Inter-rater reliability of motor unit number estimates and quantitative motor unit analysis in the tibialis anterior muscle

ObjectiveTo establish the inter-rater reliability of decomposition-based quantitative electromyography (DQEMG) derived motor unit number estimates (MUNEs) and quantitative motor unit (MU) analysis.MethodsUsing DQEMG, two examiners independently obtained a sample of needle and surface-detected motor unit potentials (MUPs) from the tibialis anterior muscle from 10 subjects. Coupled with a maximal M wave, surface-detected MUPs were used to derive a MUNE for each subject and each examiner. Additionally, size-related parameters of the individual MUs were obtained following quantitative MUP analysis.ResultsTest–retest MUNE values were similar with high reliability observed between examiners (ICC = 0.87). Additionally, MUNE variability from test–retest as quantified by a 95% confidence interval was relatively low ($\pm 28$ MUs). Lastly, quantitative data pertaining to MU size, complexity and firing rate were similar between examiners.ConclusionMUNEs and quantitative MU data can be obtained with high reliability by two independent examiners using DQEMG.SignificanceEstablishing the inter-rater reliability of MUNEs and quantitative MU analysis using DQEMG is central to the clinical applicability of the technique. In addition to assessing response to treatments over time, multiple clinicians may be involved in the longitudinal assessment of the MU pool of individuals with disorders of the central or peripheral nervous system.     

Mapping the motor point in the human tibialis anterior muscle

ObjectivePercutaneous electrical stimulation of the motor point permits selective activation of a muscle. However, the definition and number of motor points reported for a given muscle varies. Our goal was to address these problems.MethodsThe area, location and number of motor points in human tibialis anterior were examined, using isometric dorsiflexion torque responses to electrical stimuli. Three methods were used: lowest electrical threshold, maximum muscle response, and approximate motor point.ResultsA single motor point was identified in 39/40 subjects regardless of method. The area of the site of lowest electrical threshold was smaller (median, 35 mm²) than those using the maximum muscle response (144 mm²) and approximate motor point (132 mm²). There was substantial, but not significant, between-subject variation in motor point location. Fifty three percent of motor points would have been missed if located only by reference to anatomical landmarks.ConclusionsThese results suggested that the motor point’s location cannot be determined a priori and that the identification method will affect both area and location.SignificanceIf it is important to maximally activate a single muscle in isolation, the motor point is best represented by the site producing a maximal but isolated muscle response at the lowest stimulation intensity.     

Tracking motor unit action potentials in the tibialis anterior during fatigue

New surface electromyogram (SEMG) techniques offer the potential to advance knowledge of healthy and diseased motor units. Conduction velocity (CV) estimates, obtained from indwelling electrodes, may provide diagnostic information, but the standard method of CV estimation from SEMG may be of only limited value. We developed a motor unit (MU) tracking algorithm to extract motor unit conduction velocity (MUCV) and motor unit action potential (MUAP) amplitude estimates from SEMG. The technique is designed to provide a noninvasive means of accessing fatigue and recruitment behavior of individual MUs. We have applied this MU tracking algorithm to SEMG data recorded during isometric fatiguing contractions of the tibialis anterior (TA) muscle in nine healthy subjects, at 30%-40% maximum voluntary contraction (MVC). The results reveal that MUCVs and MUAP amplitudes of individual MUs can be estimated and tracked across time. Time-related changes in the MU population may also be monitored. Thus, the SEMG technique employed provides insight into the behavior of the underlying muscle at the MU level by noninvasive means.     

Macro electromyography and motor unit number index in the tibialis anterior muscle: differences and similarities in characterizing motor unit properties in prior polio

Our objective was to establish the usefulness of the noninvasive method of the motor unit number index (MUNIX) in a large muscle and to study how macro electromyography (EMG) and MUNIX complement each other in describing the motor units (MUs) in prior polio. MUNIX and macro EMG were performed in 48 tibialis anterior muscles in 33 prior polio patients. In addition, the reproducibility of MUNIX was investigated. It is shown that MUNIX can be used to characterize MUs with high reproducibility, even in a large muscle. As judged by MUNIX values, the patients had a 25% reduction of motor neurons, whereas the macro EMG indicated a loss of 60% of the neurons. Macro EMG showed more pronounced changes compared with control material than the MUNIX. One of the reasons for this finding may be the difference in MU populations studied with the two methods.     

The effect of contraction intensity on motor unit number estimates of the tibialis anterior.

OBJECTIVE: To examine the effect of contractile level on motor unit number estimates (MUNEs) and establish the contraction intensity that will yield the most representative MUNE for the tibialis anterior (TA) muscle. METHODS: Surface and intramuscular electromyographic (EMG) signals were collected during a range of submaximal (threshold, 10, 20, 30 and 40% MVC) isometric dorsiflexion contractions using decomposition-enhanced spike-triggered averaging (DE-STA). Six MUNEs were calculated, one for each of the five intensities, and an ensemble sixth MUNE that had equal MU contributions from all intensities. RESULTS: Mean surface-motor unit potential sizes increased significantly (26-69 microV) and MUNEs decreased accordingly (226-91) as contraction intensity increased from threshold to 40% MVC, respectively (P<0.05). The ensemble MUNE was 153, and extrapolated to approximately 25% MVC. CONCLUSIONS: There was a significant and progressive decline in the MUNE as contraction intensity increased, confirming the importance of monitoring torque during data collection. The ensemble MUNE suggests that collecting EMG signals at a contraction intensity of approximately 25% MVC provides the most representative sample of the actual number and sizes of MUs in the TA. SIGNIFICANCE: Establishing appropriate contraction intensities improves the utility of DE-STA as a useful method for tracking changes to the MU pool in disease states and healthy aging.     

Sural nerve stimulation and motor control of tibialis anterior muscle in spastic paresis

In patients with spastic paraparesis, increased extensor tonus can be decreased by stimulation of flexor reflex afferents. This should improve dorsiflexion of the foot and reduce the sense of effort. We therefore examined ability to maintain stable firing of a single motor unit (SMU) in tibialis anterior muscle and force of dorsiflexion in 17 normal subjects and 9 with spastic paresis, during several minutes of tonic nonpainful stimulation (20 Hz, 0.1 msec) of the sural nerve at the ankle (SNS). Subjects were asked to maintain stable SMU firing first with, then without auditory feedback of the motor unit potential. SNS was then applied for several minutes. In normal subjects, the force of dorsiflexion increased 33 +/- 26% with SNS and 2.5% +/- 5% without SNS (p less than 0.0005). Most subjects noted increased resistance to dorsiflexion during SNS that resulted in greater innervation of tibialis anterior muscle. In six abnormal subjects, the force of dorsiflexion increased 30 +/- 30% with SNS, but no increase was recorded without SNS. In normal subjects and those with spastic paresis of the legs, SNS increased innervation of tibialis anterior muscle and awareness of greater effort required to maintain constant innervation. The altered proprioception may depend on facilitation of motor neurons.     

Behavior of single motor units of human tibialis anterior muscle during voluntary shortening contraction under constant load torque

The recruitment and discharge frequency of motor units during voluntary shortening contraction with constant load torque were studied in tibialis anterior muscle of 10 human subjects trained to dorsiflex the tibiopedal joint as linearly as possible from 30 degrees plantar flexion from the neutral position (tibiopedal joint angle, 90 degrees) by 20 degrees in 1, 2, 3, 5, 8, and 10 s. A constant load torque of 0, 5, 10, 20, and 25% of maximum voluntary torque of the muscle was applied. When speed of shortening contraction was constant there was considerable degree of constancy in the muscle length at which individual motor units were recruited. However, the recruitment order was not rigidly fixed among the units whose length range of recruitment overlapped. When the contraction was performed faster the units were recruited earlier. The discharge frequencies of the motor units changed little with a given ramp shortening of the muscle. There were also few changes in frequency among different contraction speeds. With increasing load torque to the muscle, the discharge frequency increased slightly at a rate of 1 to 2 Hz by increase of the load. The results suggest that the speed of shortening was coded by recruitment of motor units and that discharge frequency did not play any major role when a muscle was shortened under constant load torque.     

Modulation of H reflexes in human tibialis anterior muscle with passive movement

Significant movement-induced gain changes in H reflexes have been observed in soleus muscle following passive movement of the lower limb. Hypotheses from these concepts were tested on magnitudes of H reflexes in tonically contracted tibialis anterior. From eleven subjects at rates of 20 and 60 r.p.m. passive leg movement, statistically significant attenuation from controls and phasic modulation occurred. The results make more general the conclusions from soleus H reflexes. However, the functional effect should be much smaller, as tibialis anterior H reflexes are smaller compared to those in soleus.     

Somatotopic relations between the motor nucleus and its innervated muscle fibers in the cat tibialis anterior

The normal development of the anatomic relationships between the motoneurons of the tibialis anterior (TA) muscle and their innervated muscle fibers was studied in 1-, 6-, and 12-week-old and adult cats. The motoneurons of the anterior branch and the contralateral posterior branch of the TA nerve were retrogradely labeled with horseradish peroxidase. Within the TA motor nucleus, anterior branch motoneurons (63% of total) were located rostrally and posterior branch motoneurons (37% of total) were located more caudally. The distributions of soma diameters of labeled motoneurons were bimodal in all age groups, allowing a presumptive division into gamma (small) and alpha (large) motoneurons. The posterior branch contained 52% of the total gamma motoneurons but only 28% of the total alpha motoneurons. Within the TA muscle, the regions innervated by the anterior and posterior branches were clearly segregated as determined by glycogen depletion. Myofibrillar ATPase staining at pH 4.4 demonstrated that the posterior branch innervated a higher proportion (56%) of types I and IIA fibers than the anterior. Our results support the hypothesis that a topographic relationship exists between the locus of a motoneuron within its motor nucleus and the position of its innervated muscle fibers within the muscle. Since these topographic relationships apply to all age groups studied, the muscle volume innervated by each muscle nerve branch appears to represent a reproducible developmental unit with distinct anatomic, physiologic and possibly functional properties. This unit may be termed a muscle “compartment.”     

Recovery time of motor evoked potentials following lengthening and shortening muscle action in the tibialis anterior

Motor evoked potentials (MEP) at rest remain facilitated following an isometric muscle contraction. Because the pre-synaptic and post-synaptic control of shortening (SHO) and lengthening (LEN) contractions differs, the possibility exists that the recovery of the MEP is also task specific. The time course of MEP recovery was assessed in the tibialis anterior following SHO and LEN (0.26 rad/s) at 25% and 80% of maximal voluntary contraction. Following LEN and SHO contractions, the MEP recovered to baseline levels within 10 s. Despite task-specific differences between SHO and LEN contractions, the MEP facilitation from the augmented neurotransmitter release appears to be short lasting and not influenced by contraction type.     

Improved motor response due to chronic electrical stimulation of denervated tibialis anterior muscle in humans

Nine patients with complete denervation of the tibialis anterior were admitted to a stimulation program in order to restore dorsiflexion of the foot. Best results were obtained with pulses of 20-msec pulse width and 20-msec interval. After 3 weeks of training for 2 X 20 min/day, dorsiflexion due to stimulation was increased in all patients. In some of them, gait could be improved during the swing phase using electrical stimulation. The applied training program thus reversed the course of disuse atrophy and proved the feasibility of functional electrical stimulation for patients with denervated muscles.     

Three-dimensional structure of cat tibialis anterior motor units

The motor unit is the basic unit for force production in a muscle. However, the position and shape of the territory of a motor unit within the muscle have not been defined precisely. The territories of five motor units in the cat tibialis anterior muscle were reconstructed three-dimensionally (3-D) from tracings of the glycogen-depleted fibers belonging to each unit. The motor unit territories did not span the entire length of the muscle and their cross-sectional areas tapered along the proximodistal axis producing a conical shape. In addition, the position of the territory of each unit shifted in an anterior–posterior plane along the longitudinal axis of the muscle, presumably as a consequence of the pinnation of the fibers. The area of the motor unit territory at any given level along the proximodistal axis was highly correlated with the number of fibers within the territory at that level. Connective tissue boundaries (outlining fascicles) appeared to have a strong influence on the shape of the territory, territories showed abrupt changes at connective tissue boundaries as groups of motor unit fibers within a fascicle often terminated together while motor unit fibers in neighboring fascicles did not terminate. It is likely that the mechanical impact of the recruitment of a motor unit is affected by the location and shape of motor units within the same muscle area. Since there is a close relationship between the area of the territory of a motor unit and the number of fibers in the motor unit, while the density of unit fibers remains the same, then the same factor(s) which regulate the number of fibers innervated by a motoneuron may also determine the territory area.© 1995 John Wiley & Sons, Inc.     

Comparison of single motor unit responses to transcranial magnetic and peroneal nerve stimulation in the tibialis anterior muscle of patients with amyotrophic lateral sclerosis

Responses of single tibialis anterior motor units to transcranial magnetic stimulation and to a synchronized la volley evoked by peripheral nerve electrical stimulation were obtained in amyotrophic lateral sclerosis (ALS) patients and normal controls. Whereas the units of normal subjects exhibited rather stereotyped short-latency spike density peaks in response to both types of stimulus, the responses of ALS patient units were much less uniform. All ALS patient units exhibited a response to the synchronized la volley indistinguishable from that of normal subjects, indicating that the investigated spinal motoneurons are capable of normal excitatory responses in ALS patients. More than half of the ALS patient units responded to the transcranial magnetic stimulus with prolonged spike-density peaks appearing at a latency consistent with the notion that these pathological peaks are evoked by some relatively hyperexcitable structures presynaptic to the corticomotoneurons.     

Shortening reaction of human tibialis anterior

The shortening reaction of tibialis anterior was observed in 6 of 25 normal subjects, in 6 of 40 patients with upper motor neuron syndromes, and in 11 of 17 patients with Parkinson's disease. The latency of the shortening reaction was comparable with that of the latter part of the long-latency stretch reflexes. The magnitude of the shortening reaction increased with the velocity of the movement that produced it and increased with background voluntary force of plantar flexion in all but the patients with Parkinson's disease. It was not affected by vibration in the patients with Parkinson's disease. The presence of the shortening reaction was not correlated with the clinical impression of increased tone.     

Effects of chronic low frequency electrical stimulation on normal human tibialis anterior muscle.

The loss of force that occurred during intermittent electrically evoked tetanic contractions was determined for the tibialis anterior muscle of normal subjects. Adult muscles showed a characteristic reduction of tension over the first two to three minutes until a steady plateau was reached. Muscles of young children showed no comparable decrease of the initial tension in response to this method of fatigue testing. After fatigue the muscles of both groups of subjects produced a higher proportion of tension at lower rates of stimulation. Following prolonged chronic low frequency stimulation at 8-10 Hz, adult muscles showed a significant increase (p less than 0.01) in fatigue resistance compared to unstimulated control: the muscles of the normal child showed no measured change. It is concluded that it is possible to alter the properties of adult human muscle by superimposed low frequency electrical stimulation.     

Motor unit number estimates in the tibialis anterior muscle of young, old, and very old men

The rate of motor unit (MU) loss and its influence on the progression of sarcopenia is not well understood. Therefore, the main purpose of this study was to estimate and compare numbers of MUs in the tibialis anterior (TA) of young men ( approximately 25 years) and two groups of older men ( approximately 65 years and >/=80 years). Decomposition-enhanced spike-triggered averaging was used to collect surface and intramuscular electromyographic signals during isometric dorsiflexions at 25% of maximum voluntary contraction. The mean surface-MU potential size was divided into the maximum M wave to calculate the motor unit number estimate (MUNE). The MUNE was significantly reduced in the old (91) compared to young (150) men, and further reduced in the very old men (59). Despite the smaller MUNE at age 65, strength was not reduced until beyond 80 years. This suggests that age-related MU loss in the TA does not limit function until a critical threshold is reached.     

Sleep influences on diaphragmatic motor unit discharge

The discharge of motor units in the costal and crural regions of the diaphragm was studied in unrestrained cats during defined sleep and waking states. Changes in motor unit recruitment and pattern of activity were observed for different sleep-waking states. During periods of active waking, many motor units were recruited and discrimination of single-unit waveforms was difficult. However, in the transition from active to quiet waking, many diaphragmatic motor units ceased discharging, thus making it possible to discern single-unit waveforms. This cessation of motor unit activity continued during the transition from quiet waking (AW) to quiet sleep (QS) and from QS to rapid eye movement (REM) sleep. In some diaphragmatic motor units, discharge stopped completely during REM sleep and resumed only upon arousal. Thus, it was apparent that the recruitment of diaphragmatic motor units was markedly affected by the sleep-waking state. Changes in the patterns of discharge of diaphragmatic motor units also occurred during different sleep-waking states. Motor unit firing rate was typically slower in QS than AW. The rate of motor unit discharge during REM sleep varied considerably. Autocorrelation histograms demonstrated periodic patterns of motor unit discharge within inspiratory bursts. Intervals of repetitive peaks in the autocorrelation histograms ranged from 40 to 110 ms. These periodic patterns were strongest during AW and REM sleep and generally attenuated during QS. Cross-correlation histograms revealed the presence of synchronous activity between motor units in the diaphragm. This coupling of diaphragmatic motor unit discharge was also attenuated during QS compared with AW and REM sleep. Together, these results demonstrated a marked influence of the sleep-waking state on the neuromotor control of the diaphragm.