Dual task-related changes in the synchronous activity of wrist extensor type-identified motor units in humans

The coupling between the firings of 33 pairs of motor units tested in the extensor carpi radialis muscles was evaluated by cross-correlation analysis and compared during isometric wrist extension and hand clenching. A slightly greater amount of synchrony was observed during hand clenching (0.042 &#45 0.024 vs 0.035 &#45 0.017 synchronous impulses per trigger). This trend did not reach however the level of significance and the changes were actually found to be heterogeneous: in 15 out of the 33 pairs tested, synchronous activity with a narrow coupling (4.6 &#45 2.4 ms) consistent with short-term synchrony was greater during hand clenching whereas in nine other pairs, synchronous activity with a broader dispersion (9.0 &#45 4.5 ms) was reduced. These opposite changes could not be explained in terms of changes in the firing pattern of the motor units and were found instead to correlate with the motor units' biomechanical properties. Motor units with high recruitment thresholds and fast rising twitches showed predominantly an increase in synchrony; whereas the motor unit pairs with low recruitment thresholds and slow twitches showed either an increase or a decrease. The enhanced short-term synchrony suggests that common inputs distributed to motoneurones of all types were more effective during hand clenching whereas the decrease in weakly coupled synchronous activity suggests that other inputs synchronized at a pre-synaptic level and distributed more specifically to motor units recruited at low force levels were less effective. The possible origins of the inputs reflected in the dual changes are discussed in terms of the supra-spinal and peripheral pathways controlling the wrist extensor motoneurones during wrist extension and hand clenching.     

Dual task-related changes in the synchronous activity of wrist extensor type-identified motor units in humans

The coupling between the firings of 33 pairs of motor units tested in the extensor carpi radialis muscles was evaluated by cross-correlation analysis and compared during isometric wrist extension and hand clenching. A slightly greater amount of synchrony was observed during hand clenching (0.042 +/- 0.024 vs 0.035 +/- 0.017 synchronous impulses per trigger). This trend did not reach however the level of significance and the changes were actually found to be heterogeneous: in 15 out of the 33 pairs tested, synchronous activity with a narrow coupling (4.6 +/- 2.4 ms) consistent with short-term synchrony was greater during hand clenching whereas in nine other pairs, synchronous activity with a broader dispersion (9.0 +/- 4.5 ms) was reduced. These opposite changes could not be explained in terms of changes in the firing pattern of the motor units and were found instead to correlate with the motor units' biomechanical properties. Motor units with high recruitment thresholds and fast rising twitches showed predominantly an increase in synchrony; whereas the motor unit pairs with low recruitment thresholds and slow twitches showed either an increase or a decrease. The enhanced short-term synchrony suggests that common inputs distributed to motoneurones of all types were more effective during hand clenching whereas the decrease in weakly coupled synchronous activity suggests that other inputs synchronized at a pre-synaptic level and distributed more specifically to motor units recruited at low force levels were less effective. The possible origins of the inputs reflected in the dual changes are discussed in terms of the supra-spinal and peripheral pathways controlling the wrist extensor motoneurones during wrist extension and hand clenching.     

A simulation study to examine the use of cross-correlation as an estimate of surface EMG cross talk.

Cross-correlation between surface electromyogram (EMG) signals is commonly used as a means of quantifying EMG cross talk during voluntary activation. To examine the reliability of this method, the relationship between cross talk and the cross-correlation between surface EMG signals was examined by using model simulation. The simulation results illustrate an increase in cross talk with increasing subcutaneous fat thickness. The results also indicate that the cross-correlation function decays more rapidly with increasing distance from the active fibers than cross talk, which was defined as the normalized EMG amplitude during activation of a single muscle. The influence of common drive and short-term motor unit synchronization on the cross-correlation between surface EMG signals was also examined. While common drive did not alter the maximum value of the cross-correlation function, the correlation increased with increasing motor unit synchronization. It is concluded that cross-correlation analysis is not a suitable means of quantifying cross talk or of distinguishing between cross talk and coactivation during voluntary contraction. Furthermore, it is possible that a high correlation between surface EMG signals may reflect an association between motor unit firing times, for example due to motor unit synchronization.     

Synchrony between neurons with similar muscle fields in monkey motor cortex

Synchronous firing of motor cortex cells exhibiting postspike facilitation (PSF) or suppression (PSS) of hand muscle EMG was examined to investigate the relationship between synchrony and output connectivity. Recordings were made in macaque monkeys performing a precision grip task. Synchronization was assessed with cross-correlation histograms of the activity from 144 pairs of simultaneously recorded neurons, while spike-triggered averages of EMG defined the muscle field for each cell. Cell pairs with similar muscle fields showed greater synchronization than pairs with nonoverlapping fields. Furthermore, cells with opposing effects in the same muscles exhibited negative synchronization. We conclude that synchrony in motor cortex engages networks of neurons directly controlling the same muscle set, while inhibitory connections exist between neuronal populations with opposing output effects.     

Amplitude cancellation reduces the size of motor unit potentials averaged from the surface EMG.

The purpose of the study was to evaluate the influence of selected physiological parameters on amplitude cancellation in the simulated surface electromyogram (EMG) and the consequences for spike-triggered averages of motor unit potentials derived from the interference and rectified EMG signals. The surface EMG was simulated from prescribed recruitment and rate coding characteristics of a motor unit population. The potentials of the motor units were detected on the skin over a hand muscle with a bipolar electrode configuration. Averages derived from the EMG signal were generated using the discharge times for each of the 24 motor units with lowest recruitment thresholds from a population of 120 across three conditions: 1) excitation level; 2) motor unit conduction velocity; and 3) motor unit synchronization. The area of the surface-detected potential was compared with potentials averaged from the interference, rectified, and no-cancellation EMGs. The no-cancellation EMG comprised motor unit potentials that were rectified before they were summed, thereby preventing cancellation between the opposite phases of the potentials. The percent decrease in area of potentials extracted from the rectified EMG was linearly related to the amount of amplitude cancellation in the interference EMG signal, with the amount of cancellation influenced by variation in excitation level and motor unit conduction velocity. Motor unit synchronization increased potentials derived from both the rectified and interference EMG signals, although cancellation limited the increase in area for both potentials. These findings document the influence of amplitude cancellation on motor unit potentials averaged from the surface EMG and the consequences for using the procedure to characterize motor unit properties.     

Limitations of the surface electromyography technique for estimating motor unit synchronization

Motor unit synchronization was estimated from the surface electromyograms (EMG) of the first dorsal interosseus muscle of human volunteers by a simplified surface-EMG technique (Milner-Brown et al. 1973, 1975). Single motor units were identified from intramuscular recordings and were used to obtain a spike-triggered average of the surface-EMG. The discharge rate of a reference motor unit was controlled at two levels (high and low), and the effect of motor unit activity on the surface-EMG estimate of synchronization was studied in 56 motor units. The surface-EMG estimate of motor unit synchronization was significantly higher when the reference motor unit discharged at the high rate than when it discharged at the low rate. A regression analysis indicated that the synchronization ratio calculated from the surface EMG was significantly correlated with the level of EMG activity in the muscle. Motor unit synchronization was also estimated from surface-EMG measurements that were derived by computer simulation. The simulation permitted manipulation of motor unit activity (discharge rate and recruitment) with a complete absence of synchrony among the units in the pool. The stimulated surface-EMG index was influenced by an artifact associated with signal rectification, and this effect changed non-monotonically with motor unit activity. Furthermore, the increase in the motor unit activity reduced the signal-to-noise ratio of the spike-triggered surface EMG average, and consequently decreased the sensitivity of the surface-EMG index as an estimate of motor unit synchronization. We conclude that the simplified surface-EMG method (Milner-Brown et al. 1973, 1975) does not provide a useful index of motor unit synchronization due to its inability to accurately distinguish the synchronization from methodological effects related to a rectification artifact and variation in the signal-to-noise ratio.     

Optimization of Input Patterns and Neuronal Properties to Evoke Motor Neuron Synchronization

The study used a computational approach to identify combinations of synaptic input timing and strength superimposed on a variety of active dendritic conductances that could evoke similar levels of motor unit synchronization in model motor neurons. Two motor neurons with low recruitment thresholds but different passive properties were modeled using GENESIS software. The timing and strength of synaptic inputs and the density of dendritic ion channels were optimized with a genetic algorithm to produce a set of target discharge times. The target times were taken from experimental recordings made in a human subject and had the synchronization characteristics that are commonly observed in hand muscles. The main finding was that the two parameters with the highest association to output synchrony were the ratio of inward-to-outward ionic conductances (r = 0.344; P = 0.003) and the degree of correlation in inhibitory inputs (r = 0.306; P = 0.009). Variation in the amount of correlation in the excitatory input was not positively correlated with variation in output synchrony. Further, the variability in discharge rate of the model neurons was positively correlated with the density of N-type calcium channels in the dendritic compartments (r = 0.727; P < 0.001 and r = 0.533; P < 0.001 for the two cells). This result suggests that the experimentally observed correlation between discharge variability and synchronization is caused by an increase in fast inward ionic conductances in the dendrites. Given the moderate level of correlation between output synchrony and each of the model parameters, especially at moderate levels of synchrony (E < 0.09 and CIS < 1.0), the results suggest caution in ascribing mechanisms to observations of motor unit synchronization.     

Task-Dependent Intermuscular Motor Unit Synchronization between Medial and Lateral Vastii Muscles during Dynamic and Isometric Squats

Purpose

Motor unit activity is coordinated between many synergistic muscle pairs but the functional role of this coordination for the motor output is unclear. The purpose of this study was to investigate the short-term modality of coordinated motor unit activity–the synchronized discharge of individual motor units across muscles within time intervals of 5ms–for the Vastus Medialis (VM) and Lateralis (VL). Furthermore, we studied the task-dependency of intermuscular motor unit synchronization between VM and VL during static and dynamic squatting tasks to provide insight into its functional role.

Methods

Sixteen healthy male and female participants completed four tasks: Bipedal squats, single-leg squats, an isometric squat, and single-leg balance. Monopolar surface electromyography (EMG) was used to record motor unit activity of VM and VL. For each task, intermuscular motor unit synchronization was determined using a coherence analysis between the raw EMG signals of VM and VL and compared to a reference coherence calculated from two desynchronized EMG signals. The time shift between VM and VL EMG signals was estimated according to the slope of the coherence phase angle spectrum.

Results

For all tasks, except for singe-leg balance, coherence between 15–80Hz significantly exceeded the reference. The corresponding time shift between VM and VL was estimated as 4ms. Coherence between 30–60Hz was highest for the bipedal squat, followed by the single-leg squat and the isometric squat.

Conclusion

There is substantial short-term motor unit synchronization between VM and VL. Intermuscular motor unit synchronization is enhanced for contractions during dynamic activities, possibly to facilitate a more accurate control of the joint torque, and reduced during single-leg tasks that require balance control and thus, a more independent muscle function. It is proposed that the central nervous system scales the degree of intermuscular motor unit synchronization according to the requirements of the movement task at hand.     

Fatigue-related changes in motor-unit synchronization of quadriceps muscles within and across legs

Two experiments were conducted to examine effects of muscle fatigue on motor-unit synchronization of quadriceps muscles (rectus femoris, vastus medialis, vastus lateralis) within and between legs. We expected muscle fatigue to result in an increased common drive to different motor units of synergists within a leg and, hence, to increased synchronization, i.e., an increased coherence between corresponding surface EMGs. We further expected fatigue-related motor overflow to cause motor-unit synchronization of homologous muscles of both legs, although to a lesser extent than for synergists within a leg. In the first experiment, different levels of fatigue were induced by varying posture (knee angle), whereas in the second experiment fatigue was induced in a fixed posture by instructing participants to produce different force levels. EMG coherence was found in two distinct frequency bands (6–11 and 13–18 Hz) and was higher within a leg than between legs. The fatigue-related increase of 6–11 Hz inter-limb synchronization resembled the increased motor overflow during unimanual contractions and thus hinted at an increase in bilateral coupling. Synchronization at 13–18 Hz was clearly different and appeared to be related to posture.     

Motor unit behavior during clonus.

Medial gastrocnemius surface electromyographic activity and intramuscular electromyographic activity were recorded from six individuals with chronic cervical spinal cord injury to document the recruitment order of motor units during clonus. Four subjects induced clonus that lasted up to 30 s while two subjects induced clonus that they actively stopped after 1 min. Mean clonus frequency in different subjects ranged from 4.7 to 7.0 Hz. Most of the 166 motor units recorded during clonus (98%) fired once during each contraction but at slightly different times during each cycle. Other motor units fired during some clonus cycles (1%) or in bursts (1%). When 59 pairs of units were monitored over consecutive clonus cycles (n = 5-89 cycles), only 8 pairs of units altered their recruitment order in some cycles. Recruitment reversals only occurred in units that fired close together in the clonus cycle. These data demonstrate that orderly motor unit recruitment occurs during involuntary contractions of muscles paralyzed chronically by cervical spinal cord injury, providing further support for the importance of spinal mechanisms in the control of human motor unit behavior.     

Correlation of the neuronal impulse activity of different areas of the neocortex in rabbits in the switching of positive and inhibitory conditioned reflexes

By cross-correlation method conjugation in impulse activity of pairs of simultaneously recorded units in the visual and sensorimotor areas of the neocortex (representations of the conditioned and unconditioned stimuli) was studied during the switching of defensive positive and inhibitory reflexes in rabbits. 30-second fragments of impulse activity were analyzed in intervals before and after three presentations of positive and inhibitory conditioned stimuli (CS). The activity of single pairs of units in the process of stimuli presentation was characterized by instability. Only in 29% of 51 units' pairs the presence or absence of correlation between their discharges was stable. Analysis of activity of 75 pairs of units showed differences in impulse activity in inhibitory and positive tonic reflexes. The number of pairs of correlated units in about 30 s after inhibitory CS decreased (27%) in comparison with the interval before its action (52%). In the inhibitory tonic conditioned reflex, temporal intervals of discharges of one unit correlated with discharges of the second unit undergo changes. The obtained results testify that such parameter as the number of pairs of units with correlated activity in intersignal time interval is very important for the realization of motor reaction to conditioned stimuli.     

Muscle functional state assessment by estimation of muscle fiber conduction velocity

In 20 healthy subjects (10 males and 10 females) aged between 24 and 45, the conduction velocity (CV) of excitation along muscle fibers was measured in m. biceps brachii muscle using level averaging of interference electromyograms (EMGs) recorded by branched and monopolar surface electrodes. The measured CV, recorded with both monopolar and branched electrodes, were essentially equal (p < 0.05) at all different muscle tensions (10, 25, 50, and 75% of maximal voluntary contractions (MVCs)) and for all investigated healthy subjects. The CV was significant higher (p < 0.05) at 50 and 75% compared to 10 and 25% of MVC. In branched averaged potentials (AvPs), the terminal positive phase was suppressed. The monopolar AvPs were with waveform similar to those of motor units potentials and the parameters of the phases of different potentials (including the terminal positive one) may give additional information on functional state of muscles.The level-triggered averaging of the interference EMG recorded from the skin surface by branched electrodes is an adequate noninvasive method for measuring the propagation velocity of excitation along muscle fibers and for evaluating changes in the muscle functional state.     

用相关分析法研究家兔两类膈神经单位电活动差异的起源

家兔25只,乌拉坦静脉麻醉(1g/kg),三碘季铵酚制动,人工通气,切断双侧颈迷走神经干。分离双侧膈神经,右侧记录神经干放电;左侧分离细束,同时记录一对单位的放电。共记录到36对单位。神经电活动经放大后输入磁带记录仪,备作脱机处理;或将信号放大、限幅后输入计算机,作连机处理。单纤维根据其放电时程同神经干放电的关系分为时相性单位(PU)和紧张性单位(TU)。分别在TU同TU之间、PU同PU之间、PU同TU之间作相关分析。 在总共36对膈运动神经单位对中,有21对的互相关直方图上出现有显著意义的中心峰,表明它们之间存在着同步化活动,是接受共同的中枢传入所致。其中8对为2PU,,11对为2TU,2对为1PU和1TU。同步化活动的类型有短时程同步化、宽峰同步化和高频振荡同步化三种。在同类单位对(2PU或2TU)与不同类单位对(1PU和1TU)出现同步化的频数之间作x~2检验,结果表明同类单位对中出现同步化的比例显著高于不同类的单位对。 据此,我们认为膈运动神经元紧张性单位和时相性单位放电特性的不同可能是由于它们接受不同的中枢支配所致。     

Synchronization of human motor unit firing during voluntary contraction of muscle and the tonic vibration reflex

We constructed cross-correlograms (CCGs) of action potentials of pairs of motor units (MUs) of human soleus, triceps brachii, and the first and second dorsal interosseous muscles. During voluntary muscle contraction, a pronounced peak in the zero bin was found in 21 out of 126 pairs investigated with the aid of the CCG; this indicates that the number of coincidental firings exceeded chance. The width of the peak did not exceed 5 msec (synchronization for a brief interval, i.e., short-term synchronization). When motoneurons of the soleus muscle were activated by vibration, correlations were found in 12 out 89 pairs of MUs investigated. On the CCGs of action potentials of MU pairs in two muscles (the first and second dorsal interosseous muscles), such correlations were found in four out of 10 pairs investigated. In all of these cases, the ratio of above-change coincidences relative to the total number of MU discharges was small, from 3.0 to 6.1%. Synchronization within a brief time interval can be considered a result of simultaneous creation of EPSPs in motoneourons reached by endings of a single pre-motor nerve fiber. In some pairs of MUs, long term synchronization (clustering) occurred, ie., synchronization lasting several tens of milliseconds. The long-term synchronization can be considered a manifestation of fatigue accompanying tremor.Institute for Problems of Information Transmission, Russian Academy of Sciences, Moscow. Translated from Neirofiziologiya, Vol. 23, No. 6, pp. 691–698, November–December, 1991.     

Influence of motoneuron firing synchronization on SEMG characteristics in dependence of electrode position.

The frequency content of the surface electromyography (SEMG) signal, expressed as median frequency (MF), is often assumed to reflect the decline of muscle fiber conduction velocity in fatigue. MF also decreases when motor unit firings synchronize, and we hypothesized that this effect can explain the electrode-dependent pattern in our previous recordings from the trapezius muscle. An existing motoneuron (MN) model describes the afterhyperpolarization following a spike as an exponential function on which membrane noise is superimposed. Splitting the noise into a common and an individual component extended the model to a MN pool with a tunable level of firing synchrony. An analytical volume conduction model was used to generate motor unit action potentials to simulate SEMG. A realistic level of synchrony decreased the MF of the simulated bipolar SEMG by approximately 30% midway between endplate position and tendon but not above the endplate. This is in accordance with experimental data from the biceps brachii muscle. It was concluded that the pattern of decrease of MF during sustained contractions indeed reflects MN synchronization.     

等长伸膝动作的运动单元放电特征分析

本研究基于表面肌电分解技术,分析伸膝动作中不同发力状态下大腿肌肉运动单元的解码准确性,并对比神经特征和肌电特征在肌肉激活程度估计中的效果. 12名大学生分别以2种发力速度和4种发力等级完成伸膝动作的等长收缩.实验同步采集受试者股内侧肌和股外侧肌处的高密度表面肌电信号和伸膝动作收缩力.基于卷积核补偿算法解码肌电信号得到运动单元动作电位,提取神经特征用于收缩力的互相关分析.结果发现,对于股内侧肌,2种任务及4种收缩力等级下平均解码得到(7±4)个运动单元,股外侧肌平均解码得到(9±5)个运动单元.它们的平均脉冲信噪比(pulse-to-noise ratio,PNR)为30.1 d B,对应解码准确率大于90%.股内侧肌的两种神经特征与力之间的平均相关性分别为(0.79±0.08)和(0.80±0.08),股外侧肌的两种神经特征与力之间的平均相关性分别为(0.85±0.05)和(0.85±0.06).综上可见,基于肌电分解技术可以准确识别不同发力状态下大腿肌肉的运动单元放电活动,并且运动单元放电频率与伸膝动作力高度相关,研究结果可用于运动康复、运动训练及人机接口等领域.     

Activity of Motor Units in Human Elbow Flexor and Extensor Muscles during Task-Dependent Unloading

Neurophysiology - Surface EMGs and activity of 73 single motor units (MUs) of the m. triceps brachii caput laterale (TBcl) and 25 units of the m. biceps brachii caput longum (BBcl) were recorded in...     

Does the activity of ankle plantar flexors differ between limbs while healthy,young subjects stand at ease?

Inferences on the active contribution of plantar flexors to the stabilisation of human standing posture have been drawn from surface electromyograms (EMGs). Surface EMGs were however often detected unilaterally, presuming the myoelectric activity from muscles in a single leg reflects the pattern of muscle activation in both legs. In this study we question whether surface EMGs detected from plantar flexor muscles in both legs provide equal estimates of the duration of activity. Arrays of surface electrodes were used to collect EMGs from gastrocnemius and soleus muscles while twelve, young male participants stood at ease for 60 s. Muscles in each leg were deemed active whenever the Root Mean Square amplitude of EMGs (40 ms epochs) detected by any channel in the arrays exceeded the noise level, defined from EMGs detected during rest. The Chi-Square statistics revealed significant differences in the relative number of active periods for both muscles in 10 out of 12 participants tested, ranging from 2% to 65% (χ² > 17.90; P < 0.01). Pearson correlation analysis indicated side differences in the duration of gastrocnemius though not soleus activity were associated with the centre of pressure mean, lateral position (R = 0.60; P = 0.035). These results suggest therefore that surface EMGs may provide different estimates of the timing of plantar flexors’ activity if collected unilaterally during standing and that asymmetric activation may be not necessarily associated with weight distribution between limbs. Depending on the body side from which EMGs are collected, the active contribution of plantar flexors to standing stabilization may be either under- or over-valued.     

Spike-triggered average torque and muscle fiber conduction velocity of low-threshold motor units following submaximal endurance contractions.

The motor unit twitch torque is modified by sustained contraction, but the association to changes in muscle fiber electrophysiological properties is not fully known. Thus twitch torque, muscle fiber conduction velocity, and action potential properties of single motor units were assessed in 11 subjects following an isometric submaximal contraction of the tibialis anterior muscle until endurance. The volunteers activated a target motor unit at the minimum discharge rate in eight 3-min-long contractions, three before and five after an isometric contraction at 40% of the maximal torque, sustained until endurance. Multichannel surface electromyogram signals and joint torque were averaged with the target motor unit potential as trigger. Discharge rate (mean +/- SE, 6.6 +/- 0.2 pulses/s) and interpulse interval variability (33.3 +/- 7.0%) were not different in the eight contractions. Peak twitch torque and recruitment threshold increased significantly (93 +/- 29 and 12 +/- 5%, P <0.05) in the contraction immediately after the endurance task with respect to the preendurance values (0.94 +/- 0.26 mN.m and 3.7 +/- 0.5% of the maximal torque), whereas time to peak of the twitch torque did not change (74.4 +/- 10.1 ms). Muscle fiber conduction velocity decreased and action potential duration increased in the contraction after the endurance (6.3 +/- 1.8 and 9.8 +/- 1.8%, respectively, P <0.05; preendurance values, 3.9 +/- 0.2 m/s and 11.1 +/- 0.8 ms), whereas the surface potential peak-to-peak amplitude did not change (27.1 +/- 3.1 microV). There was no significant correlation between the relative changes in muscle fiber conduction velocity or surface potential duration and in peak twitch torque (R2= 0.04 and 0.10, respectively). In conclusion, modifications in peak twitch torque of low-threshold motor units with sustained contraction are mainly determined by mechanisms not related to changes in action potential shape and in its propagation velocity.     

Invited review: Mechanisms underlying motor unit plasticity in the respiratory system.

Neuromotor control of skeletal muscles, including respiratory muscles, is ultimately dependent on the function of the motor unit (comprising an individual motoneuron and the muscle fibers it innervates). Considerable diversity exists across diaphragm motor units, yet remarkable homogeneity is present (and maintained) within motor units. In recent years, the mechanisms underlying the development and adaptability of respiratory motor units have received great attention, leading to significant advances in our understanding of diaphragm motor unit plasticity. For example, following imposed inactivity of the diaphragm muscle, there are changes at phrenic motoneurons, neuromuscular junctions, and muscle fibers that tend to restore the ability of the diaphragm to sustain ventilation. The role of activity, neurotrophins, and other growth factors in modulating this adaptability is discussed.