Work organization of a group of human motoneurons during voluntary muscular contraction

Needle electrodes were used to record action potentials of motor units of the rectus femoris muscle during isometric contraction (up to 50% of maximal). Up to 10 motor units working simultaneously could be identified. Under strictly stable conditions of muscular contraction the recruitment order of the motoneurons was constant. The firing rate was inversely proportional as a rule to this recruitment order. As a rule the changes in frequency connected with voluntary contraction of measured strength were in the same direction for different motoneurons. Statistical analysis of the frequency fluctuations observed during contraction of constant strength revealed direct correlation between them. The behavior of the motoneurons as described above is regarded as the result of the diffuse, indeterminate distribution of the synaptic input in the group of motoneurons innervating the muscle studied. It was also shown that even under stable conditions individual motoneurons or groups of them sometimes fired independently. During the performance of different types of movements, the firing rates of the recruited motoneurons varied in different directions and some motoneurons were replaced by others. This shows that when motoneurons function under natural conditions they use not only a common (indeterminate) but also a determinate input.Institute of Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 5, No. 1, pp. 77–87, January–February, 1973.     

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.     

Double discharges in human motoneurons

Potentials of motor units from the trapezius and rectus femoris muscles were recorded with selective needle electrodes during weak and moderately strong voluntary isometric contraction. The sequence of interspike intervals was analyzed. Double discharges (interspike interval not exceeding 20 msec) were found most commonly during recruiting of the motor units, but also at its end. Intervals between double discharges arising while the motor units were firing at a mean rate of 10–18 spikes/sec were outside the limits of statistical scatter of the remaining intervals. Double discharges were recorded chiefly in high-threshold units. The mean interval between double discharges recorded from the trapezius muscle was significantly smaller and the double discharges appeared considerably more often than in the rectus femoris muscle. Comparison of the results of these experiments with those obtained by other workers showed correlation between the mean duration of the interval between the double discharges and the duration of delayed depolarization of the motoneuron; this fact probably plays an important role in the creation of double discharges.     

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.     

Pattern of human motoneuron activity during voluntary muscular contraction

The pattern of motor unit activity of the rectus femoris muscle during isometric contraction was studied. Interspike interval sequences were analyzed. At frequencies below 8–10/sec the interval histograms were asymmetrical (long intervals predominated), the standard deviation was high and depended on the mean interval, and adjacent intervals were independent. At frequencies above 10–13/sec the interval distribution became normal in type, the standard deviation was low and independent of the mean interval duration, and negative correlation was found between adjacent intervals. During brief contraction specific for this particular (fast) muscle the activity of most neurons was of the second type, while during prolonged contraction it was of the first type. The change from activity of the first to the second type took place approximately when, with an increase in frequency, spikes began to appear against the background of after-hyperpolarization. A hypothesis is put forward to the effect that after-hyperpolarization creates the rhythm of activity (low variability of the intervals), and that the duration of after-hyperpolarization is correlated with the lower limit of working frequencies of the motoneurons. The motoneuron is regarded as performing not only a summating, but also a damping function, reducing the effect of random fluctuations of the synaptic inflow and coding information for transmission as a mean frequency.Institute of Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 3, No. 6, pp. 609–619, November–December, 1971.     

Failure of neuromuscular propagation during human maximal voluntary contraction

The mechanism for fatigue of the adductor pollicis was studied in normal subjects during maximal voluntary contractions (MVC) sustained for 90-100 s, by comparing the force and electrical response of this muscle to voluntary motor drive with that obtainable with artificial stimulation of the ulnar nerve. The adequacy of nerve stimulation was checked by recording simultaneously the electrical response of a nonfatiguing muscle, the abductor of the small finger. The decrease in force and in the natural electrical activity with fatigue was accompanied by a parallel decrease in the amplitude of synchronous muscle action potentials (M waves) evoked by artificial stimulation of the ulnar nerve at different frequencies. The decline in M-wave amplitude in the adductor pollicis was not due to a submaximal nerve stimulation, since the amplitudes recorded simultaneously from the nonfatiguing abductor digiti minimi remained unchanged. The force and the electrical responses from the adductor pollicis recovered in parallel with a half time of approximately 1 min. These results suggest that the loss of force of the adductor pollicis with fatigue and its subsequent recovery are largely determined by the extent of neuromuscular propagation failure. The slow recovery of the M-wave amplitude during repetitive stimulation suggests that it may be related to some aspect of muscle metabolism.     

Propagation direction of natural mechanical oscillations in the biceps brachii muscle during voluntary contraction

The aim of the study was to determine the directionality of the coupling of mechanical vibrations across the biceps brachii muscle at different frequencies of interest during voluntary contraction. The vibrations that are naturally generated by skeletal muscles were recorded by a two-dimensional array of skin mounted accelerometers over the biceps brachii muscle (surface mechanomyogram, S-MMG) during voluntary isometric contractions in ten healthy young men. As a measure of the similarity of vibration between a given pair of accelerometers, the spatial coherence of S-MMG at low (f < 25 Hz) and high (f > 25 Hz) frequency bands were investigated to determine if the coupling of the natural mechanical vibrations were due to the different physiological muscle activity at low and high frequencies. In both frequency bands, spatial coherence values for sensor pairs aligned longitudinally along the proximal to distal ends of the biceps were significantly higher compared with those for the sensor pairs oriented perpendicular to the muscle fibers. This difference was more evident at the higher frequency band. The findings indicated that coherent mechanical oscillations mainly propagated along the longitudinal direction of the biceps brachii muscle fibers at high frequencies (f > 25 Hz).     

Viscous properties of human muscle during contraction.

The purpose of this study was to determine viscous properties of human muscle during plantarflexion efforts. Experiments were performed on 17 subjects with an ankle ergometer allowing sinusoidal oscillations during isometric contractions and isokinetic movements. Sinusoidal oscillations led to the expression of (i) Bode diagrams of the musculo-articular system allowing the determination of a damping coefficient (Bbode); and (ii) a viscous coefficient (Bsin) using an adaptation of Hill's equation to sinusoidal oscillations. Isokinetic movements led to torque-velocity relationships. They showed a fall in torque associated to an increase in angular velocity what was quantified by calculating a damping coefficient (Biso). Both experiments gave consistent results indicating that Bbode was the lowest viscous parameter. This difference is discussed in terms of (i) "analog" viscosity originating from muscle cross-bridges; and (ii) real mechanical damping of passive structures.     

Low frequency sounds from sustained contraction of human skeletal muscle.

Low frequency audible vibrations are produced by human skeletal muscles undergoing sustained contraction. The effect is easily demonstrable with an electronic stethoscope which amplifies sound below 50 Hz. Autocorrelation analysis of the signal shows that it is periodic with a frequency 25 +/- 2.5 Hz. The quality of the sound is the same for all the skeletal muscles tested and is unaffected by changes in tension, ambient temperature, and blood flow. Electrically-stimulated contraction produces a sound which is indistinguishable from voluntary contraction. The amplitude of the sound increases linearly with tension. The sound signals are uncorrelated both in frequency and phase with electromyographic signals obtained simultaneously while the muscle is contacted. Arguments are presented to show that the sounds may be an intrinsic property of muscle contraction.     

Non-uniform mechanical activity of quadriceps muscle during fatigue by repeated maximal voluntary contraction in humans

To determine the non-uniform surface mechanical activity of human quadriceps muscle during fatiguing activity, surface mechanomyogram (MMG), or muscle sound, and surface electromyogram (EMG) were recorded from the rectus femoris (RF), vastus lateralis (VL), and vastus medialis (VM) muscles of seven subjects during unilateral isometric knee extension exercise. Time- and frequency-domain analyses of MMG and of EMG fatigued by 50 repeated maximal voluntary contractions (MVC) for 3 s, with 3-s relaxation in between, were compared among the muscles. The mean MVC force fell to 49.5 (SEM 2.0)% at the end of the repeated MVC. Integrated EMG decreased in a similar manner in each muscle head, but a marked non-uniformity was found for the decline in integrated MMG (iMMG). The fall in iMMG was most prominent for RF, followed by VM and VL. Moreover, the median frequency of MMG and the relative decrease in that of EMG in RF were significantly greater (P < 0.05) than those recorded for VL and VM. These results would suggest a divergence of mechanical activity within the quadriceps muscle during fatiguing activity by repeated MVC. Accepted: 19 January 1999     

State of monosynaptic reflex (H reflex) arc during voluntary muscle contraction in humans

Effect of an isometric voluntary contraction of the soleus muscle (5–6 sec in duration) on the H reflex was studied in persons aged 25–45 years. A sharp enhancement of the H reflex at a dynamic phase of fast contraction (in the force increase period) and its less pronounced increase at a static phase of contraction were shown. When a paired stimulation of the nerve was used (interstimulus interval, 500 msec), a voluntary contraction of the muscle fully abolished the first stimulus-related suppression of the second H reflex. When the muscle contracted against the background of vibration, the suppressed H reflex recovered up the the level observed in the resting muscle, but did not reach the level characteristic for the contracting muscle. The findings show that the two pathways controlling the H reflex (descending and afferent) function independently, and apparently there exist at least two corresponding groups of interneurons causing a presynaptic inhibition of the H reflex.Neirofiziologiya/Neurophysiology, Vol. 25, No. 5, pp. 365–371, September–October, 1993.     

Intramuscular fluid pressure during isometric contraction of human skeletal muscle

Intramuscular fluid pressures were recorded in the vastus medialis of seven healthy male volunteers. Pressures were measured simultaneously at three different sites in the muscle by a catheter-tip transducer with extremely low volume-displacement characteristics and by two extracorporeal transducers connected to slit catheters. All three recording systems gave qualitatively similar results provided the catheters had inner diameters exceeding 0.53 mm and allowed measurement of pressures lasting as short as 1 s. Wick catheters yielded slower responses than slit catheters. At any position intramuscular fluid pressure increased linearly with force up to maximal voluntary contraction (MVC). However, slopes of these curves varied greatly mainly because the pressure was also a linear function of the distance from the fascia. The highest recorded pressure was 570 Torr. At prolonged submaximal contractions intramuscular fluid pressure oscillated independent of contraction force. The linearity of both the pressure-force relationship and the pressure-depth relationship is compatible with a simple model based on the law of Laplace because the muscle fibers are curved during contraction in this muscle. It is hypothesized that blood flow is first compromised deep in the muscle where pressure is highest and in general at lower stress or tension in short bulging muscles with great curvature of the fibers compared with long slender ones.     

Detection of surface electromyography recording time interval without muscle fatigue effect for biceps brachii muscle during maximum voluntary contraction

The effects of fatigue on maximum voluntary contraction (MVC) parameters were examined by using force and surface electromyography (sEMG) signals of the biceps brachii muscles (BBM) of 12 subjects. The purpose of the study was to find the sEMG time interval of the MVC recordings which is not affected by the muscle fatigue. At least 10 s of force and sEMG signals of BBM were recorded simultaneously during MVC. The subjects reached the maximum force level within 2 s by slightly increasing the force, and then contracted the BBM maximally. The time index of each sEMG and force signal were labeled with respect to the time index of the maximum force (i.e. after the time normalization, each sEMG or force signal’s 0 s time index corresponds to maximum force point). Then, the first 8 s of sEMG and force signals were divided into 0.5 s intervals. Mean force, median frequency (MF) and integrated EMG (iEMG) values were calculated for each interval. Amplitude normalization was performed by dividing the force signals to their mean values of 0 s time intervals (i.e. ?0.25 to 0.25 s). A similar amplitude normalization procedure was repeated for the iEMG and MF signals. Statistical analysis (Friedman test with Dunn’s post hoc test) was performed on the time and amplitude normalized signals (MF, iEMG). Although the ANOVA results did not give statistically significant information about the onset of the muscle fatigue, linear regression (mean force vs. time) showed a decreasing slope (Pearson-r = 0.9462, p < 0.0001) starting from the 0 s time interval. Thus, it might be assumed that the muscle fatigue starts after the 0 s time interval as the muscles cannot attain their peak force levels. This implies that the most reliable interval for MVC calculation which is not affected by the muscle fatigue is from the onset of the EMG activity to the peak force time. Mean, SD, and range of this interval (excluding 2 s gradual increase time) for 12 subjects were 2353, 1258 ms and 536–4186 ms, respectively. Exceeding this interval introduces estimation errors in the maximum amplitude calculations of MVC–sEMG studies for BBM. It was shown that, simultaneous recording of force and sEMG signals was required to calculate the maximum amplitude of the MVC–sEMG more accurately.     

The frequency response of smooth muscle stiffness during Ca2+-activated contraction

To investigate the mechanism of smooth muscle contraction, the frequency response of the muscle stiffness of single beta-escin permeabilized smooth muscle cells in the relaxed state was studied. Also, the response was continuously monitored for 3 min from the beginning of the exchange of relaxing solution to activating solution, and then at 5-min intervals for up to 20 min. The frequency response (30 Hz bandwidth, 0.33 Hz (or 0.2 Hz) resolution) was calculated from the Fourier-transformed force and length sampled during a 3-s (or 5-s) constant-amplitude length perturbation of increasing-frequency (1-32 Hz) sine waves. In the relaxed state, a large negative phase angle was observed, which suggests the existence of attached energy generating cross-bridges. As the activation progressed, the muscle stiffness and phase angle steadily increased; these increases gradually extended to higher frequencies, and reached a steady state by 100 s after activation or approximately 40 s after stiffness began to increase. The results suggest that a fixed distribution of cross-bridge states was reached after 40 s of Ca2+ activation and the cross-bridge cycling rate did not change during the period of force maintenance.     

Influence of contraction force and speed on muscle fiber conduction velocity during dynamic voluntary exercise.

Before using electromyographic (EMG) variables such as muscle fiber conduction velocity (MFCV) and the mean or median frequency (MDF) of an EMG power spectrum as indicators of muscular fatigue during dynamic exercises, it is necessary to determine the influence of a joint angle, contraction force and contraction speed on the EMG variables. If these factors affect the EMG variables, their influence must be removed or compensated for before discussing fatigue. The vastus lateralis of eight normal healthy male adults was studied. EMG signals during non-fatiguing dynamic knee extension exercises were detected with a three-bar active surface electrode array. EMG variables were calculated from the detected signals and compared with the angle of the knee joint, the extension torque and the extension speed. The extension torque was set at four levels with 10% intervals between 40 and 70% of the maximum voluntary contraction. The extension speed was set at five levels with 60 degrees /s intervals between 0 and 240 degrees /s. Because the joint angle unsystematically affected the MFCV, EMG variables at a given joint angle were extracted for comparison. The influence of the extension torque and speed on the extracted EMG variables was clarified with an ANOVA and a regression analysis. The statistical analyses showed that MFCV increased with the extension torque but did not depend on the extension speed. In contrast, MDF was independent of the extension torque but was dependent on the extension speed. MDF thus showed a behavior different from that of MFCV. It became clear that if MFCV is used as an indicator of muscular fatigue during dynamic exercises, it is at least necessary to extract MFCV at a predetermined joint angle and then remove the influence of extension torque on MFCV.     

Dependence of average muscle fibre conduction velocity on voluntary contraction force

Average muscle fibre conduction velocity (CV) measured with multichannel surface electrodes decreases with time during sustained isometric contraction. Based on this property, CV is considered a candidate for an objective index to localized muscular fatigue. CV, however, also depends on many other factors that include muscle temperature and voluntary contraction force. In this paper, the effect of contraction force on CV was studied by defining not only the target force level but also the whole force trajectory. The contraction was isometric and lasted 14 s. The target force was set at four levels from 30% to 90% of the maximal voluntary contraction (MVC). Three typical muscles were studied in seven healthy male subjects. In the vastus lateralis, CV increased with contraction force in many cases. In the biceps brachii, CV decreased rapidly with time before the contraction force reached the target levels of 70% or 90% MVC. At these force levels, CV was smaller than that at 50% MVC. CV in the biceps consequently showed no apparent dependence on the contraction force. The tibialis anterior showed intermediate change in CV between the vastus lateralis and the biceps brachii. These results indicate that CV basically increases with contraction force, but this relationship becomes unclear when CV decreases rapidly with time.     

Analysis of impulse adaptation in motoneurons

Animal locomotion results from muscle contraction and relaxation cycles that are generated within the central nervous system and then are relayed to the periphery by motoneurons. Thus, motoneuron function is an essential element for understanding control of animal locomotion. This paper presents motoneuron input–output relationships, including impulse adaptation, in the medicinal leech. We found that although frequency-current graphs generated by passing 1-s current pulses in neuron somata were non-linear, peak and steady-state graphs of frequency against membrane potential were linear, with slopes of 5.2 and 2.9 Hz/mV, respectively. Systems analysis of impulse frequency adaptation revealed a static threshold nonlinearity at −43 mV (impulse threshold) and a single time constant (τ = 88 ms). This simple model accurately predicts motoneuron impulse frequency when tested by intracellular injection of sinusoidal current. We investigated electrical coupling within motoneurons by modeling these as three-compartment structures. This model, combined with the membrane potential–impulse frequency relationship, accurately predicted motoneuron impulse frequency from intracellular records of soma potentials obtained during fictive swimming. A corollary result was that the product of soma-to-neurite and neurite-to-soma coupling coefficients in leech motoneurons is large, 0.85, implying that the soma and neurite are electrically compact.