Coordination amongst quadriceps muscles suggests neural regulation of internal joint stresses, not simplification of task performance.

Many studies have demonstrated covariation between muscle activations during behavior, suggesting that muscles are not controlled independently. According to one common proposal, this covariation reflects simplification of task performance by the nervous system so that muscles with similar contributions to task variables are controlled together. Alternatively, this covariation might reflect regulation of low-level aspects of movements that are common across tasks, such as stresses within joints. We examined these issues by analyzing covariation patterns in quadriceps muscle activity during locomotion in rats. The three monoarticular quadriceps muscles (vastus medialis [VM], vastus lateralis [VL], and vastus intermedius [VI]) produce knee extension and so have identical contributions to task performance; the biarticular rectus femoris (RF) produces an additional hip flexion. Consistent with the proposal that muscle covariation is related to similarity of muscle actions on task variables, we found that the covariation between VM and VL was stronger than their covariations with RF. However, covariation between VM and VL was also stronger than their covariations with VI. Since all vastii have identical actions on task variables, this finding suggests that covariation between muscle activity is not solely driven by simplification of overt task performance. Instead, the preferentially strong covariation between VM and VL is consistent with the control of internal joint stresses: Since VM and VL produce opposing mediolateral forces on the patella, the high positive correlation between their activation minimizes the net mediolateral patellar force. These results provide important insights into the interpretation of muscle covariations and their role in movement control.

Shared muscle synergies in human walking and cycling.

The motor system may rely on a modular organization (muscle synergies activated in time) to execute different tasks. We investigated the common control features of walking and cycling in healthy humans from the perspective of muscle synergies. Three hypotheses were tested: 1) muscle synergies extracted from walking trials are similar to those extracted during cycling; 2) muscle synergies extracted from one of these motor tasks can be used to mathematically reconstruct the electromyographic (EMG) patterns of the other task; 3) muscle synergies of cycling can result from merging synergies of walking. A secondary objective was to identify the speed (and cadence) at which higher similarities emerged. EMG activity from eight muscles of the dominant leg was recorded in eight healthy subjects during walking and cycling at four matched cadences. A factorization technique [nonnegative matrix factorization (NNMF)] was applied to extract individual muscle synergy vectors and the respective activation coefficients behind the global muscular activity of each condition. Results corroborated hypotheses 2 and 3, showing that 1) four synergies from walking and cycling can successfully explain most of the EMG variability of cycling and walking, respectively, and 2) two of four synergies from walking appear to merge together to reconstruct one individual synergy of cycling, with best reconstruction values found for higher speeds. Direct comparison of the muscle synergy vectors of walking and the muscle synergy vectors of cycling (hypothesis 1) produced moderated values of similarity. This study provides supporting evidence for the hypothesis that cycling and walking share common neuromuscular mechanisms.

Women with patellofemoral pain show altered motor coordination during lateral step down.

Patients with patellofemoral pain (PFP) present altered activation of the hip and knee muscles. Electromyography (EMG) analyses in PFP patients are usually performed individually for each muscle. However, several studies suggest that the central nervous system may modulate neural commands directed to groups of co-activated muscles, called muscle synergies. Investigating the synergistic organization in PFP will advance our knowledge of the influence of pain on muscle coordination. This study aimed to compare the motor coordination between women with and without PFP during the lateral step down (LSD). 15 women with PFP and 14 asymptomatic women underwent three-dimensional kinematics and EMG assessment during LSD. The Movement Deviation Profile (MDP) was calculated from kinematic data. Muscle synergies were extracted from EMG data of eight lower limb muscles using a non-negative factorization algorithm. Results revealed differences in MDP and an altered synergistic control between women with PFP and asymptomatic while performing the same motor gesture. Particularly, the variability accounted for (VAF) when using 3 synergies to reconstruct EMGs of the PFP group was higher than in the control group, suggesting reduced complexity of motor control in PFP. Detailed synergy analyses highlighted specific differences between groups in vastii and rectus femoris, which are muscles with a crucial role during the squat phase and the transition to rise phase of the LSD. This study shows the ability of muscle synergies analysis to reveal impaired motor coordination in PFP patients, and has the potential to be explored as a complementary tool to current clinical assessment techniques.

Haptic Adaptive Feedback to Promote Motor Learning With a Robotic Ankle Exoskeleton Integrated With a Video Game.

Background: Robotic devices have been used to rehabilitate walking function after stroke. Although results suggest that post-stroke patients benefit from this non-conventional therapy, there is no agreement on the optimal robot-assisted approaches to promote neurorecovery. Here we present a new robotic therapy protocol using a grounded exoskeleton perturbing the ankle joint based on tacit learning control. Method: Ten healthy individuals and a post-stroke patient participated in the study and were enrolled in a pilot intervention protocol that involved performance of ankle movements following different trajectories via video game visual feedback. The system autonomously modulated task difficulty according to the performance to increase the challenge. We hypothesized that motor learning throughout training sessions would lead to increased corticospinal excitability of dorsi-plantarflexor muscles. Transcranial Magnetic Stimulation was used to assess the effects on corticospinal excitability. Results: Improvements have been observed on task performance and motor outcomes in both healthy individuals and post-stroke patient case study. Tibialis Anterior corticospinal excitability increased significantly after the training; however no significant changes were observed on Soleus corticospinal excitability. Clinical scales showed functional improvements in the stroke patient. Discussion and Significance: Our findings both in neurophysiological and performance assessment suggest improved motor learning. Some limitations of the study include treatment duration and intensity, as well as the non-significant changes in corticospinal excitability obtained for Soleus. Nonetheless, results suggest that this robotic training framework is a potentially interesting approach that can be explored for gait rehabilitation in post-stroke patients.

Adaptation of muscle activation after patellar loading demonstrates neural control of joint variables.

We evaluated whether the central nervous system (CNS) chooses muscle activations not only to achieve behavioral goals but also to minimize stresses and strains within joints. We analyzed the coordination between quadriceps muscles during locomotion in rats before and after imposing a lateral force on the patella. Vastus lateralis (VL) and vastus medialis (VM) in the rat produce identical knee torques but opposing mediolateral patellar forces. If the CNS regulates internal joint stresses, we predicted that after imposing a lateral patellar load by attaching a spring between the patella and lateral femur, the CNS would reduce the ratio between VL and VM activation to minimize net mediolateral patellar forces. Our results confirmed this prediction, showing that VL activation was reduced after attaching the spring whereas VM and rectus femoris (RF) activations were not significantly changed. This adaptation was reversed after the spring was detached. These changes were not observed immediately after attaching the spring but only developed after 3-5 days, suggesting that they reflected gradual processes rather than immediate compensatory reflexes. Overall, these results support the hypothesis that the CNS chooses muscle activations to regulate internal joint variables.

Modulation of reciprocal inhibition at the wrist as a neurophysiological correlate of tremor suppression: a pilot healthy subject study.

It has been shown that Ia afferents inhibit muscle activity of the ipsilateral antagonist, a mechanism known as reciprocal inhibition. Stimulation of these afferents may be explored for the therapeutic reduction of pathological tremor (Essential Tremor or due Parkinson's Disease, for example). However, only a few studies have investigated reciprocal inhibition of wrist flexor / extensor motor control. The main goal of this study was to characterize reciprocal inhibition of wrist flexors / extensors by applying surface electrical stimulation to the radial and median nerves, respectively. Firstly, the direct (M) and monosynaptic (H) reflex responses to increasing median and radial nerve stimulation were recorded to characterize the recruitment curve of the flexor carpi radialis (FCR) and extensor carpi radialis (ECR) muscles, respectively. Based on the recruitment curve data, we then stimulated the median and radial nerves below (<; MT) and above (> MT) motor threshold (MT) during a submaximal isometric task to assess the amount of inhibition on ECR and FCR antagonist muscles, respectively. The stimulation of both nerves produced a long-duration inhibition of the antagonist motoneuron pool activity. On average, maximum peak of inhibition was 27 ± 6% for ECR and 32 ± 9% for FCR with stimulation <; MT; maximum peak of inhibition was 45 ± 7% for ECR and 44 ± 13% for FCR when using stimulation > MT. These results validate this neurophysiological technique that demonstrates a mechanism similar to classical reciprocal Ia inhibition reported for other limb joints and that can be used to benchmark strategies to suppress pathological tremor.

Decoding neural activity to predict rat locomotion using intracortical and epidural arrays.

OBJECTIVE: Recovery of voluntary gait after spinal cord injury (SCI) requires the restoration of effective motor cortical commands, either by means of a mechanical connection to the limbs, or by restored functional connections to muscles. The latter approach might use functional electrical stimulation (FES), driven by cortical activity, to restore voluntary movements. Moreover, there is evidence that this peripheral stimulation, synchronized with patients' voluntary effort, can strengthen descending projections and recovery. As a step towards establishing such a cortically-controlled FES system for restoring function after SCI, we evaluate here the type and quantity of neural information needed to drive such a brain machine interface (BMI) in rats. We compared the accuracy of the predictions of hindlimb electromyograms (EMG) and kinematics using neural data from an intracortical array and a less-invasive epidural array. APPROACH: Seven rats were trained to walk on a treadmill with a stable pattern. One group of rats (n = 4) was implanted with intracortical arrays spanning the hindlimb sensorimotor cortex and EMG electrodes in the contralateral hindlimb. Another group (n = 3) was implanted with epidural arrays implanted on the dura overlying hindlimb sensorimotor cortex. EMG, kinematics and neural data were simultaneously recorded during locomotion. EMGs and kinematics were decoded using linear and nonlinear methods from multiunit activity and field potentials. MAIN RESULTS: Predictions of both kinematics and EMGs were effective when using either multiunit spiking or local field potentials (LFPs) recorded from intracortical arrays. Surprisingly, the signals from epidural arrays were essentially uninformative. Results from somatosensory evoked potentials (SSEPs) confirmed that these arrays recorded neural activity, corroborating our finding that this type of array is unlikely to provide useful information to guide an FES-BMI for rat walking. SIGNIFICANCE: We believe that the accuracy of our decoders in predicting EMGs from multiunit spiking activity is sufficient to drive an FES-BMI. Our future goal is to use this rat model to evaluate the potential for cortically-controlled FES to be used to restore locomotion after SCI, as well as its further potential as a rehabilitative technology for improving general motor function.

Combining muscle synergies and biomechanical analysis to assess gait in stroke patients.

The understanding of biomechanical deficits and impaired neural control of gait after stroke is crucial to prescribe effective customized treatments aimed at improving walking function. Instrumented gait analysis has been increasingly integrated into the clinical practice to enhance precision and inter-rater reliability for the assessment of pathological gait. On the other hand, the analysis of muscle synergies has gained relevance as a novel tool to describe the neural control of walking. Since muscle synergies and gait analysis capture different but equally important aspects of walking, we hypothesized that their combination can improve the current clinical tools for the assessment of walking performance. To test this hypothesis, we performed a complete bilateral, lower limb biomechanical and muscle synergies analysis on nine poststroke hemiparetic patients during overground walking. Using stepwise multiple regression, we identified a number of kinematic, kinetic, spatiotemporal and synergy-related features from the paretic and non-paretic side that, combined together, allow to predict impaired walking function better than the Fugl-Meyer Assessment score. These variables were time of peak knee flexion, VAFtotal values, duration of stance phase, peak of paretic propulsion and range of hip flexion. Since these five variables describe important biomechanical and neural control features underlying walking deficits poststroke, they may be feasible to drive customized rehabilitation therapies aimed to improve walking function. This paper demonstrates the feasibility of combining biomechanical and neural-related measures to assess locomotion performance in neurologically injured individuals.

Muscle Synergies in Cycling after Incomplete Spinal Cord Injury: Correlation with Clinical Measures of Motor Function and Spasticity.

BACKGROUND: After incomplete spinal cord injury (iSCI), patients suffer important sensorimotor impairments, such as abnormal locomotion patterns and spasticity. Complementary to current clinical diagnostic procedures, the analysis of muscle synergies has emerged as a promising tool to study muscle coordination, which plays a major role in the control of multi-limb functional movements. OBJECTIVE: Based on recent findings suggesting that walking and cycling share similar synergistic control, the analysis of muscle synergies during cycling might be explored as an early descriptor of gait-related impaired control. This idea was split into the following two hypotheses: (a) iSCI patients present a synergistic control of muscles during cycling; (b) muscle synergies outcomes extracted during cycling correlate with clinical measurements of gait performance and/or spasticity. METHODS: Electromyographic (EMG) activity of 13 unilateral lower limb muscles was recorded in a group of 10 healthy individuals and 10 iSCI subjects during cycling at four different cadences. A non-negative matrix factorization (NNMF) algorithm was applied to identify synergistic components (i.e., activation coefficients and muscle synergy vectors). Reconstruction goodness scores (VAF and r (2)) were used to evaluate the ability of a given number of synergies to reconstruct the EMG signals. A set of metrics based on the similarity between pathologic and healthy synergies were correlated with clinical scales of gait performance and spasticity. RESULTS: iSCI patients preserved a synergistic control of muscles during cycling. The similarity with the healthy reference was consistent with the degree of the impairment, i.e., less impaired patients showed higher similarities with the healthy reference. There was a strong correlation between reconstruction goodness scores at 42 rpm and motor performance scales (TUG, 10-m test and WISCI II). On the other hand, the similarity between the healthy and affected synergies presented correlation with some spasticity symptoms measured by Penn, Modified Ashworth and SCATS scales. CONCLUSION: Overall, the results of this study support the hypothesis that the analysis of muscle synergies during cycling can provide detailed quantitative assessment of functional motor impairments and symptoms of spasticity caused by abnormal spatiotemporal muscle co-activation following iSCI.