Common Synaptic Input Research Articles

Age Related Changes in Motor Function (II). Decline in Motor Performance Outcomes.

Age-related impairments in motor performance are caused by a deterioration in mechanical and neuromuscular functions, which have been investigated from the macro-level of muscle-tendon unit to the micro-level of the single muscle fiber. When compared to the healthy young skeletal muscle, aged skeletal muscle is: (1) weaker, slower and less powerful during the performance of voluntary contractions; (2) less steady during the performance of isometric contractions, particularly at low levels of force; and (3) less susceptible to fatigue during the performance of sustained isometric contractions, but more susceptible to fatigue during the performance of high-velocity dynamic contractions. These impairments have been discussed to be mainly the result of: a) loss of muscle mass and selective atrophy of type II muscle fibers; b) altered tendon mechanical properties (decreased tendon stiffness); c) reduced number and altered function of motor units; d) slower muscle fiber shortening velocity; e) increased oscillation in common synaptic input to motor neurons; and f) altered properties and activity of sarcoplasmic reticulum. In this second part of a two-part review we have detailed the age-related impairments in motor performance with a reference to the most important mechanical and neuromuscular contributing factors.

Non-invasive analysis of motor neurons controlling the intrinsic and extrinsic muscles of the hand

Objective. We present a non-invasive framework for investigating efferent commands to 14 extrinsic and intrinsic hand muscles. We extend previous studies (limited to a few muscles) on common synaptic input among pools of motor neurons in a large number of muscles. Approach. Seven subjects performed sinusoidal isometric contractions to complete seven types of grasps, with each finger and with three combinations of fingers in opposition with the thumb. High-density surface EMG (HD-sEMG) signals (384 channels in total) recorded from the 14 muscles were decomposed into the constituent motor unit action potentials. This provided a non-invasive framework for the investigation of motor neuron discharge patterns, muscle coordination and efferent commands of the hand muscles during grasping. Moreover, during grasping tasks, it was possible to identify common neural information among pools of motor neurons innervating the investigated muscles. For this purpose, principal component analysis (PCA) was applied to the smoothed discharge rates of the decoded motor units. Main results. We found that the first principal component (PC1) of the ensemble of decoded motor neuron spike trains explained a variance of (53.0 ± 10.9) % and was positively correlated with force (R = 0.67 ± 0.10 across all subjects and tasks). By grouping the pools of motor neurons from extrinsic or intrinsic muscles, the PC1 explained a proportion of variance of (57.1 ± 11.3) % and (56.9 ± 11.8) %, respectively, and was correlated with force with R = 0.63 ± 0.13 and 0.63 ± 0.13, respectively. Significance. These observations demonstrate a low dimensional control of motor neurons across multiple muscles that can be exploited for extracting control signals in neural interfacing. The proposed framework was designed for hand rehabilitation perspectives, such as post-stroke rehabilitation and hand-exoskeleton control.

The Impact Of Fatiguing, Intermittent Isometric Contractions On Muscle Force Variability

PURPOSE: To evaluate the influence of fatigue on force variability of the vastus lateralis (VL) during repeated isometric exercise performed at 30% maximal voluntary isometric contraction force (MVIC). METHODS: Twelve resistance-trained males (23.8 ± 3.6 y; 87.3 ± 10.5 kg; 176.3 ± 6 cm) completed MVIC testing and then repeated isometric contractions at 30% MVIC while tracking target force trajectories repetitively until they could no longer achieve 95% target force. Force and surface electromyographic (EMG) signals from the VL were collected during exercise. One-way repeated measures ANOVAs were used to analyze average force (FAVG), coefficient of variation of force (FCV), EMG amplitude (EMGRMS), and median power frequency (MDF) during every 25% of the repetitions (REP) completed. To examine the relationship between EMGRMS and FCV across the work bout, FCV was plotted against EMGRMS, linear regression lines were fit, and correlation coefficients were calculated for each subject. RESULTS: No main effect of REP was observed for FAVG (p = 0.07) or MDF (p = 0.29), but there was for FCV and EMGRMS (p < 0.0001). FCV increased from the first to the 50-100% REP (p ≤ 0.001-0.02), 25% to the 100% REP (p < 0.001), and the 50% to the 100% REP (p < 0.001). EMGRMS increased from the first to the 25-100% REP (p = 0.002-0.024), the 25% to the 50-100% REP (p = 0.001-0.019), the 50% to the 75-100% REP (p = 0.002-0.018) and the 75% to the 100% REP (p = 0.014). Additionally, all 12 subjects displayed strong, significant, positive relationships for FCV vs. EMGRMS across the exercise bout (Table 1). CONCLUSIONS: The increase in both FCV and EMGRMS suggest that as fatigue develops during intermittent isometric exercise, force steadiness decreases while EMG amplitude increases. It is possible that the decrease in force steadiness occurred due to increased common synaptic input to the motor neuron pool secondary to fatigue-induced increases in net excitatory input.

Interfacing With Alpha Motor Neurons in Spinal Cord Injury Patients Receiving Trans-spinal Electrical Stimulation.

Trans-spinal direct current stimulation (tsDCS) provides a non-invasive, clinically viable approach to potentially restore physiological neuromuscular function after neurological impairment, e.g., spinal cord injury (SCI). Use of tsDCS has been hampered by the inability of delivering stimulation patterns based on the activity of neural targets responsible to motor function, i.e., α-motor neurons (α-MNs). State of the art modeling and experimental techniques do not provide information about how individual α-MNs respond to electrical fields. This is a major element hindering the development of neuro-modulative technologies highly tailored to an individual patient. For the first time, we propose the use of a signal-based approach to infer tsDCS effects on large α-MNs pools in four incomplete SCI individuals. We employ leg muscles spatial sampling and deconvolution of high-density fiber electrical activity to decode accurate α-MNs discharges across multiple lumbosacral segments during isometric plantar flexion sub-maximal contractions. This is done before, immediately after and 30 min after sub-threshold cathodal stimulation. We deliver sham tsDCS as a control measure. First, we propose a new algorithm for removing compromised information from decomposed α-MNs spike trains, thereby enabling robust decomposition and frequency-domain analysis. Second, we propose the analysis of α-MNs spike trains coherence (i.e., frequency-domain) as an indicator of spinal response to tsDCS. Results showed that α-MNs spike trains coherence analysis sensibly varied across stimulation phases. Coherence analyses results suggested that the common synaptic input to α-MNs pools decreased immediately after cathodal tsDCS with a persistent effect after 30 min. Our proposed non-invasive decoding of individual α-MNs behavior may open up new avenues for the design of real-time closed-loop control applications including both transcutaneous and epidural spinal electrical stimulation where stimulation parameters are adjusted on-the-fly.

Neurophysiological correlates of force control improvement induced by sinusoidal vibrotactile stimulation

Objective. An optimal level of vibrotactile stimulation has been shown to improve sensorimotor control in healthy and diseased individuals. However, the underlying neurophysiological mechanisms behind the enhanced motor performance caused by vibrotactile stimulation are yet to be fully understood. Therefore, here we aim to evaluate the effect of a cutaneous vibration on the firing behavior of motor units in a condition of improved force steadiness. Approach. Participants performed a visuomotor task, which consisted of low-intensity isometric contractions of the first dorsal interosseous (FDI) muscle, while sinusoidal (175 Hz) vibrotactile stimuli with different intensities were applied to the index finger. High-density surface electromyogram was recorded from the FDI muscle, and a decomposition algorithm was used to extract the motor unit spike trains. Additionally, computer simulations were performed using a multiscale neuromuscular model to provide a potential explanation for the experimental findings. Main results. Experimental outcomes showed that an optimal level of vibration significantly improved force steadiness (estimated as the coefficient of variation of force). The decreased force variability was accompanied by a reduction in the variability of the smoothed cumulative spike train (as an estimation of the neural drive to the muscle), and the proportion of common inputs to the FDI motor nucleus. However, the interspike interval variability did not change significantly with the vibration. A mathematical approach, together with computer simulation results suggested that vibrotactile stimulation would reduce the variance of the common synaptic input to the motor neuron pool, thereby decreasing the low frequency fluctuations of the neural drive to the muscle and force steadiness. Significance. Our results demonstrate that the decreased variability in common input accounts for the enhancement in force control induced by vibrotactile stimulation.

The human central nervous system transmits common synaptic inputs to distinct motor neuron pools during non-synergistic digit actions.

Key points Neural connectivity between distinct motor neuronal modules in the spinal cord is classically studied through electrical stimulation or multi‐muscle EMG recordings.We quantified the strength of correlation in the activity of two distinct populations of motor neurons innervating the thenar and first dorsal interosseous muscles during tasks that required the two hand muscles to exert matched or un‐matched forces in different directions.We show that when the two hand muscles are concurrently activated, synaptic input to the two motor neuron pools is shared across all frequency bandwidths (representing cortical and spinal input) associated with force control.The observed connectivity indicates that motor neuron pools receive common input even when digit actions do not belong to a common behavioural repertoire. Neural connectivity between distinct motor neuronal modules in the spinal cord is classically studied through electrical stimulation or multi‐muscle EMG recordings. Here we quantify the strength of correlation in the activity of two distinct populations of motor neurons innervating the thenar and first dorsal interosseous muscles in humans during voluntary contractions. To remove confounds associated with previous studies, we used a task that required the two hand muscles to exert matched or un‐matched forces in different directions. Despite the force production task consisting of uncommon digit force coordination patterns, we found that synaptic input to motor neurons is shared across all frequency bands, reflecting cortical and spinal inputs associated with force control. The coherence between discharge timings of the two pools of motor neurons was significant at the delta (0–5 Hz), alpha (5–15 Hz) and beta (15–35 Hz) bands (P < 0.05). These results suggest that correlated input to motor neurons of two hand muscles can occur even during tasks not belonging to a common behavioural repertoire and despite lack of common innervation. Moreover, we show that the extraction of activity from motor neurons during voluntary force control removes cross‐talk associated with global EMG recordings, thus allowing direct in vivo interrogation of spinal motor neuron activity.

Remarkable hand grip steadiness in individuals with complete spinal cord injury.

Although no damage occurs in the brains of individuals with spinal cord injury, structural and functional reorganization occurs in the sensorimotor cortex because of the deafferentation of afferent signal input from below the injury level. This brain reorganization that is specific to individuals with spinal cord injury is speculated to contribute to the improvement of the motor function of the remaining upper limbs. However, no study has investigated in detail the motor function above the injury level. To clarify this, we designed an experiment using the handgrip force steadiness task, which is a popular technique for evaluating motor function as the index of the variability of common synaptic input to motoneurons. Fourteen complete spinal cord injury (cSCI) individuals in the chronic phase, fifteen individuals with lower limb disabilities, and twelve healthy controls participated in the study. We clarified that the force steadiness in the cSCI group was significantly higher than that in the control groups, and that sports years were significantly correlated with this steadiness. Furthermore, multiple analyses revealed that force steadiness was significantly predicted by sports years. These results suggest that brain reorganization after spinal cord injury can functionally affect the remaining upper limb motor function. These findings may have implications in the clinical rehabilitation field, such as occupational rehabilitation of the upper limbs. They also indicate that individuals with complete spinal cord injury, based on their enhanced force adjustment skills, would excel at fine motor tasks such as manufacturing and handicrafts.

A wearable neural interface for detecting and decoding attempted hand movements in a person with tetraplegia.

We are developing a wearable neural interface based on high-density surface electromyography (HDEMG) for detecting and decoding signals from spared motor units in the forearms of people with tetraplegia after spinal cord injury (SCI). A lightweight, form-fitting garment containing 150 disc electrodes and covering the entire forearm was used to map the myoelectric activity of forearm muscles during a wide range of voluntary tasks of a person with chronic tetraplegia after SCI (C5 motor and C6 sensory American Spinal Injury Association Impairment Scale B spinal cord injury). Despite exhibiting no overt finger motion, myoelectric signals were detectable for attempted movements of individual digits and were highly discriminable. Motor unit decomposition was used to identify the activity of >30 motor neurons, active specifically during rotation, pronation of the wrist (4 units), and flexion of the elbow joint (7 units), and during attempted movements of individual hand digits (1-5 units). In addition, we performed a neural connectivity analysis based on the power of the common oscillations of the identified motor neurons in the delta (~5Hz), alpha (~6-12 Hz), and beta bands (~15-30 Hz). This analysis showed clear common synaptic inputs to the identified motor neurons in all the analyzed frequency bands. This neural interface offers a new potential for the control of assistive technologies, whereby the motor neurons spared after SCI may serve as a direct readout of motor intent that allows proportional control over several distinct degrees of freedom. Moreover, this framework can be used to study the reorganization and recovery of spinal networks after injury and rehabilitation.

Investigating the Effect of Persistent Inward Currents on Motor Unit Firing Rates and Beta-Band Coherence in a Model of the First Dorsal Interosseous Muscle.

Neuromodulatory drive resulting in the generation of persistent inward currents (PICs) within motoneuron dendrites has been demonstrated to introduce nonlinearities into the motoneuron input-output function for a given motor command. It is less understood, however, as to what role PICs play during voluntary contractions or on the correlation between motoneuron firings arising as a result of common synaptic inputs to the motoneuron pool. To examine this, a biophysical model of the motoneuron pool representing the first dorsal interosseous (FDI) muscle was used to simulate the effects of PICs on motor unit firing patterns and beta-band (15-30 Hz) motor unit coherence at 20, 30, and 40 percent of maximum voluntary contraction (MVC). The contribution of PICs at each MVC was quantified by calculating the difference in the mean firing rate of each motoneuron within the pool and assessing changes in the mean firing rate distribution and motor unit coherence with and without PICs present. The results of the current study demonstrated that increased activation of PICs progressively reduced motor unit coherence, however, changes in coherence were modest when investigating activation levels consistent with experimentally observed mean motor unit firing rates in the FDI muscle during isometric voluntary contraction.

The relative strength of common synaptic input to motor neurons is not a determinant of the maximal rate of force development in humans.

Correlation between motor unit discharge times, often referred to as motor unit synchronization, is determined by common synaptic input to motor neurons. Although it has been largely speculated that synchronization should influence the rate of force development, the association between the degree of motor unit synchronization and rapid force generation has not been determined. In this study, we examined this association with both simulations and experimental motor unit recordings. The analysis of experimental motor unit discharges from the tibialis anterior muscle of 20 healthy individuals during rapid isometric contractions revealed that the average motor unit discharge rate was associated with the rate of force development. Moreover, the extent of motor unit synchronization was entirely determined by the average motor unit discharge rate (R > 0.7, P < 0.0001). The simulation model demonstrated that the relative proportion of common synaptic input received by motor neurons, which determines motor unit synchronization, does not influence the rate of force development (R = 0.03, P > 0.05). Nonetheless, the estimates of correlation between motor unit spike trains were significantly correlated with the rate of force generation (R > 0.8, P < 0.0001). These results indicate that the average motor unit discharge rate, but not the degree of motor unit synchronization, contributes to most of the variance of human contractile speed among individuals. In addition, estimates of correlation between motor unit discharge times depend strongly on the number of identified motor units and therefore are not indicative of the strength of common input. NEW & NOTEWORTHY It is commonly assumed that motor unit synchronization has an impact on the rate of force development of a muscle. Here we present computer simulations and experimental data of human tibialis anterior motor units during rapid contractions that show that motor unit synchronization is not a determinant of the rate of force production. This conclusion clarifies the neural determinants of rapid force generation.

Amplitude cancellation influences the association between frequency components in the neural drive to muscle and the rectified EMG signal.

The rectified surface EMG signal is commonly used as an estimator of the neural drive to muscles and therefore to infer sources of synaptic input to motor neurons. Loss of EMG amplitude due to the overlap of motor unit action potentials (amplitude cancellation), however, may distort the spectrum of the rectified EMG and thereby its correlation with the neural drive. In this study, we investigated the impact of amplitude cancelation on this correlation using analytical derivations and a computational model of motor neuron activity, force, and the EMG signal. First, we demonstrated analytically that an ideal rectified EMG signal without amplitude cancellation (EMGnc) is superior to the actual rectified EMG signal as estimator of the neural drive to muscle. This observation was confirmed by the simulations, as the average coefficient of determination (r2) between the neural drive in the 1–30 Hz band and EMGnc (0.59±0.08) was matched by the correlation between the rectified EMG and the neural drive only when the level of amplitude cancellation was low (<40%) at low contraction levels (<5% of maximum voluntary contraction force; MVC). This correlation, however, decreased linearly with amplitude cancellation (r = -0.83) to values of r2 <0.2 at amplitude cancellation levels >60% (contraction levels >15% MVC). Moreover, the simulations showed that a stronger (i.e. more variable) neural drive implied a stronger correlation between the rectified EMG and the neural drive and that amplitude cancellation distorted this correlation mainly for low-frequency components (<5 Hz) of the neural drive. In conclusion, the results indicate that amplitude cancellation distorts the spectrum of the rectified EMG signal. This implies that valid use of the rectified EMG as an estimator of the neural drive requires low contraction levels and/or strong common synaptic input to the motor neurons.

Oscillations in neural drive and age-related reductions in force steadiness with a cognitive challenge.

A cognitive challenge when imposed during a low-force isometric contraction will exacerbate sex- and age-related decreases in force steadiness, but the mechanism is not known. We determined the role of oscillations in the common synaptic input to motor units on force steadiness during a muscle contraction with a concurrent cognitive challenge. Forty-nine young adults (19-30 yr; 25 women, 24 men) and 36 old adults (60-85 yr; 19 women, 17 men) performed a cognitive challenge (counting backward by 13) during an isometric elbow flexion task at 5% of maximal voluntary contraction. Single-motor units were decomposed from high-density surface EMG recordings. For a subgroup of participants, motor units were matched during control and cognitive challenge trials, so the same motor unit was analyzed across conditions. Reduced force steadiness was associated with greater oscillations in the synaptic input to motor units during both control and cognitive challenge trials ( r = 0.45-0.47, P < 0.01). Old adults and young women showed greater oscillations in the common synaptic input to motor units and decreased force steadiness when the cognitive challenge was imposed, but young men showed no change across conditions (session × age × sex, P < 0.05). Oscillations in the common synaptic input to motor units is a potential mechanism for altered force steadiness when a cognitive challenge is imposed during low-force contractions in young women and old adults. NEW & NOTEWORTHY We found that oscillations in the common synaptic input to motor units were associated with a reduction in force steadiness when a cognitive challenge was imposed during low-force contractions of the elbow flexor muscles in young women and old men and women but not young men. Age- and sex-related muscle weakness was associated with these changes.

Sustained involuntary muscle activity in cerebral palsy and stroke: same symptom, diverse mechanisms.

Individuals with lesions of central motor pathways frequently suffer from sustained involuntary muscle activity. This symptom shares clinical characteristics with dystonia but is observable in individuals classified as spastic. The term spastic dystonia has been introduced, although the underlying mechanisms of involuntary activity are not clarified and vary between individuals depending on the disorder. This study aimed to investigate the nature and pathophysiology of sustained involuntary muscle activity in adults with cerebral palsy and stroke. Seventeen adults with cerebral palsy (Gross Motor Function Classification System I–V), 8 adults with chronic stroke and 14 control individuals participated in the study. All individuals with cerebral palsy or stroke showed increased resistance to passive movement with Modified Ashworth Scale >1. Two-minute surface EMG recordings were obtained from the biceps muscle during attempted rest in three positions of the elbow joint; a maximally flexed position, a 90-degree position and a maximally extended position. Cross-correlation analysis of sustained involuntary muscle activity from individuals with cerebral palsy and stroke, and recordings of voluntary isometric contractions from control individuals were performed to examine common synaptic drive. In total, 13 out of 17 individuals with cerebral palsy and all 8 individuals with stroke contained sustained involuntary muscle activity. In individuals with cerebral palsy, the level of muscle activity was not affected by the joint position. In individuals with stroke, the level of muscle activity significantly (P < 0.05) increased from the flexed position to the 90 degree and extended position. Cumulant density function indicated significant short-term synchronization of motor unit activities in all recordings. All groups exhibited significant coherence in the alpha (6–15 Hz), beta (16–35 Hz) and early gamma band (36–60 Hz). The cerebral palsy group had lower alpha band coherence estimates, but higher gamma band coherence estimates compared with the stroke group. Individuals with increased resistance to passive movement due to cerebral palsy or stroke frequently suffer sustained involuntary muscle activity, which cannot exclusively be described by spasticity. The sustained involuntary muscle activity in both groups originated from a common synaptic input to the motor neuron pool, but the generating mechanisms could differ between groups. In cerebral palsy it seemed to originate more from central mechanisms, whereas peripheral mechanisms likely play a larger role in stroke. The sustained involuntary muscle activity should not be treated simply like the spinal stretch reflex mediated symptom of spasticity and should not either be treated identically in both groups.

Non-Propagating Components of Surface Electromyogram Reflect Motor Unit Firing Rates

Interference surface electromyogram (EMG) recorded from linear electrode arrays aligned to muscle fibres can be separated into propagating and non-propagating contributions. The first reflects the propagation of action potentials along muscle fibres. The non-propagating components are here shown to be related to the overall firing pattern of active motor units (MU). Indeed, in simulations, the power spectral density (PSD) of non-propagating components shows a low frequency peak corresponding to the mean firing rate, even when such a contribution is not visible in the PSD of the EMG (either monopolar or single differential configuration, either rectified or not). Moreover, it has a high correlation with the PSD of the cumulative firings of the MUs in the detection volume of the recording system. Applications to experimental data confirm that the low frequency peak is more evident for the non-propagating components than for the raw signals and is related to the MU firing frequency. Potential future applications are expected in the study of the MU control in different conditions (e.g., training, fatigue or pathology, inducing changes, or modulation of firing rate) and in the investigation of common synaptic inputs to motor neurons.

The modulation of force steadiness by electrical nerve stimulation applied to the wrist extensors differs for young and older adults.

We compared the modulation of force steadiness by different types of electrical nerve stimulation in young (n = 13, 25 ± 4years) and older (n = 12, 78 ± 5years) adults. The protocol involved four types of isometric contractions with the wrist-extensor muscles at 10% of the maximal force. Three of the contractions involved electrical nerve stimulation that comprised two forms of neuromuscular electrical stimulation (NMES) to evoke muscle contractions and a voluntary contraction with superimposed transcutaneous electrical nerve stimulation (TENS) at an intensity less than motor threshold. The coefficient of variation (CV) for force during voluntary wrist extension was less (P = 0.03) for young (1.82 ± 0.43%) than older adults (2.80 ± 1.08%). The CV for force did not differ between age groups during the three types of electrical nerve stimulation but was reduced relative to the value observed during voluntary wrist extension for older adults. In contrast, the CV for force increased during the voluntary contraction with superimposed TENS for young adults but not for older adults. Moreover, there were significant negative correlations in older adults between the CV for force during the voluntary contraction and its decrease with electrical nerve stimulation. Differences in the CV for force between the evoked and voluntary contractions for the two age groups suggest that the variance in common synaptic input to motor neurons during steady voluntary contractions with the wrist extensors is greater for older adults than young adults.

Decrease in force steadiness with aging is associated with increased power of the common but not independent input to motor neurons.

Declines in motor function with advancing age have been attributed to changes occurring at all levels of the neuromuscular system. However, the impact of aging on the control of muscle force by spinal motor neurons is not yet understood. In this study on 20 individuals aged between 24 and 75 yr (13 men, 7 women), we investigated the common synaptic input to motor neurons of the tibialis anterior muscle and its impact on force control. Motor unit discharge times were identified from high-density surface EMG recordings during isometric contractions at forces of 20% of maximal voluntary effort. Coherence analysis between motor unit spike trains was used to characterize the input to motor neurons. The decrease in force steadiness with age ( R2 = 0.6, P < 0.01) was associated with an increase in the amplitude of low-frequency oscillations of functional common synaptic input to motor neurons ( R2 = 0.59; P < 0.01). The relative proportion of common input to independent noise at low frequencies increased with variability (power) in common synaptic input. Moreover, variability in interspike interval did not change and strength of the common input in the gamma band decreased with age ( R2 = 0.22; P < 0.01). The findings indicate that age-related reduction in the accuracy of force control is associated with increased common fluctuations to motor neurons at low frequencies and not with an increase in independent synaptic input. NEW & NOTEWORTHY The influence of aging on the role of spinal motor neurons in accurate force control is not yet understood. We demonstrate that aging is associated with increased oscillations in common input to motor neurons at low frequencies and with a decrease in the relative strength of gamma oscillations. These results demonstrate that the synaptic inputs to motor neurons change across the life span and contribute to a decline in force control.

Coherence of the Surface EMG and Common Synaptic Input to Motor Neurons.

Coherence between electromyographic (EMG) signals is often used to infer the common synaptic input to populations of motor neurons. This analysis, however, may be limited due to the filtering effect of the motor unit action potential waveforms. This study investigated the ability of surface EMG–EMG coherence to predict common synaptic input to motor neurons. Surface and intramuscular EMG were recorded from two locations of the tibialis anterior muscle during steady ankle dorsiflexions at 5 and 10% of the maximal force in 10 healthy individuals. The intramuscular EMG signals were decomposed to identify single motor unit spike trains. For each trial, the strength of the common input in different frequency bands was estimated from the coherence between two cumulative spike trains, generated from sets of single motor unit spike trains (reference measure). These coherence values were compared with those obtained from the coherence between the surface EMG signals (raw, rectified, and high-passed filtered at 250 Hz before rectification) using linear regression. Overall, the high-pass filtering of the EMG prior to rectification did not substantially change the results with respect to rectification only. For both signals, the correlation of EMG coherence with motor unit coherence was strong at 5% MVC (r2 > 0.8; p < 0.01), but only for frequencies > 5 Hz. At 10% MVC, the correlation between EMG and motor unit coherence was only significant for frequencies > 15 Hz (r2 > 0.8; p < 0.01). However, when using raw EMG for coherence analysis, the only significant relation with motor unit coherence was observed for the bandwidth 5–15 Hz (r2 > 0.68; p = 0.04). In all cases, there was no association between motor unit and EMG coherence for frequencies < 5 Hz (r2 ≤ 0.2; p ≥ 0.51). In addition, a substantial error in the best linear fit between motor unit and EMG coherence was always present. In conclusion, high-frequency (>5 Hz) common synaptic inputs to motor neurons can partly be estimated from the rectified surface EMG at low-level steady contractions. The results, however, suggest that this association is weakened with increasing contraction intensity and that input at lower frequencies during steady isometric contractions cannot be detected accurately by surface EMG coherence.

Common Synaptic Input to Motor Neurons and Neural Drive to Targeted Reinnervated Muscles.

We compared the behavior of motor neurons innervating their physiological muscle targets with motor neurons from the same spinal segment whose axons were surgically redirected to remnant muscles (targeted muscle reinnervation). The objective was to assess whether motor neurons with nonphysiological innervation receive similar synaptic input and could be voluntary controlled as motor neurons with natural innervation. For this purpose, we acquired high-density EMG signals from the biceps brachii in 5 male transhumeral amputees who underwent targeted reinnervation of this muscle by the ulnar nerve and from the first dorsal interosseous muscle of 5 healthy individuals to investigate the natural innervation of the ulnar nerve. The same recordings were also performed from the biceps brachii muscle of additional 5 able-bodied individuals. The EMG signals were decomposed into discharges of motor unit action potentials. Motor neurons were progressively recruited for the full range of submaximal muscle activation in all conditions. Moreover, their discharge rate significantly increased from recruitment to target activation level in a similar way across the subject groups. Motor neurons across all subject groups received common synaptic input as identified by coherence analysis of their spike trains. However, the relative strength of common input in both the delta (0.5-5 Hz) and alpha (5-13 Hz) bands was significantly smaller for the surgically reinnervated motor neuron pool with respect to the corresponding physiologically innervated one. The results support the novel approach of motor neuron interfacing for prosthesis control and provide new insights into the role of afferent input on motor neuron activity.SIGNIFICANCE STATEMENT Targeted muscle reinnervation surgically redirects nerves that lost their target in the amputation into redundant muscles in the region of the stump. The study of the behavior of motor neurons following this surgery is needed for designing biologically inspired prosthetic control strategies. Moreover, targeted muscle reinnervation offers a human experimental framework for studying the control and behavior of motor neurons when changing their target innervated muscle fibers and sensory feedback. Here, we show that the control of motor neurons and their synaptic input, following reinnervation, was remarkably similar to that of the physiological innervation, although with reduced common drive at some frequencies. The results advance our knowledge on the role of sensory input in the generation of the neural drive to muscles and provide the basis for designing physiologically inspired methods for prosthesis control.

Altered Motor Unit Discharge Coherence in Paretic Muscles of Stroke Survivors.

After a cerebral stroke, a series of changes at the supraspinal and spinal nervous system can alter the control of muscle activation, leading to persistent motor impairment. However, the relative contribution of these different levels of the nervous system to impaired muscle activation is not well understood. The coherence of motor unit (MU) spike trains is considered to partly reflect activities of higher level control, with different frequency band representing different levels of control. Accordingly, the objective of this study was to quantify the different sources of contribution to altered muscle activation. We examined the coherence of MU spike trains decomposed from surface electromyogram (sEMG) of the first dorsal interosseous muscle on both paretic and contralateral sides of 14 hemispheric stroke survivors. sEMG was obtained over a range of force contraction levels at 40, 50, and 60% of maximum voluntary contraction. Our results showed that MU coherence increased significantly in delta (1–4 Hz), alpha (8–12 Hz), and beta (15–30 Hz) bands on the affected side compared with the contralateral side, but was maintained at the same level in the gamma (30–60 Hz) band. In addition, no significant alteration was observed across medium–high force levels (40–60%). These results indicated that the common synaptic input to motor neurons increased on the paretic side, and the increased common input can originate from changes at multiple levels, including spinal and supraspinal levels following a stroke. All these changes can contribute to impaired activation of affected muscles in stroke survivors. Our findings also provide evidence regarding the different origins of impaired muscle activation poststroke.

Correlation between discharge timings of pairs of motor units reveals the presence but not the proportion of common synaptic input to motor neurons.

We investigated whether correlation measures derived from pairs of motor unit (MU) spike trains are reliable indicators of the degree of common synaptic input to motor neurons. Several 50-s isometric contractions of the biceps brachii muscle were performed at different target forces ranging from 10 to 30% of the maximal voluntary contraction relying on force feedback. Forty-eight pairs of MUs were examined at various force levels. Motor unit synchrony was assessed by cross-correlation analysis using three indexes: the output correlation as the peak of the cross-histogram (ρ) and the number of synchronous spikes per second (CIS) and per trigger (E). Individual analysis of MU pairs revealed that ρ, CIS, and E were most often positively associated with discharge rate (87, 85, and 76% of the MU pairs, respectively) and negatively with interspike interval variability (69, 65, and 62% of the MU pairs, respectively). Moreover, the behavior of synchronization indexes with discharge rate (and interspike interval variability) varied greatly among the MU pairs. These results were consistent with theoretical predictions, which showed that the output correlation between pairs of spike trains depends on the statistics of the input current and motor neuron intrinsic properties that differ for different motor neuron pairs. In conclusion, the synchronization between MU firing trains is necessarily caused by the (functional) common input to motor neurons, but it is not possible to infer the degree of shared common input to a pair of motor neurons on the basis of correlation measures of their output spike trains.NEW & NOTEWORTHY The strength of correlation between output spike trains is only poorly associated with the degree of common input to the population of motor neurons. The synchronization between motor unit firing trains is necessarily caused by the (functional) common input to motor neurons, but it is not possible to infer the degree of shared common input to a pair of motor neurons on the basis of correlation measures of their output spike trains.