Instability of motor unit firing rates during prolonged isometric contractions in human masseter

The firing patterns of up to 4 concurrently active masseter motor units were studied with intramuscular electrodes during a continuous isometric contraction of 15 min duration, in which the subject maintained the mean firing rate of one selected unit at 10 Hz. With this paradigm the net excitation (i.e. mean firing rate) of one unit in the muscle was controlled. This served as the reference for the functional state of other active units during the prolonged contraction. With the mean firing rate of one unit in the muscle fixed, 58% of other active units showed a slow, statistically-significant change in mean firing rate over the 15 min. The initial firing rate of the units did not influence the change in rate. The original firing rate hierarchy, which in short-term contractions reflects the recruitment order, was altered during the prolonged contraction. The explanation for these differential changes in motoneuron net excitation is not clear; they could be intrinsic to the motoneurons or perhaps mediated by reflex pathways. The selective facilitation or suppression of some motor units with continuous activation means that the original size-structured combination of motor units can be modified during a prolonged contraction.     

Time-dependent structure in the discharge rate of human motor units.

OBJECTIVES: The aim of this study was to examine the influence of visual and motor processes on the deterministic and stochastic structure of force output and motor unit discharge variability. METHODS: Young adult subjects produced continuous, isometric force at 3, 6, 12, and 24% of their maximal voluntary contraction at low and high visual gain levels through abduction of the index finger. Force and fine-wire intramuscular electromyography were recorded. RESULTS: There was a linear increase in discharge irregularity with increases in the mean motor unit discharge rate (8-30 Hz). Recurrence analysis showed that the percentage of deterministic structure in discharge variability remained high, but decreased linearly with increased motor unit discharge rate. Surrogate analyses confirmed that the motor unit discharge variability was inconsistent with an uncorrelated and linearly correlated Gaussian noise process. Spectral analysis revealed that both the force output and the mean time-varying motor unit discharge time series had a dominant frequency of 0-2 Hz. Visual feedback gain did not affect the individual motor unit discharge patterns. CONCLUSIONS: The motor unit discharge rate has deterministic time-dependent structure. The motor unit discharge rate is modulated at multiple time scales likely by pre- and post-synaptic induced fluctuations from spinal level pathways impinging on the motor neuron.     

A comparison of electromyographic and mechanical fatigue properties in motor units of the cat hindlimb

Single motor units were isolated in medial gastrocnemius (MG) or soleus (Sol) muscles of the cat. Single shocks delivered to the motor axon elicited EMG waveforms which were recorded in the muscle. The amplitude of each individual EMG waveform as well as the area under the full-wave rectified waveform were measured. Mechanical properties of the motor units were then measured so that each unit could be classified as FF, FR or S according to the criteria of Burke. Finally, each unit was stimulated continuously at 80 pulses per second (pps), and changes in electrical and mechanical responses were recorded and compared. IEMG was positively correlated with maximum tetanic tension of motor units in MG. The relationship could be fitted with a parabola showing that 'large' motor units produce relatively more electrical activity than do 'small' motor units. Two types of electrical changes were seen during continuous stimulation of motor units at 80 pps: a smooth continuous decline in IEMG was attributed to electrical changes occurring at a site or sites distal to the neuromuscular junction; and random, abrupt changes in unit-EMG waveform and hence IEMG amplitude, were attributed to failure of the action potential to propagate past axonal branch points, resulting in the intermittent failure of groups of muscle fibers to respond to stimuli. The rates of decline of electrical and mechanical activity were compared for motor units. It was found that in fast fatiguing motor units, tetanic tension declined more rapidly than did IEMG, while in slowly fatiguing motor units, IEMG declined more rapidly than did force. We conclude that fatigue of motor units induced by continuous 80 pps stimulation can occur at different sites in the motor unit, and that the site of fatigue depends on motor unit properties or motor unit type.     

Firing rate of individual motor units in voluntary contraction of abductor digiti minimi muscle in man

The frequency and variability of discharges of motor units in abductor digiti minimi muscle of 11 human subjects were investigated. In the first series, contraction was performed so as to raise the tension as linearly as possible from 0 to maximum in 2, 3.2, 5, 8, and 10 sec. There was a rise in discharge frequency when the tension was raised; this rise was steeper when the contraction was faster. The frequency at the start of discharge was higher, and the peak value of frequency was also higher at contractions with greater speeds. Irregular fluctuations in the discharge frequency was greater and appeared at earlier stages during the more rapid contractions. In the second series of experiments, the tension was held constant at various levels covering the entire range of contraction. At contractions with larger steady tension the discharge frequency of units was found to be higher and irregularity of discharge was enhanced. The units recruited at smaller tension vary over a greater range of discharge frequencies than those recruited at larger tension.     

The motor units of cat medial gastrocnemius: speed-size relations and their significance for the recruitment order of mortor units.

The interrelationships between axonal conduction velocity, tetanic tension, twitch contraction time and rate of force development during a tetanus have been studied in 126 motor units from 12 cat medial gastrocnemius muscles. While the range of axonal conduction velocities for slow- (contraction time greater than 45 msec) and fast-twitch units overlapped, the mean conduction velocity for the slow-twitch group was significantly lower. No difference could be found between the axonal conduction velocities of the fast non-fatiguing and fast fatiguing units. Within individual experiments, few significant correlations were found between conduction velocity and tetanic tension or contraction time for the fast- and slow-twitch units. Some correlations did appear when data from these populations were pooled, but such results are shown to be misleading. Some weak correlations were found between motor unit contraction strength and twitch contraction time. The rate of rise of isometric force development was found to be most strongly related to tetanic tension and only weakly related to contraction time. The ordering of motor units according to contraction strength reveals the association of motor unit mechnical properties to be ideally suited for the dual role of medial gastrocnemius as a postural and powerful phasic muscle.     

Spike train characteristics of single motor units in the human masseter muscle

Single motor unit (SMU) spike trains were recorded from the masseter muscles of human subjects while they isometrically produced interocclusal force. The majority of SMUs increased their firing rate as interocclusal force was increased, but the rate changes declined in magnitude at each successive force level and eventually reached constant values. This indicated a progressive decline in the ability of motoneurons to increase firing rate in response to increases in excitatory drive, and the evidence suggests that this is due to temporal summation of afterhyperpolarization conductances. There was a strong tendency for SMUs with low recruitment thresholds to show the largest rate changes per kilogram change in force, which may be a consequence of the decreasing input resistances associated with increases in cell size. There were also monotonic decreases in standard deviations and skewness of the interspike interval (ISI) distributions as firing rate increased, which indicates that synaptic drive to the motoneurons was increasing monotonically. The graph of standard deviation mean ISI revealed less tendency for masseter motoneurons to maintain minimum discharge variability as compared to spinal motoneurons; the lack of recurrent inhibition to masseter motoneurons may be responsible.     

Dependence of the paired motor unit analysis on motor unit discharge characteristics in the human tibialis anterior muscle

The paired motor unit analysis provides in vivo estimates of the magnitude of persistent inward currents (PIC) in human motoneurons by quantifying changes in the firing rate (ΔF) of an earlier recruited (reference) motor unit at the time of recruitment and derecruitment of a later recruited (test) motor unit. This study assessed the variability of ΔF estimates, and quantified the dependence of ΔF on the discharge characteristics of the motor units selected for analysis. ΔF was calculated for 158 pairs of motor units recorded from nine healthy individuals during repeated submaximal contractions of the tibialis anterior muscle. The mean (SD) ΔF was 3.7 (2.5)pps (range -4.2 to 8.9 pps). The median absolute difference in ΔF for the same motor unit pair across trials was 1.8 pps, and the minimal detectable change in ΔF required to exceed measurement error was 4.8 pps. ΔF was positively related to the amount of discharge rate modulation in the reference motor unit (r2 = 0.335; P<0.001), and inversely related to the rate of increase in discharge rate (r2 = 0.125; P<0.001). A quadratic function provided the best fit for relations between ΔF and the time between recruitment of the reference and test motor units (r2 = 0.229, P<0.001), the duration of test motor unit activity (r2 = 0.110, P<0.001), and the recruitment threshold of the test motor unit (r2 = 0.237, P<0.001). Physiological and methodological contributions to the variability in ΔF estimates of PIC magnitude are discussed, and selection criteria to reduce these sources of variability are suggested for the paired motor unit analysis.     

Bursting properties of units in cat globus pallidus and entopeduncular nucleus: the effect of excitotoxic striatal lesions

The bursting properties of units recorded in globus pallidus and entopeduncular nucleus were studied in awake cats sitting quietly before and after ipsilateral excitotoxic striatal lesions. A computerized statistical procedure was used to identify and evaluate bursts in the recorded spike trains. Bursts were assigned a quantitative statistical measure of burst 'strength' (or improbability) - the surprise value. Before the lesion, 34% of units in the globus pallidus and 60% of units in the entopeduncular nucleus exhibited bursts. Burst units had a significantly slower discharge rate and a significantly greater variability of discharge than non-burst units. The mean length of the interspike intervals immediately preceding the bursts was significantly longer than the overall median intervals in burst units. After the lesion, 21% of units in the globus pallidus and 11% of the units in the entopeduncular nucleus exhibited bursts. Burst units had significantly higher discharge rates and lower discharge variability after the lesion. In contrast, the lesion had no significant effect on the rate or variability of non-burst units. The differences between bursting and non-bursting units in discharge rate and variability disappeared after the lesion. In globus pallidus, the lesion resulted in a significant reduction in the mean number of bursts per unit, surprise value per burst, mean length of bursts, and number of spikes per burst, and a significant increase in the mean discharge rate of burst units. In entopeduncular nucleus, the small number of bursts recorded after the lesion precluded a useful statistical comparison of the effect of striatal lesions on the properties of the bursts. This study demonstrates that removing striatal projections to globus pallidus and entopeduncular nucleus decreases bursting in these nuclei, indicating that intact striatal projections are necessary for the normal production of bursts in these regions.     

Characteristics of motor unit discharge in subjects with hemiparesis

We studied the discharge rates recruitment characteristics of single motor units in paratic and contralateral arm muscles of 6 hemiparetic subjects. Motor unit activity in bicapes brachii was recorded at different elbow torques, and the activity related both to the mean level of surface electromyographic activity, and to the degree of weakness. In 3 of the 6 subjects, there were significant reductions in mean discharge rate of motor units in the paretic muscle. All 6 subjects showed compression of the range of motoneuron recuitment forces, and a failure to increase motor unit discharge rate during voluntary force increases in paretic muscles. These rate reductions could potentially alter the precise match of motoneuron properties to the mechanical properties of the innerved muscle fibers, and reduce the efficiency of muscle contraction. This reduction could lead, in turn to increased effort, to fatigue, and ultimately to a sense of weaknes for voluntary force generation.© 1995 John Wiley & Sons, Inc.     

Effect of motor unit firing pattern on twitches obtained by spike-triggered averaging

The spike-triggered averaging technique (STA) was used to determine the twitch profile of single motor units in human masseter during a voluntary isometric contraction. The effect of the immediate firing pattern of the unit on the twitch was assessed with a computer program which scanned the unit discharge records and selected valid trigger spikes for the averager on the basis of the interspike intervals preceding and following the trigger spike. Successive averages from the same data using different interval parameters revealed progressively more fusion of twitches as the instantaneous firing rate increased. When the data were averaged with interval parameters similar to those used in earlier studies, some fusion of the twitch profile was also evident. It is therefore likely that the degree of fusion of human motor unit twitches obtained by STA has been underestimated in the past. It is further concluded that masseter motor units are sufficiently fast-contracting to allow a relatively unfused twitch profile to be obtained with STA, provided trigger spikes are subjected to appropriate rate control.     

Organization of motor units in the axolotl: a continuously growing animal

The characteristics of motor units in the iliotibialis posterior muscle of the axolotl hindlimb are described. Tension recording and intracellular electrophysiological methods demonstrate that the physiological properties of the population of motor units are continuously distributed rather than grouped into a series of discrete types. Overlap between motor units occurs and this is positively correlated with motor unit size but negatively correlated with differences in time to peak tension. Immunocytochemical staining with antimyosin antibodies combined with histochemical demonstration of actomyosin ATPase activity revealed at least four types of muscle fibre which were distributed asymmetrically within iliotibialis posterior. The results are discussed in terms of the continuous growth of the muscle and the interactions between muscle and nerve in the formation of the axolotl motor system.     

The estimation of motor unit twitch tensions in the human masseter muscle by spike-triggered averaging

Spike-triggered averaging (STA) has been used to extract twitch profiles of single motor units (SMU) within the human masseter muscle. However, the reported twitch tensions may have been biased by the voluntary firing frequency of the SMUs, the complex architecture of the muscle, and by the biomechanical linkage of the jaw. In this study, a rigid STA paradigm was used to record spike-triggered "measured tensions" (STMTs) for 32 SMUs in the masseter muscles of four subjects. STMTs were recorded at two different orientations of a force transducer placed between the incisor teeth. The STMTs produced by each unit were used to calculate jaw torque. STMTs were also recorded in 11 units with differing degrees of muscle coactivation. STMTs for each unit varied according to the orientation of the force transducer. However, no systematic changes in STMTs occurred with reciprocal changes in the jaw moment arm. STMTs could be altered significantly by different degrees of muscle co-activation. The use of STA as a method for determining SMU tension in the human masseter muscle appears to be highly task-dependent and in the presence of co-activation may be inappropriate.     

Variability of motor unit discharge and force fluctuations across a range of muscle forces in older adults

Variability of motor unit discharge is a likely contributor to the greater force fluctuations observed in old adults at low muscle forces. We sought to determine whether the variability of motor unit discharge rate underlies the fluctuations in force during steady contractions across a range of forces in young (n = 11) and old (n = 14) adults. The coefficient of variation (CV) for discharge rate and force were measured during a force-matching task as the first dorsal interosseous muscle performed isometric contractions. The recruitment thresholds of the 78 motor units ranged from 0.04% to 34% of maximal voluntary contraction (MVC) force. The CV for discharge rate ranged from 7.6% to 46.2% and was greater (P < 0.05) for old adults (21.5% +/- 7.7%) than young adults (17.3% +/- 8.1%). Although the CV for force was similar for young and old subjects (2.53% +/- 1.6%) across all target forces, it was greater for old adults at the lowest forces. Furthermore, there was a positive relation (r2 = 0.20, P < 0.001) between the CV for force and the CV for discharge rate across the range of recruitment thresholds. This relation was significant for old adults (r2 = 0.30, P < 0.001), but not for young adults (r2 = 0.06, P > 0.05). Thus, the normalized variability (CV) of motor unit discharge was greater in old adults and was related to the amplitude of force fluctuations across a broader range of forces than previously examined. These findings underscore the contribution of variability of motor unit activity to motor output in normal human aging.     

Characteristics of the F response: a single motor unit study.

Trains of 100 to 200 stimuli result in F discharges from less than one half of motor units of hand muscles. The maximum observed F discharge frequency was 10%. There was no relation between the surface voltage of motor unit potentials and the frequency of F discharge. The motor unit potentials of larger surface voltage were recruited at higher stimulus intensity levels, usually supramaximal for the antidromic sensory nerve action potential. No correlation was observed between F latency and the surface voltage of the motor unit potentials. In only one pathological example was a clear interaction observed between the frequency of F discharge in motor unit potentials and the recruitment of other single motor unit potentials by increments in the stimulus intensity. The observations suggested that caution should be exercised before the F discharge is accepted as a method for measuring proximal conduction times in human motor nerves.     

Coherence between motor unit discharges in response to shared neural inputs

Coherence analysis is widely employed to study the correlation between discharge times of simultaneously active motor units. Despite the widespread application of the technique, it has not been fully established how the characteristics of the observed coherence are related to the properties of the shared motoneuron inputs. In addition, the exact relationship between coherence and traditional measures of motor unit synchronization remains unclear. The purpose of this study was to examine the influence of shared motoneuron inputs on coherence between motor unit discharge patterns using computer simulations. Although less sensitive to motor unit firing rates than traditional synchronization-based indices, coherence tended to decrease with increasing frequency of the common input and to increase slightly when the common input frequency was close to the motor unit firing rates. In addition, coherence tended to be highest between motor units with similar firing rates. A linear association was observed between synchronization and coherence in the 15-30 Hz range and between 'common drive' and coherence in the 0-5 Hz range. The results suggest that caution should be taken when interpreting differences in coherence observed between motor units with significantly different firing properties or when comparing data with coherence in different frequency ranges.     

Motor unit function during evolution of proximal axonal swellings.

beta,beta'-Iminodipropionitrile (IDPN) impairs axonal transport of neurofilaments; their accumulation leads to the formation of proximal swellings in motor axons. Similar proximal swellings are a feature of some cases of motor neuron disease such as amyotrophic lateral sclerosis (ALS). Motor units in IDPN-treated animals were assessed to determine their relative susceptibilities to impaired function and whether the functional changes resulting from proximal axonal swellings share certain electromyographic features with ALS. Intrinsic properties of medial gastrocnemius motoneurones (MN) and contractile responses of their motor units were examined during the evolution of proximal axonal swellings in cats administered IDPN (50 mg/kg once weekly) for 7, 14 or 35 days. While conduction velocities were significantly decreased in all motor unit types by 35 days, the conduction slowing was greater in fast fatigable (types FF and FI) motor units than in fatigue resistant (types FR and S) motor units. Normal correlations between axonal conduction velocity and MN input resistance (Rin) and the inverse relationship between Rin and rheobase were lost with progression of the neuropathy. Twitch and maximum tetanic tension developed by fast-fatigable motor units declined early in the neuropathy, whereas fatigue-resistant units did not show similar changes until later stages of the intoxication. In some motor units, irregular and abnormal tetanic tensions were elicited by repetitive MN discharge. At 14 and 35 days, a novel, intermediate motor unit response classified as slow and fatigable (SF) was observed. Conduction block, characterized by repetitive MN firing without a corresponding contractile response, was observed in some type FF and S units by 35 days. Morphometric analysis of muscle fiber types showed significant atrophy, particularly in the type I fibers at 14-35 days; the atrophy reversed following cessation of IDPN administration. The influence of proximal axonal swellings on motor unit function in IDPN neuropathy is discussed in terms of reported electrophysiological alterations in motoneurone disease.     

Recruitment and firing rate modulation of motor unit tension in a small muscle of the cat's foot.

Maintained contractions were elicited in the first deep lumbrical muscle of the cat's foot by electrical stimulation of the contralateral motor cortex or, reflexly, by pinching of the foot pad. The discharges of all significant motor units of the muscle were monitored by electromyography, and contractions of the various motor units were observed in isometric recordings of muscle tension. Over a wide range, muscle tension could be enhanced by an increased intensity of pad pinching or cortical stimulation. This increase in muscle tension was caused by a recruitment of new motor units as well as by an increase in the firing rate of already active motor units. The latter mechanism was clearly of great importance. Pad pinching or cortical stimulation could sometimes cause the muscle to produce a tension close to that of a maximum tetanic contraction. This was several times greater than the mean tension that would have been caused by motor unit recruitment alone (i.e. by the motor units firing at their minimum steady rate). Cortical stimulation as well as pad pinching commonly recruited weak units more easily than stronger ones of the same muscle. The recruitment order obtained in response to pad pinching often differed, however, in various details from the recruitment caused by cortical stimulation.     

Tonic and kinetic motor units revisited: does motor unit firing behavior differentiate motor units?

OBJECTIVE: We tried to differentiate motor unit into two distinct populations, tonic and kinetic, on the basis of the relationship between the mean inter-spike interval and its variability. METHODS: During voluntary isometric contraction myoelectric activity was recorded with a special quadrifilar electrode from first dorsal interosseous, biceps brachii, soleus, and tibialis anterior muscle. Motor unit action potentials (MUAP) were decomposed into individual MUAP trains, by electromyography (EMG) signal decomposition. The variability in the instantaneous firing rate was assessed at two or more levels of contraction in each muscle. RESULTS: We found each muscle tested had a homogeneous population. There were no tonic and kinetic motor units. But there were differences in the variability in the instantaneous firing rate in the 4 muscles tested. CONCLUSION: Motor unit firing behavior in a muscle may be fitted for its function.     

Properties of motor units in the first deep lumbrical muscle of the cat's foot.

Isometric contractions of single motor units were studied in the first deep lumbrical muscle of the cat's hind-foot. Motor units with short twitch contraction times (15-20 msec) generally differed from those with longer ones (23-50 msec; contraction time measured in unpotentiated twitches) in showing (1) a greater maximum tetanic tension, (2) a smaller resistance to fatigue, (3) more post-tetanic potentiation of twitch tension, and (4) no post-tetanic occurrence of repetitive activity in response to single nerve stimuli (such "post-tetanic repetitive activity" was seen in several of the slower units). The ratio between unpotentiated twitch tension and maximum tetanic tension was similar for units with brief and long contraction times. The peak-to-peak amplitude of a single motor unit spike, recorded with gross electrodes, tended to be directly proportional to the maximum tetanic tension of the same motor unit.     

Disturbances in the voluntary recruitment order of anterior tibial motor units in ataxia.

The recruitment order of motor units was studied with an electromyographic technique for secure identification of single motor unit potentials. It has been shown in previous studies of normal subjects that the recruitment order in sustained voluntary contraction is predominantly stable, and that motor units which increase slowly in discharge rate with increasing contraction strength and which already attain regular discharge intervals at low frequencies are always recruited before motor units which increase more rapidly in discharge rate and which do not attain regular discharge intervals until at higher frequencies. In this study 15 patients with severe cerebellar ataxia were examined. It was shown that the recruitment order in sustained voluntary contraction in attaxia is unstable and that low- and high-frequency motor units may alternate as the unit of lowest threshold.