Inhibition of motor unit firing during experimental muscle pain in humans

Electromyographic activity was recorded in the masseter muscle to investigate whether the firing characteristics of single motor units (SMUs) were affected by muscle pain. Capsaicin was injected into the masseter to induce pain. The interspike interval (ISI) and recruitment threshold of SMUs were measured while subjects performed isometric contractions at 5, 7.5, 10, 15, and 20% of maximum voluntary contraction. All subjects were able to maintain a stable isometric force during pain, but the mean ISI was significantly increased without changing the recruitment threshold. In all the experimental conditions, the firing frequency increased with increasing force, and SMUs recruited at low force fired at higher rates for all force levels. These results suggest that acute stimulation of nociceptive muscle afferents inhibits SMU activity without changing recruitment order in the homonymous muscle.     

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.     

Proprioceptive control of human wrist extensor motor units during an attention-demanding task

The responsiveness of the tonically firing single motor units (SMU) to Ia afferent volleys elicited by either mechanical (T-reflex) or electrical nerve stimulation (H-reflex) was tested in the extensor carpi radialis muscle (ECR) while the subjects were maintaining a steady wrist extension force using visual feedback set either at low or high gain. The aim was to determine whether the proprioceptive control of tonic motoneuronal activity depends on the level of attentiveness required by the behavioural context. The response probability of the SMUs to tendon taps was significantly higher (p<0.0001) and that to electrical nerve stimulation was lower (p<0.001) during the more demanding task. Since these changes in SMU responsiveness were not accompanied by any differences in either the motor unit firing patterns or the mean levels of EMG muscle activity, it can be concluded that there were no attention-related changes in the net excitatory drive to the ECR motoneurons. These results are consistent with the idea that fusimotor sensitization of the muscle spindle may have occurred in the more demanding task: an increase in the mechanical sensitivity of the muscle spindles would certainly account for both the T-reflex facilitation and the H-reflex depression observed. The attention-demanding task therefore seemed to involve an independent fusimotor drive activation process. The results of this study suggest that an adaptation of the fusimotor system occurs in humans, depending on the levels of attention and accuracy required to perform the ongoing motor task, as previously reported to occur in animals.     

Recruitment stability in masseter motor units during isometric voluntary contractions

Recruitment of single motor units (SMUs) of the masseter muscle was studied using macro representation (MacroRep) as the indicator of motor unit size. When subjects followed a slow isometric force ramp, units were usually recruited in order of MacroRep size. However, pooling the data from repeated ramps in the same subject resulted in a weak relationship between MacroRep size and force recruitment threshold, probably due to marked variations in the relative contributions of the jaw muscles, and varying levels of cocontraction, in the development of total bite force in each ramp. The force recruitment thresholds of individual SMUs showed marked variability, but recruitment threshold stability was improved when expressed as a percentage of maximum surface electromyographic (SEMG) activity in the ipsilateral masseter. Therefore the SEMG recruitment threshold was concluded to be a more stable and accurate indicator of the SMU's position in the recruitment hierarchy in a given muscle. It was concluded that SMUs in masseter are recruited according to the size principle, and that when investigating recruitment in jaw muscles, SEMG recruitment threshold should be used in preference to force recruitment threshold. © 1998 John Wiley & Sons, Inc. Muscle Nerve 21:1290–1298, 1998.     

Analysis of the fluctuations in the interspike intervals of abducens nucleus neurons during ocular fixation in the alert cat

The behavior of abducens nucleus motoneurons and internuclear neurons was recorded during eye fixation in the alert cat. The interspike interval (ISI) values during a given fixation followed a normal distribution, with coefficients of variation for motoneurons and interneurons ranging from 4.6 to 16% and 5.7 to 21.7%, respectively. The ISI mean was linearly related to its standard deviation and to the coefficient of variation. The power spectral density of ISI fluctuations did not reveal any relevant peak. The autocorrelation function of ISI fluctuations was flat except at the origin. Results suggest the presence of a gaussian white noise superimposed on the clock-like firing of the activity of abducens neurons during ocular fixation. Some physiological implications of the results are discussed.     

Discharge variability and physiological properties of human masseter motor units

Intramuscular electrodes were used to study discharge variability in motor units of human masseter whose physiological properties were determined using spike-triggered averaging. Subjects voluntarily controlled the mean firing rate of a selected motor unit at 10 Hz for 15 min of continuous activation. Discharge variability was assessed at the beginning and end of this period. In 81% of units, the discharge variability at a mean interspike interval (ISI) of 100 ms increased after 15 min of continuous activity. There was a wide range of discharge variability within the population of masseter units studied, but no significant correlations were found between initial discharge variability and recruitment threshold, twitch tension or time-to-peak tension (TTP). There was, however, a significant correlation between motor unit fatigability and its initial discharge variability. This represents a link between the motoneuron and the functional properties of the muscle fibers in innervates.     

Effects of premotion silent period on single motor unit firing at initiation of rapid contraction

We compared the single motor unit (SMU) activity between movements with a premotion silent period (PMSP) and without PMSP in EMG. Fourteen SMUs in the gastrocnemius muscle and 6 SMUs in the soleus muscle were recorded from 5 volunteers during isometric plantar flexion. Tonically firing SMUs failed to fire just before the onset of rapid contraction with PMSP more frequently than without PMSP. SMUs tended to fire within 10 msec (the gastrocnemius SMUs) or 20 msec (the soleus SMUs) from the onset of the phasic EMG discharge when PMSP occurred. In a rapid contraction without PMSP, the initial firing of SMUs occurred with longer latency than that in a rapid contraction with PMSP. The latency of the initial SMU firing in a rapid contraction related to the preceding time of the last SMU firing during a sustained contraction to the onset of the phasic EMG discharge. When the preceding firing was long enough, the latency distributed around 10 msec. On the other hand, for shorter preceding times, the latency lengthened with shortening of the preceding time. It is suggested that the PMSP makes the preceding time long and increases the susceptibility of motor units to the descending command at the initiation of a rapid contraction.     

Effects of experimental muscle pain on mechanical properties of single motor units in human masseter.

OBJECTIVE: Muscle pain is known to influence muscle activity but the details of its effects on the mechanical properties of single motor units (SMU) have not been described. We have recently reported a decreased firing rate of SMU in the human masseter muscle during painful contractions with a constant force output. Force output can be modulated by the SMU discharge rate in relation to the contractile properties of SMU. Therefore, the objective of the present study was to measure the mechanical properties of SMU in the masseter to clarify the mechanism which underlies the decrease in SMU firing rate during jaw-muscle pain. METHODS: A spike-triggered averaging (STA) technique was used to determine the mechanical properties of low-threshold SMU in the masseter muscle recorded with fine wire electrodes during a voluntary isometric contraction. The twitch amplitude, contraction time, and half-relaxation time were determined from the averaged force records before and during experimental jaw-muscle pain induced by injection of 0.2 ml (100 microg/ml) capsaicin in 8 healthy subjects. Injections of 0.2 ml isotonic saline served as a non-painful control in 11 healthy subjects. RESULTS: The twitch amplitude was significantly increased during capsaicin-evoked muscle pain (P<0.001) without significant changes of half-relaxation time and contraction time. No significant changes in SMU twitch properties were observed during the control injections. CONCLUSIONS: Potentiation of twitch force could be a possible compensatory mechanism to maintain a constant force output during painful isometric contractions when SMU firing decreases. This finding therefore provides new information on the adaptation of motor function by muscle pain.     

Detecting neuronal activity changes using an interspike interval algorithm compared with using visual inspection

A universally accepted method for efficiently detecting neuronal activity changes (NACs) in neurophysiological studies has not been established. Visual inspection is still considered to be one of the most reliable methods, although it is limited when it is used for analyzing large quantities of data. In this study, an algorithm that considers interspike intervals (ISIs) was developed to define the onset of NACs. Two criteria, involving the mean and the standard deviation (S.D.) of the ISIs during a control period, were used in the ISI algorithm to evaluate the NACs that occurred during a detection period. The first, an ISI decrease of more than 1 S.D. from the mean ISI of the control period, proved to be an effective criterion for qualifying the increased NACs (firing rate increases). The second, an ISI increase greater than 3 S.D.s, efficiently demarcated periods of decreased NACs (firing rate decreases). Statistically significant correlations between the detection of NAC onset times by the ISI algorithm and the detection of those times by visual inspections were observed after offline analyses of recorded neuronal activity. The present results suggest that this ISI algorithm is a reliable and efficient way of defining the onset of NACs.     

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.     

Postnatal development of synaptic inputs to rat masseter motoneurons

We examined postnatal changes in rat masseter motoneuron morphology and the density of synaptic inputs to masseter motoneurons using retrograde labeling combined with synaptophysin immunohistochemistry. The cross-sectional area and perimeter of masseter motoneurons increased through P21 whereas synaptic input density increased throughout the time frame sampled. Data suggest that changes in masseter motoneuron morphology and the density of its synaptic input contribute to the maturation of mastication behavior.     

AAEM minimonograph #3: motor unit recruitment.

Motor unit recruitment is the process by which different motor units are activated to produce a given level and type of muscle contraction. At minimal levels of muscle contraction (innervation), muscle force is graded by changes in firing rate (rate coding) of individual motoneurons (MNs). At higher levels of innervation, recruitment is accomplished by the addition of different motor units firing at or above physiologic tremor rate. During slowly graded and ballistic increases in force, motor units are recruited in rank order of their size. In addition to MN soma diameter, other factors contribute to the selectivity of MN activation. For la afferent MN activation in the cat, synaptic density and efficacy as well as specific membrane resistance are also rank ordered for slow, fatigue resistant, and fast fatigue motor units with slow motor units recruited first. The central drive for motor unit activation is distributed to all the MNs of the pool serving a given muscle. Size-structure organization of the MN pool determines the order of recruitment and how MNs interact with each other. Disorders of the motor unit affect recruitment. A method for the clinical electromyographic assessment of recruitment is suggested. Assessment is made at three levels of innervation: minimal contraction for onset and recruitment firing rates; moderate contraction required to maintain the limb against gravity for the maximum number of motor units, their firing rates, and motor unit spikes/s; maximal voluntary contraction (MVC) for detection of high threshold enlarged motor units characteristic of reinnervation and completeness of the interference pattern (IP). Loss of muscle fibers results in early and excessive recruitment at minimal and moderate levels of innervation. Loss of motor units can result in both an increased rate and range of single motor unit firing at all levels of innervation. With reinnervation and enlargement of motor units, firing rates increase significantly and the interference pattern during MVC is incomplete.     

Further evidence for corticomotor hyperexcitability in amyotrophic lateral sclerosis

A collision experiment has been used to investigate repetitive firing of first dorsal interosseous motoneurons following a single transcranial magnetic stimulus (TMS) in healthy subjects and patients with amyotrophic lateral sclerosis (ALS). An appropriately timed supramaximal peripheral nerve shock blocks the first descending impulses in the motor axons and allows the response due to repetitive firing to be quantified. Multiple firing of motoneurons in healthy subjects increases as TMS intensity rises and saturates at about 1.25 times threshold. Increasing background force also augments repetitive firing and saturates at force levels above 50% maximum. The ratio of the area of the response attributed to repetitive motoneuron firing to the area of the initial direct response to TMS was compared in 10 ALS patients and 10 healthy controls. In ALS patients, the ratio was significantly higher (P = 0. 0005), indicating a greater degree of repetitive firing of motoneurons. This suggests that, in ALS, there is corticomotor hyperexcitability either at the spinal motoneuron or motor cortex.     

Approximate entropy of motoneuron firing patterns during a motor preparation task

The aim of this study was to test whether approximate entropy (ApEn) analysis provides a suitable method of detecting differences induced by a motor preparation task in time-ordered inter-spike intervals (ISIs) recorded in tonically firing motoneurons. Unlike classical methods of analyzing neuronal discharge variability, in which serial order is no taken into account, the approximate entropy (ApEn) was proposed by Pincus [Pincus SM. Approximate entropy as a measure of system complexity. Proc Natl Acad Sci USA 1991;88:2297-301] to analyze ordered series. ApEn statistic is a number assigned to an ordered series, where higher values correspond to greater serial irregularity. In the present study, the activity of 31 single motor units (SMUs) was recorded in human extensor carpi radialis muscles and the ISI durations were analyzed during the performance of a pre-cueing reaction time motor task involving a 3-s preparatory period. ApEn values were computed for each SMU during three steps of the preparatory period and during the preceding control period. Lower ApEn values, were found during preparatory period. The decrease in ApEn values, i.e., the increase in serial regularity, was monotonic from the control to the end of the preparatory period. These results show that ApEn model-independent statistics are a relevant means of detecting changes related to motor preparation in the regularity of time-ordered inter-spike intervals (ISIs).     

Are motoneurons involved in muscular dystrophy?

In the early seventies, a suggestion that even in muscular dystrophy a neurogenic factor may be involved, was formulated. The argument which followed this suggestion, resulted in eventual abandoning of this concept even by its author. This discussion however has never been supported by any systematic study of motoneuron activity in muscular dystrophy. We examined an activity of motoneurons supplying brachial biceps in eight controls and 26 patients affected by Duchenne muscular dystrophy by studying single motor unit (MU) potentials picked up by fine wire bipolar electrodes. In the majority of patients, MU firing rates were higher as compared to controls and increased more rapidly with increasing force level. The relationship between standard deviation of interspike intervals and their mean value, SD(x), was shifted towards the shorter intervals and lower SDs. The numerical values describing these changes were correlated with severity of the disease. There is evidence that the break-point of the function SD(x) is correlated with motoneuron properties, in particular with after-hyperpolarization duration. In muscular dystrophy, this break-point corresponds to the shorter interspike intervals. We suggest that the motoneurons in muscular dystrophy are altered either in response to the muscle degeneration, or as a result of the disease itself.     

The volitional unit: a functional concept in cortico-motoneuronal connections in humans

We used the EMG precision decomposition technique to resolve complex EMG signals and derive information about the firing times of a family of motor units (MUs) and the force they produce. The active units shared a common behavior among their firing rates, a concept described by DeLuca et al. and termed the ‘common drive’. This ‘common’ behavior was extracted as the average of the firing rates of MUs and found to track the subject's force trajectory. In this paper, we propose the existence of functional cortico-motoneuronal connections which provide for a large number of combinations between affector cortical motoneurons (CMNs) and effector spinal motoneurons (SMNs) for the generation of a purposeful movement. We argue that these connections provide the essential link between volition and movement and function as a ‘volitional unit’ which consists of the CMNs, the SMNs and the anatomical and interneuronal connections between them.     

Adult mouse motor units develop almost all of their force in the subprimary range: a new all-or-none strategy for force recruitment?

Classical studies of the mammalian neuromuscular system have shown an impressive adaptation match between the intrinsic properties of motoneurons and the contractile properties of their motor units. In these studies, the rate at which motoneurons start to fire repetitively corresponds to the rate at which individual twitches start to sum, and the firing rate increases linearly with the amount of excitation ("primary range") up to the point where the motor unit develops its maximal force. This allows for the gradation of the force produced by a motor unit by rate modulation. In adult mouse motoneurons, however, we recently described a regime of firing ("subprimary range") that appears at lower excitation than what is required for the primary range, a finding that might challenge the classical conception. To investigate the force production of mouse motor units, we simultaneously recorded, for the first time, the motoneuron discharge elicited by intracellular ramps of current and the force developed by its motor unit. We showed that the motor unit developed nearly its maximal force during the subprimary range. This was found to be the case regardless of the input resistance of the motoneuron, the contraction speed, or the tetanic force of the motor unit. Our work suggests that force modulation in small mammals mainly relies on the number of motor units that are recruited rather than on rate modulation of individual motor units.     

Changes in the firing properties of neurons in the dentate gyrus with denervation and reinnervation: implications for behavioral recovery

The present study evaluates how the activity of neurons in the dentate gyrus of adult rats is affected by removal of the projection from the ipsilateral entorhinal cortex (EC) and by the reinnervation which follows this injury. We evaluated the average firing rate and characterized interstimulus interval (ISI) parameters for single units in the granule cell layer of the dentate gyrus in two ways: (I) by recording the activity of single neurons prior to and at 15 min and 2, 4, 6, and 8 h. following a unilateral EC lesion; and (II) by calculating average rates for samples of neurons at 2, 4, 6, 8, and 14 days postlesion. Of a sample of 31 neurons whose activity was recorded before and after an EC lesion, 27 (87%) showed decreased activity, and 4 (13%) showed increased activity. The average prelesion firing rate for all cells was 6.5 spikes/s, and the average rate decreased to 2.5 spikes/s at 15 min postlesion. The average firing rate remained depressed for the 8-h recording session, although it was not possible to maintain the recordings for all cells. Evaluations of ISI histograms revealed three general types: (a) a skewed distribution with a single peak; (b) a bimodal distribution with an early peak at intervals of a few ms and a later peak at approximately the same interval as the distributions with single peaks; (c) cells with low firing rates and more or less rectangular distributions. Cells producing each type of ISI histogram exhibited decreases in firing after EC lesions. However, the 4 neurons that exhibited increases in firing had relatively low firing rates prior to the lesion. There were no significant changes in the coefficient of variation or skewness of the ISI histograms following the lesions. The statistical dependency of successive ISIs as revealed by serial correlograms was relatively low in the prelesion sample, and showed no consistent change following the lesion. Comparison of the average firing rates of different samples of neurons at 2-14 days postlesion revealed that the average activity of neurons in the granule cell layer remained depressed at 2 and 4 days postlesion. However, the activity recovered to a level comparable to the prelesion control by 8 days postlesion. The time course of recovery of unit activity was comparable to the time course of sprouting as revealed by previous electrophysiological studies.(ABSTRACT TRUNCATED AT 400 WORDS)     

Recording single motor unit activity of human nasal muscles with surface electrodes: applications for respiration and speech.

A method is presented for recording nasal single motor unit (SMU) potentials from the skin surface using a 3-pole 'branched' bipolar electrode. Stable, high-quality recordings of single motor unit activity were obtained for up to 3 h. Branched electrode arrays were capable of locating an SMU's maximal voltage point within 5 mm. We examined nasal SMU discharge patterns in relation to respiration in 9 adult humans. The majority of SMUs which discharged during quiet breathing began firing late in expiration and ceased firing in mid-inspiration, other SMUs discharged only during expiration, and a few fired continually with frequency modulation during breath cycles. With increased ventilation, new SMUs were recruited, and previously active SMUs increased the frequency and duration of their discharge. We examined the discharge of 13 units (5 adults) which discharged during speech but were never active during quiet or moderately increased breathing. Some of these SMUs fired during production of nasal consonants, and others were active for articulations involving facial movements (bilabial stops, labio-dental fricatives, and vowels produced with lip movement). By providing information about motor neuron recruitment which cannot be obtained from gross EMG recordings, surface recording of unit potentials may be useful in studying the central nervous control of the nasal upper airway, face, and neck for respiration and speech.     

Discharge properties of single motor units in patients with spinal cord injuries

To study neurophysiological correlates of spastic paresis, we analyzed the discharge pattern of single motor units (SMUs) during sustained voluntary contraction from muscles weakened by spinal cord injury (SCI) and from muscle of near normal strength just at or above the level of injury., The average firing rate of SMUs was reduced in patients' biceps brachii and tibialis anterior muscles compared with controls, but not in the triceps brachii. Floating serial correlation coefficients obtained form successive interdischarge intervals were significantly more positive in patients than in controls in all three muscles. One statistical measure of regularity of discharge, akin to a coefficient of variation, was best able to differentiate patient and control SMUs. Increased discharge variability in muscle just above the level of injury suggested that subtle effects of traumatic SCIs were more extended than was clinically apparent. Although consistent statistical differences could be measured, these changes were not specific to SCI, nor were all SMUs equally affected. © 1993 John Wiley & Sons, Inc.