Effect of the tendon reflex on motoneurons of the antagonist muscle in man

The knee jerk was elicited during regular firing of relatively low-threshold motor units of the biceps femoris muscle (during weak voluntary contraction). Besides the reflex response of the rectus femoris muscle, synchronous discharges of motor units of the biceps femoris muscle and activation of new motor units also were observed. Poststimulus histograms and statistical analysis of interspike intervals of motor units of the biceps femoris muscle revealed well-marked excitatory influences synchronous with the reflex response of the rectus femoris. This result can be explained by the presence of excitatory inputs of Ia afferents on motoneurons of the antagonist muscle. In the knee jerk, excitation of motoneurons of the antagonist was followed by later inhibitory influences which evidently correspond to the "silent period" of motoneurons of the agonist muscle during the elicitation of its tendon reflex.Institute for Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 8, No. 6, pp. 624–632, November–December, 1976.     

Detection and analysis of recurrent inhibition of firing motoneurons in man

During regular firing of "small" motor units, activated during weak voluntary contraction of the human soleus muscle, thick efferent fibers of n. tibialis were stimulated (a small M response was evoked, in which the small units did not participate). Peristimulus histograms of potentials of single motor units were constructed and the effect of stimulation on interspike interval duration was analyzed. The firing rate of the motor units was 4.5–7.6 spikes/sec. Stimulation of the nerve led to a sharp decrease in probability of their discharge or even complete temporary cessation of firing, i.e., it had a well marked inhibitory effect (lasting 10–20 msec). The latent period of inhibition (35–40 msec) was only a little longer than the latent period of the monosynaptic reflex of the soleus muscle. The effect of an inhibitory volley on duration of the interspike interval of the motor units depended on the time when the volley arrived during the interval. Lengthening of the interval was observed only if the inhibitory volley arrived in the second half or at the end of the interval. It is concluded that inhibition of firing of small motor units is due to Renshaw cells, activated on stimulation of axons of large motoneurons. The efficiency of a short (compared with the duration of the interspike interval) inhibitory volley reaching a motoneuron firing at low frequency characteristic of its adequate activation, is discussed.Institute for Problems of Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 16, No. 1, pp. 88–96, January–February, 1984.     

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.     

The role of reflex mechanisms in postinhibitory rebound studied by analysis of human single motor unit activity

The mechanism of onset of rebound after inhibition induced by electrical stimulation of a nerve of maximal and submaximal strength for M-response was studied in single motor units of normal human soleus, rectus femoris, and hand muscles. Poststimulus histograms and changes in the duration of interspike intervals were compared with mechanical recordings of muscle contractions. In all muscles tested, during strong isotonic contraction, the increase in motor unit activity after a silent period was partly due to synchronization of their emergence from inhibition. However, it also contained a component of true facilitation of motoneurons, which was evidently a reflex response to lengthening of the muscle in the relaxation phase after evoked contraction. The latent period of this facilitation in the soleus and rectus femoris muscles coincided in value with the latent period of the monosynaptic spinal reflex, whereas in the hand muscles, in which a monosynaptic response to electrical nerve stimulation could not be evoked, the latent period of facilitation as a result of spindle activation during muscle relaxation was significantly longer than the latent period of the monosynaptic reflex. These findings support the hypothesis of presynaptic suppression of monosynaptic connections of Ia afferents with the motoneurons of some human muscles by descending tonic influences and of the use of information coming from spindles by supraspinal levels of the CNS.     

Relationship between the discharge rate of a firing motoneuron and the effectiveness of excitatory la afferent volleys in man

The H-reflex was evoked after producing regular unit firing in the flexor carpi ulnaris set up by moderate voluntary isometric muscular contraction. The firing index was used to quantify the effectiveness of the monosynaptic afferent signal traveling to the firing motoneuron. An analysis was made of the 3.3–16.0 spikes/sec firing range characteristic of naturally occurring muscular contraction. Effectiveness of afferent signals for motor units in the "fast" muscles under study were found to depend on motoneuronal background firing rate; the former declined as the latter rose, as previously discovered during research into "slow" soleus muscle units [2]. Afferent signals were most effective for motoneurons belonging to the "fast" muscles over the entire range of firing rates. It was found from analyzing afferent signal efficacy in relation to its point of occurrence within the interspike interval that variations in motoneuronal excitability within this interval are the reason for this relationship.Institute for Research into Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 19, No. 5, pp. 595–600, September–October, 1987.     

Testing excitability in human firing motoneurons during the interspike interval

Monosynaptic testing of excitability in firing triceps surae muscle motoneurons activated during volitional contraction was performed using a technique for recording potentials from single motor units and by producing H-reflex. Motoneuronal excitability was assessed according to level of firing index. Motoneuronal firing index decreased during transition from a low background rhythmic firing rate of less than 6 spikes/sec to one of 6–8 spikes/sec. It hardly changed with a further rise in rate to 12 spikes/sec. The dependence between firing index and spike rate are put down to changes occurring in motoneuronal excitability during the interspike interval. Findings indicate that in the low frequency range of motoneuronal firing characteristic of natural muscle contraction, discharge rate may be considered one of the factors determining excitability in the motoneuron and hence its transmission qualities.Institute of Problems in Information Transmission, Academy of Sciences of the USSR. Translated from Neirofiziologiya, Vol. 19, No. 2, pp. 210–216, March–April, 1987.     

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.     

Stochastic properties of motoneuron activity and the effect of muscular length

The activity of single motor units contributing to small tonic isometric contractions in human muscle at different muscular lengths was analyzed. The form of motor unit firing patterns shows that the interspike intervals compose independent sequences with about a 10% coefficient of variation and have a gamma distribution. The variability and the distribution shape curves show that as the mean interval decreases the variance also decreases and the interval density function becomes more symmetric. More significant is the fact that the form of the firing pattern remains unchanged when a motor unit has the same mean interval but with the muscle at different lengths. Comparison of these facts with experimental data from neuron models and cat motoneurons indicates that in the human the only relevant input-output relationship in motoneurons is that the net excitation adjusts the firing rate.     

Investigation of the frequency of impulse discharges of human motoneurons during voluntary muscle contraction

The motor unit (MU) potentials of the human m. rectus femoris were recorded during voluntary isometric contraction by means of a bipolar needle electrode. The frequency of impulse discharge of individual motoneurons was defined as a quantity inverse to the average interval between impulses during 0.5 or 1.0 sec. The force of contraction varied from 0 to 4–14 kg (17–47% of the maximum). The investigations showed that in addition to switching on and off of motoneurons during a change of contraction force, the frequency of their impulse discharges also changes. Motoneurons recruited at a low force (low-threshold) reached the highest frequency (up to 18–21 impulses/sec). As a rule, the higher the threshold, the lower the frequency in the entire range of changes. In the case of prolonged contraction with a constant force the frequency of discharges dropped during the first 1–2 min. The established frequency level did not exceed 10–13 impulses/sec. A voluntary increase of contraction force at this period was related with a new increase of frequency. Recruitment of new motoneurons was observed during prolonged contraction. The data obtained show that the mechanism of change of the firing frequency of motoneurons actively participates in contraction gradation, mainly its dynamic component. It is regarded as a mechanism of smooth and precise control. The decrease of frequency during prolonged contraction is apparently due to adaptation, although the participation of inhibition is not precluded.Institute of Problems of Information Transmission, Academy of Sciences of the USSR. Institute of Higher Nervous Activity and Neurophysiology, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 3, No. 2, pp. 200–209, March–April, 1971.     

Ia-afferent input to motoneurons during shortening and lengthening muscle contractions in humans.

The central nervous system employs different strategies to execute specific motor tasks. Because afferent feedback during shortening and lengthening muscle contractions differs, the neural strategy underlying these tasks may be quite distinct. Cortical drive may be adjusted or afferent input regulated. The exact mechanisms are not clear. Here, we examine the control of synaptic transmission across the Ia synapse during shortening and lengthening muscle contractions. Subjects were instructed to maintain isolated activity in a single tibialis anterior (TA) motor unit while muscle length was varied from flexion to extension and back. At a fixed interval after a firing of the active motor unit, a single electrical stimulus was applied to the common peroneal nerve to activate Ia afferents from the TA muscle. We investigated the stimulus-induced change in firing probability of 19 individual low-threshold TA motor units during shortening and lengthening contractions. Any change in firing probability depends on both pre- and postsynaptic mechanisms. In this experiment, motoneuron firing rate was similar during both contraction types. There was no difference in the firing probability between shortening and lengthening contractions (0.23 +/- 0.03 and 0.20 +/- 0.02, respectively). We suggest that there is no contraction type-specific control of Ia input to the motoneurons during shortening and lengthening muscle contractions. Cortical adjustments may have occurred.     

Activity of fusimotor neurons during reflex muscle contraction

The influence of fusimotor activity via the gamma-loop on reflex responses of motoneurons to stretch or vibration stimulation of mm. triceps surae was studied in decerebrate cats. Action potentials of single fusimotor neurons were derived from thin filaments isolated from nerves innervating this muscle group, leaving their main nerve supply intact. Most fusimotor neurons tested were found to be coactivated with motor units during reflex muscle contraction. In the initial period of development of reflex muscle contraction a weak autogenetic inhibitory effect on discharge of fusimotor neurons was found. The results suggest that reduction of the reflex motor signal, leading to a "silent period," is partly the result of a transient decrease in the fusimotor output effect on contracting muscles. A study of changes in fusimotor discharge generation during the ascending phase of reflex muscle contraction may provide data useful for identification of autogenetic reflex influences on these motoneurons and for elucidating the conditions necessary for servoassistance of muscle contractions.Medical Research Institute, Belgrade, Yugoslavia. Translated from Neirofiziologiya, Vol. 16, No. 5, pp. 630–637, September–October, 1984.     

Recurrent inhibition of human firing motoneurons (experimental and modeling study)

Recurrent inhibition between tonically activated single human motoneurons was studied experimentally and by means of a computer simulation. Motor unit activity was recorded during weak isometric constant-force muscle contractions of brachial biceps (BB) and soleus (SOL) muscles. Three techniques (cross correlogram, frequencygram, and interspike interval analysis) were used to gauge the relations between single motor unit potential trains. Pure inhibition was detected in 5.6% of 54 BB motoneuron pairs and in 5.2% of 43 SOL motoneuron pairs. In 27.8% (BB) and 23.7% (SOL) presumed inhibition symptoms were accompanied by a synchrony peak; 37% (BB) and 48.8% (SOL) exhibited synchrony alone. The demonstrated inhibition was very weak, at the edge of detectability. Computer simulations were based on the threshold-crossing model of a tonically firing motoneuron. The model included synaptic noise as well as threshold and postsynaptic potential (PSP) amplitude change within interspike interval. Inhibition efficiency of the model neurons increased with IPSP amplitude and duration, and with increasing source firing rate. The efficiency depended on target motoneuron interspike interval in a manner similar to standard deviation of ISI. The minimum detectable amplitude estimated in the simulations was about 50V, which, compared with the experimental results, suggests that amplitudes of detectable recurrent IPSPs in human motoneurons during weak muscle contractions do not exceed this magnitude. Since recurrent inhibition is known to be progressively depressed with an increase in the force of voluntary contraction, it is concluded that the recurrent inhibition hardly plays any important role in the isometric muscle contractions of constant force.     

Reduction in maximal firing rate of motoneurons after 1-week immobilization of finger muscle in human subjects.

We investigated the effects of immobilization on the maximal motoneuronal firing rate recorded from the first dorsal interosseous (FDI) during voluntary isometric contraction. In five human subjects, the middle finger, index finger, and thumb were immobilized for 1 week in a fiber-glass cast, which kept FDI in a shortened position. During a maximal voluntary contraction, single muscle-fiber action potentials were recorded using a tungsten microelectrode, and mean firing rate was calculated for each action-potential train. Three recording sessions were held: before immobilization (pre), after immobilization (post), and after a 1-week recovery period (recovery). The mean firing rate of FDI motoneurons during maximal voluntary contraction was decreased immediately after the 1-week immobilization (pre: 39.0+/-3.2 Hz, number of detected spike trains (n)=353; post: 33.1+/-1.5 Hz, n=285; p<0.05), and there was a return to control after the recovery period (40.2+/-3.4 Hz, n=236). This suggests that the maximal motoneuronal firing rate achieved during maximal voluntary contraction is reduced after short-term immobilization. The functional implications and the contribution of this phenomenon to the immobilization-induced reduction in maximal voluntary force are discussed.     

Motor unit firing behavior during prolonged 50% MVC dorsiflexion contractions in young and older adults

The purpose of this study was to investigate changes in motor unit firing behavior during prolonged contractions in young and older adults. Motor unit activity was recorded from the tibialis anterior of 16 subjects (8 young and 8 older), while they performed isometric dorsiflexion at 50% MVC until task failure. Mean motor unit firing rate, the standard deviation (SD), and coefficient of variation (CV) of the interspike intervals, and number of doublet discharges were calculated for a total of 52 motor units, tracked for an average of 92.9 ± 68.6 s. There was no age-related difference in the time to task failure. A modest decline in firing rate was observed in 71% of the motor units, with no significant age-related difference. The SD and CV of the interspike interval had a positive slope in 65% and 69% of the motor units, respectively, with no significant age-related differences. The number of doublet discharges remained stable throughout the contraction. Both groups exhibited motor unit dropout (discharge cessation) during the contraction. Thus, a fatiguing task producing modest changes in firing rate in young and older adults is accompanied by an appreciable increase in firing rate variability. The incidence of doublet discharges is not increased during fatiguing contractions.     

Human motoneuron firing behavior and single motor unit F-wave

In motor control studies, the F-wave (a recurrent discharge evoked by an axonal antidromic volley) widely used for obtaining information on motoneuron pool behavior. However, such F-wave using is a matter of discussion and still has been not validated experimentally. The aim of the present study was investigation of F-wave properties of single firing motor units (MUs) in healthy humans, the properties, which could give evidence for F-wave origin in motoneuron soma and, therefore, could be used for estimation of a relation between MU firing and motoneuron firing behavior. In total, 91 MUs in five muscles of six healthy subjects, during gentle voluntary contractions, were studied. Peri-stimulus time histograms of single MUs were plotted. None of them revealed statistically significant increasing in MU firing probability at the F-wave latency. Analysis of relationships between characteristics of motoneuron firing behavior (mean firing frequency and target interspike interval duration) and properties of F-waves showed their independence. At the same time, it was found that F-waves were recorded in MUs, whose axons possessed the marked supernormal period in excitability recovery cycle after a discharge. Thus, the present results are in contrast to that which should be expected if the F-wave originated in the motoneuronal soma and could provide evidence for motoneuron firing behavior.     

Pyramidal unit activity in unanesthetized cats

Pyramidal unit activity in unanesthetized cats at rest and during voluntary movement was recorded by a microelectrode technique from the motor cortex for the forelimb. Some pyramidal neurons were not spontaneously active. The conduction velocity along the axon of these neurons was sometimes high (up to 71.5 m/sec), sometimes low (up to 11.2 m/sec). The remaining pyramidal neurons had spontaneous activity with a mean frequency of 1.29 to 43 spikes/sec. Analysis of interspike interval histograms of spontaneous activity and of autocorrelation histograms showed grouping of the spikes into volleys in most pyramidal neurons (irrespective of the conduction velocity). During voluntary movements the change in the activity of many pyramidal units correlated with changes in the EMG. The firing rate of the pyramidal neurons under these circumstances began to rise at least 50 msec before the increase in amplitude of the EMG and it remained high throughout the movement. The firing rate of most neurons during movement was 40–60/sec. The results are compared with those obtained by other workers who studied pyramidal unit activity of monkeys during voluntary movement.     

The effects of four time-varying factors on the mean frequency of a myoelectric signal.

Daily activities involve dynamic muscle contractions that yield nonstationary myoelectric signals (MESs). The purpose of this work was to determine the individual effects of four time-varying factors (the number and firing rate of active motor units, muscle force and joint angle) on the mean frequency of a MES. Previous theoretical and experimental work revealed that although changes in the number and firing rate of active motor units contribute to the nonstationarities of the signal, they do not significantly affect the mean frequency. In the experimental work, 12 subjects performed 25 static contractions, one for each force (20, 30, 40, 50 and 60% of maximum voluntary contraction) and elbow joint angle (50, 70, 90, 110 and 130 degrees extension) combination. A MES was recorded from the surface of the biceps brachii during each contraction. The results indicated that muscle force only weakly affects the mean frequency. Also shown was that alteration in muscle geometry resulting from changes in elbow joint angle does significantly affect the mean frequency. Knowing this is important for the assessment of muscle fatigue during dynamic contractions.     

Motor unit activation patterns during concentric wrist flexion in humans with different muscle fibre composition

Muscle activity was recorded from the flexor carpi radialis muscle during static and dynamic-concentric wrist flexion in six subjects, who had exhibited large differences in histochemically identified muscle fibre composition. Motor unit recruitment patterns were identified by sampling 310 motor units and counting firing rates in pulses per second (pps). During concentric wrist flexion at 30% of maximal exercise intensity the mean firing rate was 27 (SD 13) pps. This was around twice the value of 12 (SD 5) pps recorded during sustained static contraction at 30% of maximal voluntary contraction, despite a larger absolute force level during the static contraction. A similar pattern of higher firing rates during dynamic exercise was seen when concentric wrist flexion at 60% of maximal exercise intensity [30 (SD 14) pps] was compared with sustained static contraction at 60% of maximal voluntary contraction [19 (SD 8) pps]. The increase in dynamic exercise intensity was accomplished by recruitment of additional motor units rather than by increasing the firing rate as during static contractions. No difference in mean firing rates was found among subjects with different muscle fibre composition, who had previously exhibited marked differences in metabolic response during corresponding dynamic contractions. It was concluded that during submaximal dynamic contractions motor unit firing rate cannot be deduced from observations during static contractions and that muscle fibre composition may play a minor role. Accepted: 5 May 1998     

Reciprocal inhibition studied in discharging human motor units

The effect of excitation of group Ia afferents, evoked by stimulation of a mixed nerve, on the firing pattern of voluntarily activated single motor units of an antagonist muscle (biceps femoris, triceps surae, and tibialis anterior muscles) was studied. Poststimulus histograms were constructed for rhythmic sequences of motor unit potentials recorded by needle electrodes and the duration of interspike intervals was analyzed. Reciprocal inhibition and other effects accompanying nerve stimulation were discovered in the motoneurons of all three muscles. Distinguishing features of the manifestation of reciprocal inhibition in a discharging motoneuron were investigated; the effect was shown to depend on the time of occurrence of the inhibitory action in the interspike interval.Institute for Problems in Information Transmission, Academy of Sciences of the USSR, Moscow. Translated from Neirofiziologiya, Vol. 10, No. 6, pp. 626–636, November–December, 1978.     

Does the frequency content of the surface mechanomyographic signal reflect motor unit firing rates? A brief review.

The purpose of this review is to examine the literature that has investigated the potential relationship between mechanomyographic (MMG) frequency and motor unit firing rates. Several different experimental designs/methodologies have been used to address this issue, including: repetitive electrical stimulation, voluntary muscle actions in muscles with different fiber type compositions, fatiguing and non-fatiguing isometric or dynamic muscle actions, and voluntary muscle actions in young versus elderly subjects and healthy individuals versus subjects with a neuromuscular disease(s). Generally speaking, the results from these investigations have suggested that MMG frequency is related to the rate of motor unit activation and the contractile properties (contraction and relaxation times) of the muscle fibers. Other studies, however, have reported that MMG mean power frequency (MPF) does not always follow the expected pattern of firing rate modulation (e.g. motor unit firing rates generally increase with torque during isometric muscle actions, but MMG MPF may remain stable or even decrease). In addition, there are several factors that may affect the frequency content of the MMG signal during a voluntary muscle action (i.e. muscle stiffness, intramuscular fluid pressure, etc.), independent of changes in motor unit firing rates. Despite the potential influences of these factors, most of the evidence has suggested that the frequency domain of the MMG signal contains some information regarding motor unit firing rates. It is likely, however, that this information is qualitative, rather than quantitative in nature, and reflects the global motor unit firing rate, rather than the firing rates of a particular group of motor units.