Short latency trigemino-sternocleidomastoid response in muscles in patients with spasmodic torticollis and blepharospasm.

OBJECTIVES: To further elucidate the pathogenesis of focal dystonias. METHODS: Short latency responses can be recorded in tonically active sternocleidomastoid muscles after stimulation of the infraorbital branch of the trigeminal nerve. Such trigemino-sternocleidomastoid response consists of a bilateral positive/negative wave in the average of unrectified surface EMG, corresponding to a short period of inhibition of motor unit firing. This brain stem reflex was investigated in 10 normal subjects, in 16 patients affected by spasmodic torticollis (ST) and in 10 patients with blepharospasm (BSP). RESULTS: All ST patients presented abnormalities of SCM responses after infraorbital nerve stimulation. The abnormalities were bilateral in all but one of the patients and were independent from previous treatment with botulinum toxin. No BSP patients showed alterations of this reflex. CONCLUSIONS: Abnormalities of brain stem interneurons which are responsible for oligosynaptic exteroceptive suppression reflexes occur specifically in ST. These findings further support the relevance of sensory inputs in the determinism of focal dystonias.     

A method for quantifying reflex responses from intra-muscular and surface electromyogram

Measuring human reflex responses from electromyogram (EMG) traces in an accurate, repeatable and reliable way with a high degree of specificity has traditionally been a difficult task. This paper describes a new method that can be used to quantify reflex responses from both surface and intra-muscular EMG. This technique extends the classical cumulative sum (CUSUM) calculations by defining precise points for the calculation of latencies, durations and strengths to facilitate automatic reflex detection and permit the strength of a reflex to be defined in absolute units. The effect of varying the pre-stimulus time, the number of trials averaged and the amount of filtering used on the identification and classification of reflex parameters are also investigated. Furthermore, the effect of noise on these values, and how to remove it, is discussed. The new method, which is an expansion of the CUSUM analysis, is compared and contrasted with the more common threshold-crossing method in two different muscles: masseter and first dorsal interosseous (FDI), in experiments utilizing both mechanical and electrical stimulation. There are a number of advantages to using the new method; not only does the modified CUSUM method detect reflexes earlier than threshold-crossing methods but also the strength and duration are less susceptible to averaging and filtering parameters while giving a better indication of the reflex size. The data suggests that a pre-stimulus analysis period of at least 100 ms be used to correctly identify the variability inherent in EMG traces. It is also concluded that for subtle reflexes, 50 stimuli should be the minimum number used when spike trigger averaging is employed as lower numbers are associated with much greater pre-stimulus variability. Zero-phase filtering the rectified averaged EMG traces is recommended as this makes it easier to identify significant changes in the electrical activity of the muscle in question. In addition, noise estimation and removal from averaged rectified EMG recordings yields results that are a more accurate representation of the synaptic activity of the motor units in question.     

Reflex responses of masseter muscles to sound

Acoustic stimuli can evoke reflex EMG responses (acoustic jaw reflex) in the masseter muscle. Although these were previously ascribed to activation of cochlear receptors, high intensity sound can also activate vestibular receptors. Since anatomical and physiological studies, both in animals and humans, have shown that masseter muscles are a target for vestibular inputs we have recently reassessed the vestibular contribution to masseter reflexes. We found that high intensity sound evokes two bilateral and symmetrical short-latency responses in active unrectified masseter EMG of healthy subjects: a high threshold, early p11/n15 wave and a lower threshold, later p16/n21 wave. Both of these reflexes are inhibitory but differ in their threshold, latency and appearance in the rectified EMG average. Experiments in healthy subjects and in patients with selective lesions showed that vestibular receptors were responsible for the p11/n15 wave (vestibulo-masseteric reflex) whereas cochlear receptors were responsible for the p16/n21 wave (acoustic masseteric reflex). The possible functional significance of the double vestibular control over masseter muscles is discussed.     

Surface EMG recording of heteronymous reflex excitation of semitendinosus motoneurones by group II afferents.

OBJECTIVE: A potent stretch reflex originates in muscle spindle secondary endings and is mediated by group II muscle afferents. Electrical stimulation of peripheral nerve could also induce group II facilitation, as found in single motor unit recordings for various nerve-muscle combinations in man. The aim of the present investigation was to use surface electromyogram (EMG) to record and to quantify heteronymous excitation of semitendinosus (ST) motoneurones by group II afferents of the tibial nerve. METHODS: This study included 20 healthy subjects. The conditioning stimulation of the tibial nerve was delivered at the popliteal fossa at two intensity levels and for two levels of ST contraction. EMG activity was recorded by surface electrodes placed over the ST muscle, and the averaged and rectified ST EMG signal was analyzed. RESULTS: We observed 4 periods of interest: a first period of prestimulus background EMG activity; a second period of early reinforcement of ST EMG activity starting 30 ms poststimulus and lasting for 35-45 ms; a third period of relative inhibition of ST contraction; a fourth period of late reinforcement of poststimulus ST EMG activity. CONCLUSIONS: We hypothesized that the early period of facilitation was mainly related to heteronymous excitation of ST motoneurones by group II afferents on the basis of the following observations: (i) the amount of facilitation increased for a high stimulus intensity level, which was suitable for group II recruitment; (ii) the onset latency of this facilitation was consistent with the theoretically calculated latency of a group II-mediated reflex. SIGNIFICANCE: Surface EMG recording offers various advantages compared to single motor unit recording to study group II facilitation in the ST muscle. This technique could be applied in the future to confirm that heteronymous reflex excitation by group II afferents is enhanced in spastics and plays an important role in the development of lower limb spasticity.     

Rectification of the EMG is an unnecessary and inappropriate step in the calculation of Corticomuscular coherence

Corticomuscular coherence (CMC) estimation is a frequency domain method used to detect a linear coupling between rhythmic activity recorded from sensorimotor cortex (EEG or MEG) and the electromyogram (EMG) of active muscles. In motor neuroscience, rectification of the surface EMG is a common pre-processing step prior to calculating CMC, intended to maximize information about action potential timing, whilst suppressing information relating to motor unit action potential (MUAP) shape. Rectification is believed to produce a general shift in the EMG spectrum towards lower frequencies, including those around the mean motor unit discharge rate. However, there are no published data to support the claim that EMG rectification enhances the detection of CMC. Furthermore, performing coherence analysis after the non-linear procedure of rectification, which results in a significant distortion of the EMG spectrum, is considered fundamentally flawed in engineering and digital signal processing. We calculated CMC between sensorimotor cortex EEG and EMG of two hand muscles during a key grip task in 14 healthy subjects. CMC calculated using unrectified and rectified EMG was compared. The use of rectified EMG did not enhance the detection of CMC, nor was there any evidence that MUAP shape information had an adverse effect on the CMC estimation. EMG rectification had inconsistent effects on the power and coherence spectra and obscured the detection of CMC in some cases. We also provide a comprehensive theoretical analysis, which, along with our empirical data, demonstrates that rectification is neither necessary nor appropriate in the calculation of CMC.     

The "Functional -QEMG" method -- a substantial progress in electromyography (EMG)

In contradistinction to the traditional quantitative EMG, our new "Functional-QEMG" method provides new information about structural and functional changes in the whole population of active motor units (MUs) in various neuromuscular disorders. Individual motor unit action potentials (MUAPs) and the interference pattern (IP) recordings are analyzed not as complementary measurements but as one integral test. Such a complex of EMG signals is submitted to a non-linear dynamic analysis determining interrelationships between an active MU size and its functional properties. Structural changes in MU size represent the primary destructive process, while the resulting changes in MU functional properties due to a compensatory mechanism (a secondary restorative process) provide new and very useful diagnostic information. All EMG data are processed online and automatically classified by a special computer-assisted diagnostic program as either a normal or pathological (myogenic or neurogenic) EMG recording. At the same time severity of muscle damage is assessed. This article illustrates how both the efficacy and limitations of compensatory mechanisms are related to structural damage in various neuromuscular disorders. The "Functional-QEMG" method application in clinical practice for over ten years has evidenced that this new approach is a turning point in improving the EMG diagnosis. This automatic method provides online reliable answers to most of the questions facing an electromyographer in daily routine investigations.     

Motor units in incomplete spinal cord injury: electrical activity, contractile properties and the effects of biofeedback.

The electrical and contractile properties of hand muscles in a selected population of quadriplegic subjects were studied intensively before and after EMG biofeedback. Spontaneously active motor units and units that could only be slowly and weakly activated were observed in these subjects, in addition to units that were voluntarily activated normally. This suggests a considerable overlap of surviving motor neurons to a single muscle that are below, near or above the level of a lesion. Despite the common occurrence of polyphasic potentials and other signs of neuromuscular reinnervation, the average twitch tension of single motor units in hand muscles of quadriplegic subjects was not significantly different from that in control subjects. Nor did it increase after biofeedback training that typically increased the peak surface EMG by a factor of 2-5 times. The percentage of spontaneously active units was also constant. The surface EMG may be increased during biofeedback by using higher firing rates in motor units that can already be activated, rather than by recruiting previously unavailable motor units.     

Electrodiagnostic findings in syringomyelia

Electrodiagnostic abnormalities are well known to occur in syringomyelia although the findings are nonspecific. The objective of this work was to describe different types of spontaneous electromyographic (EMG) activity and reflex responses, which may be useful and more specific than conventional findings for the electrodiagnosis of syringomyelia. We studied 43 patients with syringomyelia by four-channel surface EMG and by recording the long-latency responses to distal stimulation of the median and tibial nerves. Continuous motor unit activity (CMUA) was found in 18 patients, synchronous motor unit potentials (SMUP) in 10, respiratory synkinesis (RS) in 5, and myokymic discharges in 4. Long-latency responses (LLR) with latencies ranging from 55 to 150 ms were found in 14 patients. Patients with syringomyelia thus show a wide variation of spontaneous EMG activity. An increase in excitability of spinal motor neurons is probably the basic underlying mechanism.     

Relationships between sensory input, motor output and unit activity in interpositus and red nuclei during intentional movement

The relationship between unit activity in interpositus (8 units) and red nuclei (11 units) and the EMG activity of the biceps during intentional elbow flexion movements was investigated by means of cross-correlation analysis. This analysis showed that there were long-lasting (200 msec) changes in the probability of EMG activity both before and after a single spike in neurons which covaried with the motor output. The dependence of the activity of these units on sensory inputs was investigated by (1) calculating the quantitative relationship between angular displacement and unit activity and (2) recording unit activity after the sensory input from peripheral afferents had been eliminated by dorsal rhizotomy.     

Motor unit recruitment and bursts of activity in the surface electromyogram during a sustained contraction

Bursts of activity in the surface electromyogram (EMG) during a sustained contraction have been interpreted as corresponding to the transient recruitment of motor units, but this association has never been confirmed. The current study compared the timing of trains of action potentials discharged by single motor units during a sustained contraction with the bursts of activity detected in the surface EMG signal. The 20 motor units from 6 subjects [recruitment threshold, 35.3 +/- 11.3% maximal voluntary contraction (MVC) force] that were detected with fine wire electrodes discharged 2-9 trains of action potentials (7.2 +/- 5.6 s in duration) when recruited during a contraction that was sustained at a force below its recruitment threshold (target force, 25.4 +/- 10.6% MVC force). High-pass filtering the bipolar surface EMG signal improved its correlation with the single motor unit signal. An algorithm applied to the surface EMG was able to detect 75% of the trains of motor unit action potentials. The results indicate that bursts of activity in the surface EMG during a constant-force contraction correspond to the transient recruitment of higher-threshold motor units in healthy individuals, and these results could assist in the diagnosis and design of treatment in individuals who demonstrate deficits in motor unit activation.     

TVR and vibration-induced timing of motor impulses in the human jaw elevator muscles.

In order to investigate myotatic reflex involvement in jaw muscle control, an analysis was made of the motor responses induced by mechanical vibration (120-160 Hz) of the jaw elevator muscles in healthy subjects. As seen in torque measurements and mean-voltage electromyographic (EMG) recordings, the vibration caused involuntary reciprocal changes in jaw muscle tone, the contraction force increasing in jaw elevators and decreasing in antagonistic jaw opening muscles. This tonic vibration reflex (TVR) elicited from the jaw elevators exhibited many characteristics similar to those previously described for limb muscle tonic vibration reflexes: it varied in strength from one subject to the next independently of the briskness of the jaw elevator tendon jerks; it had a gradual onset with successive recruitment of jaw elevator motor units firing largely out of phase with one another and at rates much lower than the vibration frequency; it was susceptible to voluntary control--when allowed visual feed-back from the torque meter all subjects were able to suppress the TVR and keep mean contraction force constant. The results indicate that with respect to the tonic motor response to sustained inflow in the Ia afferent nerve fibres, the jaw elevators do not differ markedly from other skeletal muscles. Independently of whether a TVR was present or not, the vibration caused a timing of the motor unit discharges in the jaw elevators that could not be controlled voluntarily and that showed up in gross EMG recordings as a marked grouping of discharges synchronous with each wave of vibration. A similar but less distinct grouping of the gross EMG pattern was seen in limb muscles exposed to vibration, the dispersion increasing with the peripheral conduction distances of the reflex arcs. It is suggested that contrary to the TVR, which depends on the sustained mean level of the Ia afferent input, the timing phenomenon depends, like the tendon jerk, on the degree of synchrony in the afferent Ia volleys. Monosynaptic projections may well be involved in the dynamic timing of motor discharges during tonic firing, but this does not imply that the TVR or the tonic stretch reflex is dependent upon such projections.     

Changes of the average muscle fiber conduction velocity during a varying force contraction

The average conduction velocity of muscle fibers measured with a surface electrode has been reported to increase with the level of contraction force. To clarify the factors causing this increase, the authors decomposed the interference surface EMG signal into its constituent motor unit action potentials and compared the average conduction velocity with the conduction velocity measured at the individual discharges of motor units. The conduction velocity within individual motor units increased with the contraction force and contributed to the increase of the average conduction velocity. However, the increase of the conduction velocity within motor units was relatively small and was insufficient to cause the increase of the average conduction velocity. This result indicates that the motor units recruited at higher thresholds of force should have higher conduction velocities.     

Inhibitory phenomena in individual motor units induced by transcranial magnetic stimulation

It is well known that a silent period (SP) can be observed in voluntary tonic EMG activity starting directly after the initial early response when magnetic stimuli are delivered through the skull over the contralateral primary motor cortex. It is, however, unknown as to how an individual motoneurone (MN) contributes to the SP observed in the surface EMG. The present investigation was conducted to investigate inhibitory phenomena at the level of individual motor units. It demonstrates that the duration of the SP in single motor units is inhomogeneously distributed within the pool of active MNs. At various stimulation strengths, SP durations in single motor units can be similar or longer when compared to that observable in surface EMG records. In some motor units, which show low thresholds for early excitation and appearance of the SP, durations of SP can exceed 1000 msec. The length of suppression of spontaneous MN firing is maximal at stimulus intensities a little higher than those required for an early excitatory response. Although in general thresholds for early excitation and appearance of SPs are similar, at threshold stimulation in a number of trials inhibitory effects on the firing of voluntarily activated motoneurones were present, even in the absence of early excitations. This proves the independent nature of inhibitory as opposed to excitatory effects induced by transcranial magnetic stimulation. An SP in the absence of early excitation underlines its cortical origin. Inhibition and excitation of single MNs were maximal over the same small scalp area. We suggest that cortical inhibitory control plays an important role in the organization of natural movements.     

Reflex origin of parkinsonian tremor

The 8-Hz wrist tremor seen in normal subjects results from an oscillation in the spinal stretch reflex arc but the resting 4-Hz tremor of Parkinson's disease is believed to result from synchronization of motor unit activity by periodic descending inputs driven by an oscillator which resides within the brain. Accelerometer and smoothed EMG (0.8 to 16.0-Hz pass) recordings of resting tremor were taken from the upper limbs of 10 volunteers with Parkinson's disease for several different limb positions and while the limb was fixed to prevent tremor movements. The smoothed EMG and accelerometer records produced a complex periodic waveform with prominent 4- and 8-Hz components. Spectral analysis of both records produced large peaks at those frequencies which were harmonically related. The appearance of the regular tremor waveform in accelerometer and smoothed EMG records was greatly altered by changes in limb posture in all patients. Fixing of the shoulder and elbow joints only, also altered the smoothed EMG waveform and reduced the tremor amplitude. Fixing of the entire limb removed all signs of synchronization of motor unit activity in raw and smoothed EMG records. Similarly, the prominent 4- and 8-Hz peaks, found in the smoothed EMG power spectra from trembling muscles, were eliminated if the limb was effectively prevented from trembling. These experiments showed that the synchronization of motor unit activity at Parkinson's tremor frequency is wholly dependent on the oscillation in limb position and thus proprioceptive reflex activity. It is suggested that the known properties of the 4-Hz resting tremor of Parkinson's disease can be attributed to a flip-flop oscillation involving the mutually inhibitory connections between the spinal stretch reflexes of antagonist muscles. The supraspinal contribution to the tremor may thus be confined to an "aperiodic" descending facilitation of spinal reflex pathways.     

Recording characteristics of the surface EMG electrodes

Routine motor nerve conduction studies are conducted using surface EMG electrodes. Most techniques of estimating the number of motor units (MUs) are based on surface EMG recordings. Therefore, it is important to assess the uptake area of these electrodes. We recorded surface EMG motor unit action potentials (SMUAPs) from the biceps muscle of normal subjects. The SMUAP amplitude fell from 42 μV for the superficially located MUs (i.e., within 10 mm of skin surface) to 11 μV for the deep MUs (i.e., more than 20 mm from the skin surface). We infer that the pickup radius of the surface electrode is less than 20 mm. The implications of the limited uptake area of the surface electrodes to the analysis of compound muscle action potentials, estimation of the number of MUs, and the surface EMG recordings are discussed. © 1994 John Wiley & Sons, Inc.     

The evolving role of surface electromyography in amyotrophic lateral sclerosis: A systematic review

ObjectiveAmyotrophic lateral sclerosis (ALS) is an adult-onset neurodegenerative disease that leads to inexorable motor decline and a median survival of three years from symptom onset. Surface EMG represents a major technological advance that has been harnessed in the development of novel neurophysiological biomarkers. We have systematically reviewed the current application of surface EMG techniques in ALS.MethodsWe searched PubMed to identify 42 studies focusing on surface EMG and its associated analytical methods in the diagnosis, prognosis and monitoring of ALS patients.ResultsA wide variety of analytical techniques were identified, involving motor unit decomposition from high-density grids, motor unit number estimation and measurements of neuronal hyperexcitability or neuromuscular architecture. Some studies have proposed specific diagnostic and prognostic criteria however clinical calibration in large ALS cohorts is currently lacking. The most validated method to monitor disease is the motor unit number index (MUNIX), which has been implemented as an outcome measure in two ALS clinical trials.ConclusionSurface EMG offers significant practical and analytical flexibility compared to invasive techniques. To capitalise on this fully, emphasis must be placed upon the multi-disciplinary collaboration of clinicians, bioengineers, mathematicians and biostatisticians.SignificanceSurface EMG techniques can enrich effective biomarker development in ALS.     

The role of different EMG methods in evaluating myopathy.

For the diagnosis of myopathy, EMG may have an important role along with blood tests, muscle biopsies and genetic testing. This review evaluates different EMG methods in the diagnosis of myopathy. These include manual analysis of individual motor unit potentials and multi-motor unit potential analysis sampled at weak effort. At high effort, turns-amplitude analyses such as the cloud analysis and the peak ratio analysis have a high diagnostic yield. The EMG can seldom be used to differentiate between different types of myopathy. In the channelopathies, myotonia, exercise test and cooling of the muscle are helpful. Macro-EMG, single-fibre EMG and muscle fibre conduction velocity analysis have a limited role in myopathy, but provide information about the changes seen. Analysis of the firing rate of motor units, power spectrum analysis, as well as multichannel surface EMG may have diagnostic potential in the future. EMG is of great importance in the diagnosing of patients with myopathy, preferably a needle electrode and quantitative analyses should be used. A combination of a method at weak effort as well as a method at stronger effort seems optimal.     

Simulation of EMG in pathological situations.

OBJECTIVE: A mathematical model for simulation of the EMG from a muscle with its motor units is used. The study aims at correlating EMG findings (single-fiber EMG and concentric-needle EMG) with various induced morphological changes. METHODS: Reinnervation has been simulated by removing motor units randomly followed by a complete reinnervation from adjacent surviving motor units. Fibre type grouping and grouped atrophy can be seen. Myopathy is simulated by increased fibre diameter variation, loss of fibres and muscle fibre splitting. RESULTS AND CONCLUSION: The simulation gives quantitative aspects of the importance of each of these factors. It indicates the relative sensitivity of various EMG parameters. The model can be used both for education and for research.     

Twenty Years of Ictal EEG–EMG

Summary: This study aimed to evaluate the use of ictal EEG recordings combined with simultaneous surface EMG in the diagnosis and analysis of motor events, both epileptic and non-epileptic. All ictal registrations were performed utilizing radio/cable telemetry. Routine recordings consisted of 18-channel EEG plus 8-channels bipolar surface EMG in freely moving patients. Combined ictal EEG—EMG recordings in freely moving patients enabled us to identify and define the following pathomechanisms of epileptic drop seizures, epileptic axial spasms, atonic, myoclonic-atonic, and akinetic seizures. Precise differentiation could be made between tonic and nontonic postural seizures and between startle-induced reflex seizures and hyperekplexia. The findings from telemetered ictal recordings in freely moving patients with combined EEG and surface EMG offer the only means of identifying, defining, and differentiating motor events, both epileptic and nonepileptic, of a short duration that cannot be properly differentiated by clinical examination alone.     

Motoneuronal drive during human walking

Recent technical advances have made it possible to reveal some of the inputs that drive spinal motoneurones during normal human walking. These techniques are based either on a temporary removal of the drive to the motoneurones or on an analysis of the coupling of motor unit activity. During walking a sudden unloading of the plantarflexor muscles leads to a pronounced drop in the soleus EMG activity. This unloading effect is caused by cessation of activity in the sensory afferents, which mediate positive feedback from the active muscles in the stance phase. Somewhat surprisingly the drop in EMG activity following unloading is still observed when Ia afferents are blocked, suggesting that these afferents do not make an important contribution to the motoneuronal drive. It would seem that gr. Ib and/or gr. II afferents are the main contributors to the positive feedback. It has been known for a long time that transcranial magnetic stimulation (TMS) at low intensities may selectively activate local inhibitory circuits in the cortex. At such low intensities TMS applied over the motor cortex may thus inhibit the output from the cortex. The removal of the corticospinal drive in this way may be revealed as a drop in EMG activity from the active muscle. During walking TMS may evoke such a drop in EMG activity from the active muscles, which demonstrates that the corticospinal tract makes a contribution to the muscle activity. Time- and frequency domain analysis of motor unit activity have been shown to be effective tools in the analysis of synaptic drive to spinal motoneurones during tonic voluntary contraction. Applying these techniques to human walking reveals that motor units recorded from the same muscle or from close synergists show short-term synchrony and coherence in the 15–20 Hz frequency band. However, motor units from muscles acting at different joints show no coupling. This suggests that leg muscles are generally activated relatively independently of each other during human walking. These techniques show great promises for revealing changes in the sensory and corticospinal drive to motoneurones in relation to different tasks as well as in patients after injury to the central motor system.