Motor unit synchronization in FDI and biceps brachii muscles of strength-trained males

Motor unit (MU) synchronization is the simultaneous or near-simultaneous firing of two MUs which occurs more often than would be expected by chance. The present study sought to investigate the effects of exercise training, muscle group, and force level, by comparing the magnitude of synchronization in the biceps brachii (BB) and first dorsal interosseous (FDI) muscles of untrained and strength-trained college-aged males at two force levels, 30% of maximal voluntary contraction (MVC) and 80% MVC. MU action potentials were recorded directly via an intramuscular needle electrode. The magnitude of synchronization was assessed using previously-reported synchronization indices: k′, E, and CIS. Synchronization was significantly higher in the FDI than in the BB. Greater synchronization was observed in the strength-trained group with CIS, but not with E or k′. Also, synchronization was significantly greater at 80% MVC than at 30% MVC with E, but only moderately greater with CIS and there was no force difference with k′. Synchronization prevalence was found to be greater in the BB (80.1%) than in the FDI (71.5%). Thus, although the evidence is a bit equivocal, it appears that MU synchronization is greater at higher forces, and greater in strength-trained individuals than in untrained subjects.     

Modeling investigation of learning a fast elbow flexion in the horizontal plane—prediction of muscle forces and motor units action

Experimental investigation of practicing a dynamic, goal-directed movement reveals significant changes in kinematics. Modeling can provide insight into the alterations in muscle activity, associated with the kinematic adaptations, and reveal the potential motor unit (MU) firing patterns that underlie those changes. In this paper, a previously developed muscle model and software (Raikova and Aladjov, Journal of Biomechanics, 35, 2002) have been used to investigate changes in MU control, while practicing fast elbow flexion to a target in the horizontal plane. The first trial (before practice) and the last trial (after extensive practice) of two subjects have been simulated. The inputs for the simulation were the calculated external moments at the elbow joint. The external moments were countered by the action of three flexor muscles and two extensor ones. The muscles have been modeled as a mixture of MUs of different types. The software has chosen the MU firing times necessary to accomplish the movement. The muscle forces and MUs firing statistics were then calculated. Three hypotheses were tested and confirmed: (1) peak muscle forces and antagonist co-contraction increase during training; (2) there is an increase in the firing frequency and the synchronization between MUs; and (3) the recruitment of fast-twitch MUs dominates the action.     

Modeling investigation of learning a fast elbow flexion in the horizontal plane--prediction of muscle forces and motor units action

Experimental investigation of practicing a dynamic, goal-directed movement reveals significant changes in kinematics. Modeling can provide insight into the alterations in muscle activity, associated with the kinematic adaptations, and reveal the potential motor unit (MU) firing patterns that underlie those changes. In this paper, a previously developed muscle model and software (Raikova and Aladjov, Journal of Biomechanics, 35, 2002) have been used to investigate changes in MU control, while practicing fast elbow flexion to a target in the horizontal plane. The first trial (before practice) and the last trial (after extensive practice) of two subjects have been simulated. The inputs for the simulation were the calculated external moments at the elbow joint. The external moments were countered by the action of three flexor muscles and two extensor ones. The muscles have been modeled as a mixture of MUs of different types. The software has chosen the MU firing times necessary to accomplish the movement. The muscle forces and MUs firing statistics were then calculated. Three hypotheses were tested and confirmed: (1) peak muscle forces and antagonist co-contraction increase during training; (2) there is an increase in the firing frequency and the synchronization between MUs; and (3) the recruitment of fast-twitch MUs dominates the action.     

The muscle sound properties of different muscle fiber types during voluntary and electrically induced contractions.

Soundmyogram (SMG) and electromyogram signals were recorded simultaneously from the relatively fast medial gastrocnemius (MG) and slow soleus (SOL) during voluntary and electrically induced contractions. Using a spike-triggered averaging technique, the averaged elementary sound and corresponding MU spikes were also obtained from about 35 different MUs identified. The rms-SMG of MG increased as a function of force (P < 0.01). On the contrary, these values for SOL increased up to 60% MVC (P < 0.01), but decreased at 80% MVC. The relationship between the peak to peak amplitude of SMG and MU spike indicated significant positive correlations (r = 0.631 to approximately 0.657, P < 0.01). During electrical stimulation at 5 Hz, the SMG power spectral peak frequency (PF) was matched with stimulation frequency in both muscles. At higher stimulation frequencies, e.g., > 15 Hz, only in the MG was SMG-PF synchronized with stimulation frequency; the slow SOL did not show such synchronization. Our data suggest that the SMG frequency components might reflect active motor unit firing rates, and that the SMG amplitude depends upon mechanical properties of contraction, muscle fiber composition, and firing rate during voluntary and electrically induced contractions.     

Correlation between discharges of human motor units during prolonged muscle contraction

Motor unit (MU) potentials were recorded from the human rectus femoris and biceps brachii muscles during prolonged isometric contraction. Interspike intervals and intervals between adjacent discharges of 2 MUs (cross-intervals of MU pairs) were measured. Synchronization was expressed by the following criteria: the cross-interval histogram; comparison of the number of coincidences between discharges of 2 MUs observed experimentally with the mean probable number of coincidences; the frequency of appearance of N successive coincidences of spikes from different MU pairs; comparison of the mean duration of interspike intervals preceding a synchronized discharge with the mean duration of the remaining interspike intervals for the same MU. For some MU pairs the number of coinciding spikes was greater than the expected number of random coincidences. Synchronized spikes could form a train of consecutive coincidences. The mean duration of interspike intervals preceding a synchronized discharge was somewhat less than the mean duration of the remaining interspike intervals for MUs forming a synchronously firing pair.Institute of Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 4, No. 1, pp. 68–74, January–February, 1972.     

Effect of synchronization of firings of different motor unit types on the force variability in a model of the rat medial gastrocnemius muscle

The synchronized firings of active motor units (MUs) increase the oscillations of muscle force, observed as physiological tremor. This study aimed to investigate the effects of synchronizing the firings within three types of MUs (slow—S, fast resistant to fatigue–FR, and fast fatigable–FF) on the muscle force production using a mathematical model of the rat medial gastrocnemius muscle. The model was designed based on the actual proportion and physiological properties of MUs and motoneurons innervating the muscle. The isometric muscle and MU forces were simulated by a model predicting non-synchronized firing of a pool of 57 MUs (including 8 S, 23 FR, and 26 FF) to ascertain a maximum excitatory signal when all MUs were recruited into the contraction. The mean firing frequency of each MU depended upon the twitch contraction time, whereas the recruitment order was determined according to increasing forces (the size principle). The synchronization of firings of individual MUs was simulated using four different modes and inducing the synchronization of firings within three time windows (± 2, ± 4, and ± 6 ms) for four different combinations of MUs. The synchronization was estimated using two parameters, the correlation coefficient and the cross-interval synchronization index. The four scenarios of synchronization increased the values of the root-mean-square, range, and maximum force in correlation with the increase of the time window. Greater synchronization index values resulted in higher root-mean-square, range, and maximum of force outcomes for all MU types as well as for the whole muscle output; however, the mean spectral frequency of the forces decreased, whereas the mean force remained nearly unchanged. The range of variability and the root-mean-square of forces were higher for fast MUs than for slow MUs; meanwhile, the relative values of these parameters were highest for slow MUs, indicating their important contribution to muscle tremor, especially during weak contractions.     

Modelling motor units in 3D: influence on muscle contraction and joint force via a proof of concept simulation

Functional heterogeneity is a skeletal muscle’s ability to generate diverse force vectors through localised motor unit (MU) recruitment. Existing 3D macroscopic continuum-mechanical finite element (FE) muscle models neglect MU anatomy and recruit muscle volume simultaneously, making them unsuitable for studying functional heterogeneity. Here, we develop a method to incorporate MU anatomy and information in 3D models. Virtual fibres in the muscle are grouped into MUs via a novel “virtual innervation” technique, which can control the units’ size, shape, position, and overlap. The discrete MU anatomy is then mapped to the FE mesh via statistical averaging, resulting in a volumetric MU distribution. Mesh dependency is investigated using a 2D idealised model and revealed that the amount of MU overlap is inversely proportional to mesh dependency. Simultaneous recruitment of a MU’s volume implies that action potentials (AP) propagate instantaneously. A 3D idealised model is used to verify this assumption, revealing that neglecting AP propagation results in a slightly less-steady force, advanced in time by approximately 20 ms, at the tendons. Lastly, the method is applied to a 3D, anatomically realistic model of the masticatory system to demonstrate the functional heterogeneity of masseter muscles in producing bite force. We found that the MU anatomy significantly affected bite force direction compared to bite force magnitude. MU position was much more efficacious in bringing about bite force changes than MU overlap. These results highlight the relevance of MU anatomy to muscle function and joint force, particularly for muscles with complex neuromuscular architecture.

     

Summation of slow motor unit forces at constant and variable interpulse intervals in rat soleus muscle

Effects of the summation of forces generated by functionally isolated slow-twitch motor units (MU) of the rat soleus muscle were examined in this study. Initially, the twitch, fused tetanic and unfused tetanic contractions evoked by trains of stimuli at variable interpulse intervals were recorded for each MU. Then, two, three or four MUs were co-activated, and the recorded forces were compared to the algebraic sum of the forces of individual MUs. The mean cumulative force of twitches and the mean cumulative force of fused tetani were not statistically different from the respective algebraic sums of forces, which revealed a high degree of linearity in the summation. However, relaxation of the recorded tetanic contractions (either fused or unfused) was faster than that predicted by the linear summation of individual contractions. Moreover, for twitch and tetanic contractions, a tendency to shorten relaxation with an increasing number of co-active MUs was noted. The results indicate that forces of rat soleus slow MUs sum up more linearly than in the respective cat muscle as well as more linearly than for fast MUs in the medial gastrocnemius muscle.     

Human motor unit recruitment and derecruitment during long lasting intermittent contractions.

Seven healthy subjects were investigated in cyclic ramp-and-hold long lasting isometric contractions. Wire branched electrodes were used for selective recording of single motor unit (MU) potentials from m. biceps brachii. MU behaviour was defined in terms of recruitment/derecruitment thresholds (RT and DT) and the duration of interspike intervals (ISI). A total of 63 MUs was investigated: 40 units were active from the beginning of the task performance and another 23 were recruited later. There were no changes in the recruitment pattern of MUs with fatigue development - a short first ISI followed by a very long second one and an almost constant firing rate after this transient phase. The tendency of RT to gradually decrease dominates the results. Thus, the required constant rate of force increase with fatigue development was maintained mostly by the mechanisms of space coding (i.e., decrease of RT and recruitment of additional MUs). Oppositely, the time behaviour of the DT changes was not uniform and rate coding was an essential mechanism in the adaptation of MU activity to muscle fatigue during relaxation phases. The recruitment pattern and fatigue related behaviour of the additionally recruited MUs were similar to those of MUs active from the first cycle of the motor task performance.     

Investigation of motor unit recruitment during stimulated contractions of tibialis anterior muscle

This work investigated motor unit (MU) recruitment during transcutaneous electrical stimulation (TES) of the tibialis anterior (TA) muscle, using experimental and simulated data. Surface electromyogram (EMG) and torque were measured during electrically-elicited contractions at different current intensities, on eight healthy subjects.EMG detected during stimulation (M-wave) was simulated selecting the elicited MUs on the basis of: (a) the simulated current density distribution in the territory of each MU and (b) the excitation threshold characteristic of the MU. Exerted force was simulated by adding the contribution of each of the elicited MUs. The effects of different fat layer thickness (between 2 and 8 mm), different distributions of excitation thresholds (random excitation threshold, higher threshold for larger MUs or smaller MUs), and different MU distributions within the muscle (random distribution, larger MU deeper in the muscle, smaller MU deeper) on EMG variables and torque were tested.Increase of the current intensity led to a first rapid increase of experimental M-wave amplitude, followed by a plateau. Further increases of the stimulation current determined an increase of the exerted force, without relevant changes of the M-wave. Similar results were obtained in simulations.Rate of change of conduction velocity (CV) and leading coefficient of the second order polynomial interpolating the force vs. stimulation level curve were estimated as a function of increasing current amplitudes. Experimental data showed an increase of estimated CV with increasing levels of the stimulation current (for all subjects) and a positive leading coefficient of force vs. stimulation current curve (for five of eight subjects). Simulations matched the experimental results only when larger MUs were preferably located deeper in the TA muscle (in line with a histochemical study). Marginal effect of MU excitation thresholds was observed, suggesting that MUs closer to the stimulation electrode are recruited first during TES regardless of their excitability.     

Effects of whole body vibration on motor unit recruitment and threshold

Whole body vibration (WBV) has been suggested to elicit reflex muscle contractions but this has never been verified. We recorded from 32 single motor units (MU) in the vastus lateralis of 7 healthy subjects (34 ± 15.4 yr) during five 1-min bouts of WBV (30 Hz, 3 mm peak to peak), and the vibration waveform was also recorded. Recruitment thresholds were recorded from 38 MUs before and after WBV. The phase angle distribution of all MUs during WBV was nonuniform (P < 0.001) and displayed a prominent peak phase angle of firing. There was a strong linear relationship (r = -0.68, P < 0.001) between the change in recruitment threshold after WBV and average recruitment threshold; the lowest threshold MUs increased recruitment threshold (P = 0.008) while reductions were observed in the higher threshold units (P = 0.031). We investigated one possible cause of changed thresholds. Presynaptic inhibition in the soleus was measured in 8 healthy subjects (29 ± 4.6 yr). A total of 30 H-reflexes (stimulation intensity 30% Mmax) were recorded before and after WBV: 15 conditioned by prior stimulation (60 ms) of the antagonist and 15 unconditioned. There were no significant changes in the relationship between the conditioned and unconditioned responses. The consistent phase angle at which each MU fired during WBV indicates the presence of reflex muscle activity similar to the tonic vibration reflex. The varying response in high- and low-threshold MUs may be due to the different contributions of the mono- and polysynaptic pathways but not presynaptic inhibition.     

The fatigability of two agonistic muscles in human isometric voluntary submaximal contraction: an EMG study. II. Motor unit firing rate and recruitment

The recruitment and firing rate of biceps brachii (BB) and brachioradialis (BR) motor units (MUs) were studied in the course of fatiguing isometric contractions at 20%-30% of maximal voluntary contraction (MVC). MU recruitment generally occurred throughout the maintained contraction and was similar for BB and BR muscles. Newly recruited MUs started to discharge in the form of bursts, the duration of which increased until a continuous rhythmical firing was achieved. Within each burst, the first interval between two consecutive discharges was usually the shortest. MU threshold was lowered just after the limit time of the maintained contraction. The MU's firing rate either increased or remained stable as a function of the elapsed time. It is concluded that (1) in fatiguing isometric contractions at 20%-30% MVC contractile failure is mainly compensated for by MU recruitment and a lowered MU threshold and (2) differences between in surface changes in the electromyogram of BB and BR muscles cannot easily be explained by related differences in MU firing rate and recruitment.     

Effect of aging on properties of motor unit action potentials in the rat medial gastrocnemius muscle

The purpose of this study was to investigate whether age-related changes in motor unit (MU) contractile properties are reflected in parameters of motor unit action potentials (MUAPs). MUs of the medial gastrocnemius muscle were functionally isolated in anaesthetized Wistar rats. A control group of young animals (5–10 mo) was compared to two groups of old rats (24–25 mo and 28–30 mo). The basic contractile properties of MUs as well as the amplitude, total duration, peak-to-peak time, and number of turns within MUAPs were measured. Effects of aging were mainly observed for fast fatigable MUs (a prolongation of MUAPs and increased number of turns). The MUAP amplitude did not change significantly with aging in either MU type, but it correlated to the twitch or tetanic forces, which tended to increase with age, especially for slow MUs. We concluded that the prolongation of MUAPs and the greater incidence of signal turns was probably a result of a decrease in muscle fiber conduction velocity and/or an increase in their dispersion, and enlargement of MU territories – presumably caused by axonal sprouting of surviving motoneurons. The latter might also be responsible for the observed age-related tendency for a increase in MUAP amplitudes in slow MUs.     

Comparative analysis of motor unit action potentials of the medial gastrocnemius muscle in cats and rats

Properties of motor unit action potentials (MUAPs) were compared for medial gastrocnemius (MG) motor units (MUs) in cats and rats. The experiments on functionally isolated MUs were performed under general anaesthesia, under comparable conditions (surgery, stimulating protocol and recording methods) for both species investigated. The proportions of motor units and contractile properties of the sample used in the study were consistent with previous studies performed on the MG muscle in both animal species, so comparisons of action potentials of individual types of MUs were acknowledged as fully reliable. The most prominent differences concerning MUAPs were observed in total duration and peak-to-peak times which for all MU types were about twice longer in cat MUs, in comparison to the rat MUs. The considerable disproportions were observed between the MUAP amplitudes of FF (fast fatigable), FR (fast resistant to fatigue) and S (slow) MUs in each species (the highest amplitudes were measured for FF and the lowest for S MUs), but there were no significant differences between cat and rat when respective types of MUs were compared. The shapes of MUAPs were commonly characterized by biphasic waveforms composed of two or three turns in all types of units, and no interspecies differences were revealed. Several factors influencing MUAP parameters were discussed indicating most of all importance of variable length of cat and rat muscle fibres and ambiguous influence of motor unit size, thickness of muscle fibres and their density around the recording electrode in the MG muscle of both species.     

Motor unit tracking with high-density surface EMG

Following (tracking) individual motor units over time can provide important new insights, both into the relationships among various motor unit (MU) morphological and functional properties and into how these properties are influenced by neuromuscular disorders or interventions. The present study aimed to determine whether high-density surface EMG (HD-sEMG) recordings, which use an array of surface electrodes over a muscle, can increase the yield of MU tracking studies in terms of the number of MUs that can be tracked. For that purpose, four HD-sEMG recording sessions were performed on the thenar muscles of ten healthy subjects. Decomposition of the recorded composite responses yielded a study total of 2849 motor unit action potentials (MUAPs). MUAPs that were found in both of the first two sessions, performed on the same day, were defined as trackable MUAPs. Our results show that 22 (median value; range, 13–34) MUAPs per nerve were trackable, which represented approximately 5% of the total MU population. Of these trackable MUAPs, 16 (11–26) could also be found in one or both of the third and fourth sessions, which were performed between 1 and 13 weeks after the initial studies. Nine (4–18) MUAPs were found in all four sessions. Many of the characteristic MUAP shapes matched well between sessions, even when these sessions were several weeks apart. However, some MUAPs seem very sensitive to changes in arm position or in the muscle’s morphology (e.g., to changes in muscle fiber length due to variable degrees of thumb flexion or extension), particularly those from larger and/or superficial MUs. Standardization is, therefore, essential to detect even small MUAP changes, as may occur with pathology or interventions. If this is accomplished, MU tracking with HD-sEMG may prove to be a powerful tool for a promising type of neurophysiological investigation.     

Using two-dimensional spatial information in decomposition of surface EMG signals.

Recently, high-density surface EMG electrode grids and multi-channel amplifiers became available for non-invasive recording of human motor units (MUs). We present a way to decompose surface EMG signals into MU firing patterns, whereby we concentrate on the importance of two-dimensional spatial differences between the MU action potentials (MUAPs). Our method is exemplified with high-density EMG data from the vastus lateralis muscle of a single subject. Bipolar and Laplacian spatial filtering was applied to the monopolar raw signals. From the single recording in this subject six different simultaneously active MUs could be distinguished using the spatial differences between MUAPs in the direction perpendicular to the muscle fiber direction. After spike-triggered averaging, 125-channel two-dimensional MUAP templates were obtained. Template-matching allowed tracking of all MU firings. The impact of spatial information was measured by using subsets of the MUAP templates, either in parallel or perpendicular to the muscle fiber direction. The use of one-dimensional spatial information perpendicular to the muscle fiber direction was superior to the use of a linear array electrode in the longitudinal direction. However, to detect the firing events of the MUs with a high accuracy, as needed for instance for estimation of firing synchrony, two-dimensional information from the complete grid electrode appears essential.     

Impairment of human soleus motor units during ischemia

It is generally accepted that ischemia produced by limb compression affects rapidly conducting large-diameter Ia afferents in the early stage and that the motor nerve-muscle complex is blocked later. This notion, however, seems to be controversial for several reasons, so an attempt to reveal the amount of motor unit (MU) impairment during ischemia was made. Observation of human soleus muscle electromyographic (EMG) signal recorded either by bipolar needle electrode or by surface electrodes at various levels of voluntary contraction during the course of ischemia showed that low-threshold small MUs were affected first while high-threshold large MUs survived longer. The changes in EMG patterns were temporally correlated with T-reflex deterioration. It is suggested that the early loss of low-threshold MUs may play a definite role in alterations of reflexes during ischemia.     

A model for steady isometric muscle activation

The present model of the motoneuronal (MN) pool – muscle complex (MNPMC) is deterministic and designed for steady isometric muscle activation. Time-dependent quantities are treated as time-averages. The character of the model is continuous in the sense that the motor unit (MU) population is described by a continuous density function. In contrast to most already published models, the wiring (synaptic weight) between the input fibers to the MNPMC and the MNs (about which no detailed data are known) is deduced, whereas the input–force relation is given. As suggested by experimental data, this relation is assumed to be linear during MU recruitment, but the model allows other, nonlinear relations. The input to the MN pool is defined as the number of action potentials per second in all input fibers, and the excitatory postsynaptic potential (EPSP) conductance in MNs evoked by the input is assumed to be proportional to the input. A single compartment model with a homogeneous membrane is used for a MN. The MNs start firing after passing a constant voltage threshold. The synaptic current–frequency relation is described by a linear function and the frequency–force transformation of a MU by an exponential function. The sum of the MU contraction forces is the muscle force, and the activation of the MUs obeys the size principle. The model parameters were determined a priori, i.e., the model was not used for their estimation. The analysis of the model reveals special features of the activation curve which we define as the relation between the input normalized by the threshold input of the MN pool and the force normalized by the maximal muscle force. This curve for any muscle turned out to be completely determined by the activation factor, the slope of the linear part of the activation curve (during MU recruitment). This factor determines quantitatively the relation between MU recruitment and rate modulation. This property of the model (the only known model with this property) allows a quantification of the recruitment gain (Kernell and Hultborn 1990). The interest of the activation factor is illustrated using two human muscles, namely the first dorsal interosseus muscle, a small muscle with a relatively small force at the end of recruitment, and the medial gastrocnemius muscle, a strong muscle with a relatively large force at the end of recruitment. It is concluded that the present model allows us to reproduce the main features of muscle activation in the steady state. Its analytical character facilitates a deeper understanding of these features. Received: 24 November 1997 / Accepted in revised form: 30 November 1998     

Discharge properties of human motor units during sustained contraction at low level force.

The characteristic of discharge behaviors of motor units (MUs) during low level contraction was investigated. The discharge of MUs in the m. vastus medialis was observed during the sustained contraction at 4 different levels below 10% MVC (2, 4, 8 and 10% MVC) for 15 min. The spike interval of all observed MUs gradually elongated during an initial several minutes of the contraction and the characteristic discharge patterns following the elongation were observed. i.e. continuous discharge throughout the contraction (CONT), decruitment (D-N), and re-recruitment following decruitment (D-REC).The relationship between recruitment threshold force (F(th)) and discharge pattern was not significant at 2% MVC but, at 10% MVC, there were significant differences in F(th) between D-N and CONT, and between D-REC and CONT MU populations.In pooled data, the MUs with the shorter mean spike interval at the beginning of the contraction (MSI(0), below 90 ms) tend to discharge continuously, but the MUs with longer MSI(0) showed various discharge patterns.In conclusion, during low level contraction MUs discharge characteristically, and the MU with high excitation levels tend to discharge continuously, but individual MU represents an intrinsic discharge pattern at not a high excitation level.