Motor-unit synchronization increases EMG amplitude and decreases force steadiness of simulated contractions

The purpose of the study was to determine the effect of motor-unit synchronization on the surface electromyogram (EMG) and isometric force using a computer model of muscle contraction. The EMG and force were simulated by generating muscle fiber action potentials, defining motor-unit mechanical characteristics and territories, estimating motor-unit action potentials, specifying motor-unit discharge times, and imposing various levels of motor-unit synchronization. The output (EMG and force) was simulated at 11 levels of excitation, ranging from 5 to 100% of maximum. To synchronize motor-unit activity, selected motor-unit discharge times were adjusted; however, the number of motor units recruited and the average discharge rate of each unit was constant across synchronization conditions for a given level of excitation. Two levels of synchronization were imposed on the discharge times: a moderate and a high level, which approximated the experimentally observed range of motor-unit synchronization. The moderate level of synchrony caused the average EMG to increase by approximately 65%, whereas the high level caused a 130% increase in the EMG with respect to the no-synchrony condition. Neither synchrony condition influenced the magnitude of the average force. However, motor-unit synchronization did increase the amplitude of the fluctuations in the simulated force, especially at intermediate levels of excitation. In conclusion, motor-unit synchronization increased the amplitude of the average rectified EMG and decreased the steadiness of the force exerted by the muscle in simulated contractions.     

Motor-unit synchronization is not responsible for larger motor-unit forces in old adults

Motor-unit synchronization, which is a measure of the near simultaneous discharge of action potentials by motor units, has the potential to influence spike-triggered average force and the steadiness of a low-force isometric contraction. The purpose of the study was to estimate the contribution of motor-unit synchronization to the larger spike-triggered average forces and the decreased steadiness exhibited by old adults. Eleven young (age 19-30 yr) and 14 old (age 63-81 yr) adults participated in the study. Motor-unit activity was recorded with two fine-wire intramuscular electrodes in the first dorsal interosseus muscle during isometric contractions that caused the index finger to exert an abduction force. In a separate session, steadiness measurements were obtained during constant-force isometric contractions at target forces of 2.5, 5, 7. 5, and 10% of the maximum voluntary contraction (MVC) force. Mean (+/-SD) motor-unit forces measured by spike-triggered averaging were larger in old (15.5 +/- 12.1 mN) compared with young (7.3 +/- 5.7 mN) adults, and the differences were more pronounced between young (8.7 +/- 6.4 mN) and old (19.9 +/- 12.2 mN) men. Furthermore, the old adults had a reduced ability to maintain a steady force during an isometric contraction, particularly at low target forces (2.5 and 5% MVC). Mean (+/-SD) motor-unit synchronization, expressed as the frequency of extra synchronous discharges above chance in the cross-correlogram, was similar in young [0.66 +/- 0.4 impulses/s (imp/s); range, 0.35-1.51 imp/s; 53 pairs) and old adults (0.72 +/- 0.5 imp/s; range, 0.27-1.38 imp/s; 56 pairs). The duration of synchronous peaks in the cross-correlogram was similar for each group (approximately 16 ms). These data suggest that motor-unit synchronization is not responsible for larger spike-triggered average forces in old adults and that motor-unit synchronization does not contribute to the decreased steadiness of low-force isometric contractions observed in old adults.     

Motor-unit recruitment in human first dorsal interosseous muscle for static contractions in three different directions

Spike-triggered averaging was used to extract the twitch tensions and contraction times of 144 motor units from the first dorsal interosseous muscle of four subjects for three different directions of static contraction: abduction of the index finger, flexion of the index finger, and adduction of the thumb coupled with flexion of the index finger (hereafter referred to as adduction). Although the twitch tensions were generally largest for the abduction contraction, all units contributed tension to all three directions of contraction. A linear correlation was found for twitch tensions of motor units for the three directions of static contractions. Linear correlations were also found between twitch tension and threshold force of these motor units for each direction, which suggests that an orderly pattern of recruitment, according to increasing twitch size, adequately describes the function of human first dorsal interosseous muscle for all contraction directions. No clear evidence was found for separate groups of motor units in the muscle that were selectively activated for the different tasks. Rank order of recruitment for motor units in the three directions of contraction was correlated, but was not identical. The scatter in our data is discussed in relation to earlier reports of altered motor-unit recruitment during different movements.     

Motor-unit coherence during isometric contractions is greater in a hand muscle of older adults

The purpose of this study was to quantify the strength of motor-unit coherence from the first dorsal interosseus muscle in young and old adults using data obtained in a previous study, where no differences in motor-unit synchronization between the two groups were observed. The strength of motor-unit coherence was quantified from 47 motor-unit pairs in 11 young adults (age 24.1 +/- 4.1 yrs) and from 48 motor-unit pairs in 14 old adults (age 70.4 +/- 5.9 yrs). The strength of motor-unit coherence was greater in old adults, particularly at low frequencies of 5-9 Hz (85% greater in old adults at 5 Hz). In addition, the older adults expressed an extra oscillation at approximately 12-13 Hz that was not present in the young subjects. These data demonstrate that common oscillatory inputs to motor neurons (motor-unit coherence) are enhanced in older adults despite no age-related difference in the strength of shared inputs (synchronization). Furthermore, the data emphasize that measures of motor-unit synchronization and coherence highlight different features of the same common input, and a coherence analysis may be a more sensitive tool to characterize shared input to motor neurons.     

Removal of visual feedback alters muscle activity and reduces force variability during constant isometric contractions

The purpose of this study was to compare force accuracy, force variability and muscle activity during constant isometric contractions at different force levels with and without visual feedback and at different feedback gains. In experiment 1, subjects were instructed to accurately match the target force at 2, 15, 30, 50, and 70% of their maximal isometric force with abduction of the index finger and maintain their force even in the absence of visual feedback. Each trial lasted 22 s and visual feedback was removed from 8–12 to 16–20 s. Each subject performed 6 trials at each target force, half with visual gain of 51.2 pixels/N and the rest with a visual gain of 12.8 pixels/N. Force error was calculated as the root mean square error of the force trace from the target line. Force variability was quantified as the standard deviation and coefficient of variation (CVF) of the force trace. The EMG activity of the agonist (first dorsal interosseus; FDI) was measured with bipolar surface electrodes placed distal to the innervation zone. Independent of visual gain and force level, subjects exhibited lower force error with the visual feedback condition (2.53 ± 2.95 vs. 2.71 ± 2.97 N; P < 0.01); whereas, force variability was lower when visual feedback was removed (CVF: 4.06 ± 3.11 vs. 4.47 ± 3.14, P < 0.01). The EMG activity of the FDI muscle was higher during the visual feedback condition and this difference increased especially at higher force levels (70%: 370 ± 149 vs. 350 ± 143 μV, P < 0.01). Experiment 2 examined whether the findings of experiment 1 were driven by the higher force levels and proximity in the gain of visual feedback. Subjects performed constant isometric contractions with the abduction of the index finger at an absolute force of 2 N, with two distinct feedback gains of 15 and 3,000 pixels/N. In agreement with the findings of experiment 1, subjects exhibited lower force error in the presence of visual feedback especially when the feedback gain was high (0.057 ± 0.03 vs. 0.095 ± 0.05 N). However, force variability was not affected by the vastly distinct feedback gains at this force, which supported and extended the findings from experiment 1. Our findings demonstrate that although removal of visual feedback amplifies force error, it can reduce force variability during constant isometric contractions due to an altered activation of the primary agonist muscle most likely at moderate force levels in young adults.     

Non-invasive assessment of single motor unit mechanomyographic response and twitch force by spike-triggered averaging

A method for non-invasive assessment of single motor unit (MU) properties from electromyographic (EMG), mechanomyographic (MMG) and force signals is proposed. The method is based on the detection and classification of single MU action potentials from interference multichannel surface EMG signals and on the spike-triggered average of the MMG (detected by an accelerometer) and force signals. The first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles were investigated at contraction levels of 2% and 5% of the maximum voluntary contraction (MVC) force. A third contraction was performed by selective activation of a single MU with surface MU action potential visual feedback provided to the subject. At 5% MVC, the mean (±standard error) single MU MMG peak-to-peak value was 11.0±1.8 mm s⁻² (N=17) and 32.3±6.5 mm s⁻² (N=20) for the FDI and AMD muscles, respectively. The peak of the twitch force was, at the same contraction livel, 7.41±1.34 mN and 14.42±2.92 mN, for the FDI and ADM muscles, respectively. The peak-to-peak value of the MMG was significantly different for the same MU at different contraction levels, indicating a non-linear summation of the single MU contributions. For the FDI muscle, the MMG peak-to-peak value of individual MUs was 21.5±7.8 mm s⁻², when such MUs were activated with visual feedback provided to the subject, whereas, for the same MUs, it was 11.8±3.8 mm s⁻², when the subject maintained a constant force level of 2% MVC. The method proposed allows the non-invasive assessment of single MU membrane and contractile properties during voluntary contractions.     

Distribution of motor unit force in human extensor digitorum assessed by spike-triggered averaging and intraneural microstimulation

A peculiar aspect of the muscular organization of the human hand is that the main flexors and extensors of the fingers are muscles that each give rise to four parallel tendons that insert on all the fingers. It has been hypothesized that these multi-tendoned muscles are comprised of functional compartments, with each finger controlled by a discrete population of motor units. The purpose of this study was to determine the force distribution across the four fingers for motor units in human extensor digitorum (ED), a multi-tendoned muscle that extends the fingers. The force distribution was assessed by spike-triggered averaging and intraneural microstimulation for 233 and 18 ED units, respectively. A selectivity index from 0 (force equally distributed across the fingers) to 1.0 (force concentrated on a single finger) was used to quantify the distribution of motor unit force across the four digits. The mean selectivity index was high for ED motor units assessed with intraneural microstimulation (0.90 +/- 0.28) and was significantly greater than that obtained with spike-triggered averaging (0.38 +/- 0.14). Therefore it is likely that each finger is acted on by ED through a discrete population of motor units and that weak synchrony between motor units in different compartments of ED may have contributed to the appearance of spike-triggered average force on multiple fingers. Moreover, the high selectivity of motor units for individual fingers may provide the mechanical substrate needed for highly fractionated movements of the human hand.     

Menopause alters temperature sensitivity of muscle force in humans

Isometric maximum voluntary force (MVF) of the adductor pollicis and first dorsal interosseous muscles was measured in 11 pre- and 11 post-menopausal (Pre-M and Post-M) human subjects. The temperature of the hand varied in the range 18°–38°C by water immersion and skin temperature was recorded. MVF at each temperature was expressed relative to the value at skin temperature above 35°C to give MVF_REL. The form of the relation between MVF_REL and temperature was different in the Pre-M and Post-M groups (p < 0.01). In the Pre-M group the maximum value of MVF_REL occurred near 30°C and force fell at both higher and lower temperatures. In the Post-M group MVF_REL showed an approximately linear decline with cooling across the whole temperature range. The maximum value of MVF_REL for the Post-M group was near 35°C. The values of MVF_REL for the Post-M group were significantly lower than for the Pre-M group at temperatures between 18° and 30°C.     

Bilateral and unilateral contractions: possible differences in maximal voluntary force.

The issue of whether there is a difference in the amount of force produced from a simultaneous two-limb maximal contraction compared to the sum of individual one-limb contractions has received considerable debate in the literature. A bilateral deficit (BLD) is when the resultant force from bilateral homonymous limb contractions is less than the summed force of individual limb contractions. Determining whether differences exist between one- and two-limb movements may provide insight into complex neuromuscular control patterns. Many dynamic two-limb studies report a BLD, whereas isometric studies are more numerous and controversial. It is important to categorize the movements studied in order to establish consistency. This paper purports that the BLD is an unstable phenomenon, and its presence should be considered in the context of the movement studied. Most likely, this phenomenon is dependent upon some minor deviation in descending drive between the cortical level and peripheral motor neuron     

Multiple features of motor-unit activity influence force fluctuations during isometric contractions

To identify the mechanisms responsible for the fluctuations in force that occur during voluntary contractions, experimental measurements were compared with simulated forces in the time and frequency domains at contraction intensities that ranged from 2 to 98% of the maximum voluntary contraction (MVC). The abduction force exerted by the index finger due to an isometric contraction of the first dorsal interosseus muscle was measured in 10 young adults. Force was simulated with computer models of motor-unit recruitment and rate coding for a population of 120 motor units. The models varied recruitment and rate-coding properties of the motor units and the activation pattern of the motor-unit population. The main finding was that the experimental observations of a minimum in the coefficient of variation (CV) for force (1.7%) at approximately 30% MVC and a plateau at higher forces could not be replicated by any of the models. The model that increased the level of short-term synchrony with excitatory drive provided the closest fit to the experimentally observed relation between the CV for force and the mean force. In addition, the results for the synchronization model extended previous modeling efforts to show that the effect of synchronization is independent from that of discharge-rate variability. Most of the power in the force power spectra for the models was contained in the frequency bins below 5 Hz. Only a model that included a low-frequency oscillation in excitation, however, could approximate the experimental finding of peak power at a frequency below 2 Hz: 38% of total power at 0.99 Hz and 43% at 1.37 Hz, respectively. In contrast to the experimental power spectra, all model spectra included a second peak at a higher frequency. The secondary peak was less prominent in the synchronization model because of greater variability in discharge rate. These results indicate that the variation in force fluctuations across the entire operating range of the muscle cannot be explained by a single mechanism that influences the output of the motor-unit population.     

Parallel neuronal mechanisms underlying physiological force tremor in steady muscle contractions of humans

We present results from a study of the 6-to 12-Hz force tremor in relation to motor unit (MU) firing synchrony. Our experimental observations from 32 subjects, 321 contractions, and 427 recorded MUs reveal that tremor is accompanied by corresponding, in-phase MU rhythms that are additional to the ones at the MU intrinsic firing rates. This rhythmical synchrony is widespread and has a uniform strength that ranges from near zero to very large (MU/MU coherence > 0.50) in different contractions. Both the synchrony and the tremor are suppressed during ischemia, and this strongly suggests an involvement of spindle feedback in their generation. Furthermore, in the presence of substantial synchrony, the tremor enhancement, relative to the minimal tremor of ischemia, reflects the strength of the synchrony. Theoretical considerations based on these observations indicate that the muscle force signal is expected to show 1) frequency components in the band of the firing rates of the last-recruited, large MUs, and 2) because of the synchronized MU rhythms, an additional, distinct component with a size reflecting the strength of synchrony. Furthermore, synchronized MU rhythms, with frequencies in the 6- to 12-Hz range, are expected to arise from self-oscillations in the monosynaptic stretch reflex loop, due primarily to the associated muscle delay (several tens of milliseconds). Our results therefore reveal the parallel action of two tremor mechanisms, one of which involves MU synchrony probably caused by loop action. Clearly, the results on the synchrony and its impact also apply to other possible generators of tremor synchrony, including supraspinal ones.     

Reductions in recruitment force thresholds in human single motor units by successive voluntary contractions

Summary Recruitment force thresholds of biceps brachii single motor units were studied in 4 male subjects before and after an isometric muscle contraction, passive muscle stretch, or following successive muscle contractions, muscle stretches or during alternations between muscle stretches and muscle contractions. Isometric muscle contractions of 5 s duration decreased subsequent single motor unit force thresholds. These force thresholds could usually be reset at or near precontraction force threshold values by passive muscle stretch induced by elbow extension. Single motor units showing reduced force thresholds following contraction were momentarily derecruited during and/or after muscle stretch. Successive muscle stretches alone did not significantly alter single motor unit force thresholds. In contrast, single motor unit recruitment force thresholds during successive weaker contractions were progressively lowered. Intercontraction muscle stretches maintained the single motor unit force thresholds at or near the initial force threshold level. The mechanism(s) underlying a muscle contraction-induced lowering of single motor unit force thresholds may reside in stretch reflex pathways.