orbicularis oris superior (OOS) muscle by using the temporal transformation (second-order dynamics with time delay) from EMG to stiffness, whose parameters were experimentally determined. The dynamical simulation using stiffness estimated from empirical EMG successfully reproduced the temporal profile of the upper lip compensatory articulations. Moreover, the estimated stiffness variation significantly contributed to reproduce a functional modulation of the compensatory response. This result supports the idea that the mechanical impedance highly contributes to organizing coordination among the lips and jaw. The motor command would be programmed not only to generate movement in each articulator but also to regulate mechanical impedance among articulators for robust coordination of speech motor control.     

Influences of experimental factors on spinal stretch reflex latency and amplitude in the human triceps surae.

The spinal stretch reflex (SSR) is commonly assessed via electromyographic (EMG) analysis of joint perturbations inducing changes in muscle length. Previous literature indicates that when large experimental changes in magnitude of agonist background EMG, perturbation velocity, and perturbation amplitude are employed, SSR latency and amplitude are significantly altered. The purpose of this investigation was to evaluate the relative dependence of SSR latency and amplitude on inherent variability in these experimental variables. Soleus SSR latency and amplitude were assessed in 40 healthy subjects following dorsiflexion perturbation under an active state ( approximately 14% MVC). Experimental variables displayed limited variability (means +/- SD): soleus background EMG (13.47 +/- 7.08% MVC), perturbation velocity (96.1 +/- 30 degrees /s), and perturbation amplitude (4 +/- 1 degrees ). SSR latency was not significantly related to soleus background EMG (r = 0.189), perturbation velocity (r = 0.213), or perturbation amplitude (r = 0.202). Similarly, SSR amplitude was not significantly related to soleus background EMG (r = 0.306), perturbation velocity (r = 0.053), or perturbation amplitude (r = 0.056). Variability in experimental variables was much smaller than what has been reported in the literature to significantly impact SSR characteristics. These results suggest that SSR latency and amplitude are independent of agonist background EMG, perturbation velocity, and perturbation amplitude when experimental variability is relatively limited.     

Acute effects of whole body vibration on directionality and reaction time latency of trunk muscles: The importance of rest and implications for spine stability

Workplace exposure to whole body vibration (WBV) has been identified as one of the major physical risk factors encountered by the population. There are indications that, subsequent to a perturbation, impaired reflex response could allow for destabilization of the spine, possibly leading to injury. The purpose of this study was to investigate if WBV alters reflex response of trunk muscles and if the direction of perturbation (flexion or extension or lateral) and delay between exposure and perturbation influences the response. The results indicate that EMG latency was increased more in the vibration condition than in sitting without vibration. Significant effects with respect to directionality were observed in Erector Spinae muscles. The EMG latency reduced from the effect of perturbation after a 20 s rest period. Even though the EMG latency did not fully return to its Pre-test state, the present results still show that recovery from the acute effects of WBV is possible with a rest period.     

Lower-limb amputee recovery response to an imposed error in mediolateral foot placement

Despite walking with a wider step width, amputees remain 20% more likely to fall than non-amputees. Since mediolateral (ML) balance is critical for ambulation and contingent on ML foot placement, we used a ML disturbance to perturb walking balance and explore the influence of prosthetic foot stiffness on balance recovery. Ten transtibial amputees were fit with two commonly prescribed prosthetic feet with differing stiffness characteristics; 12 non-amputees also participated. A perturbation device that released an air burst just before heel strike imposed a repeatable medial or lateral disturbance in foot placement. After a medial disturbance, the first recovery step width was narrowed (p<0.0001) for the prosthetic limb (−103%), the sound limb (−51%) and non-amputees (−41%) and more than twice as variable. The ML inclination angle remained reduced (−109%) for the prosthetic limb, while the sound limb and non-amputees approached undisturbed levels (p<0.0004). Amputees required five steps to return to undisturbed step width after a prosthetic medial disturbance versus two steps for the sound limb and for non-amputees. After a lateral disturbance, the first recovery step was widened for the prosthetic limb (+82%), sound limb (+75%), and wider than non-amputees (+51%; p<0.0001), with all participants requiring three steps to return to undisturbed step width. Amputees also exhibited a similar upper torso response compared to the non-amputees for both disturbances. Prosthetic feet with different stiffness properties did not have a significant effect. In conclusion, amputee balance was particularly challenged by medial disturbances to the prosthetic limb implying a need for improved interventions that address these balance deficits.     

Selective lateral muscle activation in moderate medial knee osteoarthritis subjects does not unload medial knee condyle

There is some debate in the literature regarding the role of quadriceps-hamstrings co-contraction in the onset and progression of knee osteoarthritis. Does co-contraction during walking increase knee contact loads, thereby causing knee osteoarthritis, or might it be a compensatory mechanism to unload the medial tibial condyle? We used a detailed musculoskeletal model of the lower limb to test the hypothesis that selective activation of lateral hamstrings and quadriceps, in conjunction with inhibited medial gastrocnemius, can actually reduce the joint contact force on the medial compartment of the knee, independent of changes in kinematics or external forces. “Baseline” joint loads were computed for eight subjects with moderate medial knee osteoarthritis (OA) during level walking, using static optimization to resolve the system of muscle forces for each subject?s scaled model. Holding all external loads and kinematics constant, each subject?s model was then perturbed to represent non-optimal “OA-type” activation based on mean differences detected between electromyograms (EMG) of control and osteoarthritis subjects. Knee joint contact forces were greater for the “OA-type” than the “Baseline” distribution of muscle forces, particularly during early stance. The early-stance increase in medial contact load due to the “OA-type” perturbation could implicate this selective activation strategy as a cause of knee osteoarthritis. However, the largest increase in the contact load was found at the lateral condyle, and the “OA-type” lateral activation strategy did not increase the overall (greater of the first or second) medial peak contact load. While “OA-type” selective activation of lateral muscles does not appear to reduce the medial knee contact load, it could allow subjects to increase knee joint stiffness without any further increase to the peak medial contact load.     

Above- and below-lesion EMG pattern mapping for controlling electrical stimulation of paraplegics to facilitate unbraced walker-assisted walking

We describe and evaluate above- and below-lesion EMG control of functional electrical stimulation (FES) in upper motor neuron paraplegics, in order to provide them with a patient-responsive system for walking with a walker support. Control is considered in terms of a combination of above-lesion EMG control and below-lesion response-EMG control. The above-lesion EMG is used to control the activation of limb functions involved in standing up and walking with FES, control being accomplished by analysing raw surface-EMG time-series patterns to discriminate between upper-trunk muscle contraction patterns, which in turn, are correlated with intended lower-limb functions involved in walking, so that natural and instinctive balance changes in paraplegics are controlled by the patient from above the lesion. The below-lesion response-EMG is the EMG produced in response to the FES pulses at the stimulation sites, for adjusting stimulation levels as needed when contractions weaken due to muscle fatigue. Above-lesion EMG is a stochastic (random-like) signal, being a response to unsynchronized motor neuron firings, whereas the below-lesion EMG is a deterministic signal responding to synchronized firings that result solely from the FES pulses. We also discuss the merits and difficulties of EMG control, and evaluate patient performance under such control, noting that FES-activated walking without adequate and patient-responsive control is of very limited use to paraplegics.     

Slower Visuomotor Corrections with Unchanged Latency are Consistent with Optimal Adaptation to Increased Endogenous Noise in the Elderly

We analyzed age-related changes in motor response in a visuomotor compensatory tracking task. Subjects used a manipulandum to attempt to keep a displayed cursor at the center of a screen despite random perturbations to its location. Cross-correlation analysis of the perturbation and the subject response showed no age-related increase in latency until the onset of response to the perturbation, but substantial slowing of the response itself. Results are consistent with age-related deterioration in the ratio of signal to noise in visuomotor response. The task is such that it is tractable to use Bayesian and quadratic optimality assumptions to construct a model for behavior. This model assumes that behavior resembles an optimal controller subject to noise, and parametrizes response in terms of latency, willingness to expend effort, noise intensity, and noise bandwidth. The model is consistent with the data for all young (n = 12, age 20–30) and most elderly (n = 12, age 65–92) subjects. The model reproduces the latency result from the cross-correlation method. When presented with increased noise, the computational model reproduces the experimentally observed age-related slowing and the observed lack of increased latency. The model provides a precise way to quantitatively formulate the long-standing hypothesis that age-related slowing is an adaptation to increased noise.     

Influence of amplitude cancellation on the accuracy of determining the onset of muscle activity from the surface electromyogram

The purpose of the study was to quantify the influence of amplitude cancellation on the accuracy of detecting the onset of muscle activity based on an analysis of simulated surface electromyographic (EMG) signals. EMG activity of a generic lower limb muscle was simulated during the stance phase of human gait. Surface EMG signals were generated with and without amplitude cancellation by summing simulated motor unit potentials either before (cancellation EMG) or after (no-cancellation EMG) the potentials had been rectified. The two sets of EMG signals were compared at forces of 30% and 80% of maximum voluntary contraction (MVC) and with various low-pass filter cut-off frequencies. Onset time was determined both visually and by an algorithm that identified when the mean amplitude of the signal within a sliding window exceeded a specified standard deviation (SD) above the baseline mean. Onset error was greater for the no-cancellation conditions when determined automatically and by visual inspection. However, the differences in onset error between the two cancellation conditions appear to be clinically insignificant. Therefore, amplitude cancellation does not appear to limit the ability to detect the onset of muscle activity from the surface EMG.     

Locus of control and frontal electromyographic response training

Forty-eight normal subjects from a college population, representing extreme internal and external orientations on a locus of control scale, were provided an auditory signal in a laboratory relaxation setting. For one group (feedback) the pitch of the signal varied as a function of frontal electromyographic (EMG) levels, while for another group (control) the pitch was constant. The feedback subjects acquired lower EMG potentials than did the control subjects, and the internal subjects in the feedback condition acquired lower levels than did the external subjects. In the control condition, no consistent differences in EMG levels between internal and external subjects were obtained. These results were stable across two replications, three ethnically distinct groups, and both sexes. Additional measures designed to reflect the effects of the frontal EMG training as a generalized relaxation technique for this population, including finger temperatures and a variety of postexperiment questionnaire ratings of relaxation, yielded negative results. Tests of other predictions from the locus of control construct are also discussed.This research was supported by NIMH Special Postdoctoral Fellowship No. MH58202-01.     

Optimal control of antagonistic muscle stiffness during voluntary movements

This paper presents a study on the control of antagonist muscle stiffness during single-joint arm movements by optimal control theory with a minimal effort criterion. A hierarchical model is developed based on the physiology of the neuromuscular control system and the equilibrium point hypothesis. For point-to-point movements, the model provides predictions on (1) movement trajectory, (2) equilibrium trajectory, (3) muscle control inputs, and (4) antagonist muscle stiffness, as well as other variables. We compared these model predictions to the behavior observed in normal human subjects. The optimal movements capture the major invariant characteristics of voluntary movements, such as a sigmoidal movement trajectory with a bell-shaped velocity profile, an N-shaped equilibrium trajectory, a triphasic burst pattern of muscle control inputs, and a dynamically modulated joint stiffness. The joint stiffness is found to increase in the middle of the movement as a consequence of the triphasic muscle activities. We have also investigated the effects of changes in model parameters on movement control. We found that the movement kinematics and muscle control inputs are strongly influenced by the upper bound of the descending excitation signal that activates motoneuron pools in the spinal cord. Furthermore, a class of movements with scaled velocity profiles can be achieved by tuning the amplitude and duration of this excitation signal. These model predictions agree with a wide body of experimental data obtained from normal human subjects. The results suggest that the control of fast arm movements involves explicit planning for both the equilibrium trajectory and joint stiffness, and that the minimal effort criterion best characterizes the objective of movement planning and control.     

Principles for learning horizontal-planar arm movements with reversal

PurposeThis study tested the hypothesis that muscle and interaction torques can be altered independently in order to improve in specific kinematics performance observed following practice. We also tested the hypothesis that a simple set of rules of EMG-control and kinetic-control models could explain the EMG and kinetic changes due to practice of movements with reversal.ScopeKinematics of the upper arm with reversal, performed over three distances, was reconstructed using motion analysis. The muscle and interaction torques were calculated using inverse-dynamics. EMG activities of the major arm muscles were also recorded. The results demonstrate that improved performance is facilitated by an increase in muscle torque (and therefore acceleration) at the proximal joint (shoulder) and by an increase in the interaction torque at the distal joint (elbow). No changes were observed in the amount of muscle activity underlying these kinetic modifications, except for a decrease in the shoulder antagonist latency.ConclusionThe results confirm Bernstein’s idea that the central nervous system takes advantage of the passive-interactive properties of the moving system. Also the modulation of the EMG patterns should be explained taking in account the reactive forces and the dual functions (maintenance of posture and generation of movement) of the muscles.     

Termination of upper limb movement by cutaneous afferents.

We tested whether cutaneous afferents from the skin field close to an upper limb muscular region would carry information to spinal neurons at the onset or at the offset of a voluntary elbow extension movement lasting 1 s. We detected a depression of EMG activity both at onset and at the offset of the reaching movement but in the latter case depression was significantly larger and immediate. The marked depression of EMG activity suggests an inhibition, via spinal neurons, of the descending excitation to the motoneurones supplying the triceps brachii. This spinal control might be a very efficient mechanism for the termination of voluntary movement.     

Mechanomyogram and electromyogram responses of upper limb during sustained isometric fatigue with varying shoulder and elbow postures

To investigate the behavior of mechanomyogram (MMG) and electromyogram (EMG) signals in the time and frequency domains during sustained isometric contraction, MMG and surface EMG were obtained simultaneously from four muscles: upper trapezius (TP), anterior deltoid (DL), biceps brachii (BB), and brachioradialis (BR) of 10 healthy male subjects. Experimental conditions consisted of 27 combinations of 9 postures [3 shoulder angles (SA): 0 degree, 30 degrees, 60 degrees and 3 elbow angles (EA): 120 degrees, 90 degrees, 60 degrees] and 3 contraction levels: 20%, 40%, and 60% of maximum voluntary contraction (MVC). Subjective evaluations of fatigue were also assessed using the Borg scale at intervals of 60, 30, and 10 sec at 20%, 40%, and 60% MVC tests, respectively. The mean power frequency (MPF) and root mean square (RMS) of both signals were calculated. The current study found clear and significant relationships among physiological and psychological parameters on the one hand and SA and EA on the other. EA's effect on MVC was found to be significant. SA had a highly significant effect on both endurance time and Borg scale. In all experimental conditions, significant correlations were found between the changes in MPF and RMS of EMG in BB with SA and EA (or muscle length). In all four muscles, MMG frequency content was two or three times lower than EMG frequency content. During sustained isometric contraction, the EMG signal showed the well-known shift to lower frequencies (a continuous decrease from onset to completion of the contraction). In contrast, the MMG spectra did not show any shift, although its form changed (generally remaining about constant). Throughout the contraction, increased RMS of EMG was found for all tests, whereas in the MMG signal, a significant progressive increase in RMS was observed only at 20% MVC in all four muscles. This supports the hypothesis that the RMS amplitude of the MMG signal produced during contraction is highly correlated with force production. Possible explanations for this behavioral difference between the MMG and EMG signals are discussed.     

The utility of an empirically derived co-activation ratio for muscle force prediction through optimization

Biomechanical optimization models that apply efficiency-based objective functions often underestimate or negate antagonist co-activation. Co-activation assists movement control, joint stabilization and limb stiffness and should be carefully incorporated into models. The purposes of this study were to mathematically describe co-activation relationships between elbow flexors and extensors during isometric exertions at varying intensity levels and postures, and secondly, to apply these co-activation relationships as constraints in an optimization muscle force prediction model of the elbow and assess changes in predictions made while including these constraints. Sixteen individuals performed 72 isometric exertions while holding a load in their right hand. Surface EMG was recorded from elbow flexors and extensors. A co-activation index provided a relative measure of flexor contribution to total activation about the elbow. Parsimonious models of co-activation during flexion and extension exertions were developed and added as constraints to a muscle force prediction model to enforce co-activation. Three different PCSA data sets were used. Elbow co-activation was sensitive to changes in posture and load. During flexion exertions the elbow flexors were activated about 75% MVC (this amount varied according to elbow angle, shoulder flexion and abduction angles, and load). During extension exertions the elbow flexors were activated about 11% MVC (this amount varied according to elbow angle, shoulder flexion angle and load). The larger PCSA values appeared to be more representative of the subject pool. Inclusion of these co-activation constraints improved the model predictions, bringing them closer to the empirically measured activation levels.     

The effect of textured surfaces on postural stability and lower limb muscle activity

Textured insoles may enhance sensory input on the plantar surfaces of the feet, thereby influencing neuromuscular function. The aim of this study was to investigate whether textured surfaces alter postural stability and lower limb muscle activity during quiet bipedal standing balance with eyes open. Anterior–posterior (AP) and mediolateral (ML) sway variables and the intensity of electromyographic (EMG) activity in eight dominant lower limb muscles were collected synchronously over 30 s in 24 young adults under three randomised conditions: control surface (C), texture 1 (T1) and texture 2 (T2). Repeated measures ANOVA showed that the textured surfaces did not significantly affect AP or ML postural sway in comparison to the control condition (p > 0.05). Neither did the textured surfaces significantly alter EMG activity in the lower limbs (p > 0.05). Under the specific conditions of this study, texture did not affect either postural sway or lower limb muscle activity in static bipedal standing. The results of this study point to three areas of further work including the effect of textured surfaces on postural stability and lower limb muscle activity: (i) in young healthy adults under more vigorous dynamic balance tests, (ii) post-fatigue, and (iii) in older adults presenting age-related deterioration.     

Startle-evoked changes in diaphragmatic activity during wakefulness and sleep

Tonic inhibition of some respiratory muscles occurs as part of the generalized muscle atonia of rapid-eye-movement sleep (REMS). A second type of inhibition of the diaphragm during REMS, fractionations, consists of brief pauses in the diaphragmatic electromyogram (DIA EMG) in association with phasic events. Because motor inhibition can occur as part of the startle response, and the brain is highly activated during REMS, we hypothesized that the neural basis of the fractionations might be activation of a startle network. To test this hypothesis, tone bursts (100 dB, 20-ms duration at 15-s intervals) were applied to cats at a fixed inspiratory level in the DIA moving average during REMS, non-rapid-eye-movement sleep (NREMS), and wakefulness. Parallel sham studies (no tone applied) were obtained for each state. The response of the DIA EMG was averaged over 100 ms by using the tone pulse as a trigger, and the following parameters of the DIA EMG were measured: latency to peak and/or nadir, increment or decrement in activity, and duration of peak and/or nadir. After a tone, all five animals studied displayed a profound suppression of DIA activity during REMS (latency to nadir 42.4 +/- 10.0 ms, duration of suppression 35.9 +/- 17.6 ms). Similarly, DIA activity was suppressed in all cats during NREMS (latency to nadir 40.9 +/- 13.3 ms, duration 23.9 +/- 13.4 ms). An excitatory response was observed in only two cats during NREMS and wakefulness. The similarity of startle-induced DIA EMG pauses to spontaneous fractionations of DIA activity during REMS suggests that the latter result from activation of a central startle system.