Stimulation Principles and Techniques

Percutaneous (surface) stimulation of a peripheral nerve is the most widely used nerve conduction technique in clinical practice. The output impulse is a rectangular wave with a duration of 0.1 or 0.2 ms, although this may be increased up to 1 ms in order to record a maximal response. Two different types of percutaneous (surface) electric stimulators are used: both are bipolar having a cathode (negative pole) and anode (positive pole). The first type is a constant voltage stimulator that regulates voltage output so that current varies inversely with the impedance of the skin and subcutaneous tissues. The second type is a constant current stimulator that changes voltage according to impedance, so that the amount of current that reaches the nerve is specified within the limits of skin resistance. In bipolar stimulation, both electrodes are placed over the nerve trunk. As the current flows between the cathode and anode, negative charges accumulate under the cathode depolarizing the nerve, and positive charges gather under the anode hyperpolarizing the nerve.

With bipolar stimulation, the cathode should be, in most situations, closer to the recording site. If the cathode and anode of the stimulator are inadvertently reversed, anodal conduction block of the propagated impulse may occur. This is due to hyperpolarization at the anode that may prevent the depolarization that occurs under the cathode from proceeding past the anode. In situations where it is intended for the volley to travel proximally (such as with F wave or H reflex recordings), the bipolar stimulator is switched and the cathode is placed more proximally.

Supramaximal stimulation of nerves that results in depolarization of all the available axons is a paramount prerequisite to all NCS measurements. To achieve supramaximal stimulation, current (or voltage) intensity is slowly increased until it reaches a level where the recorded potential is at its maximum. Then, the current should be increased an additional 20–30% to ensure that the potential does not increase in size further (Figure 2-1). Stimulation via a needle electrode deeply inserted near a nerve is used less often in clinical practice. This is usually reserved for circumstances where surface stimulation is not possible, such as in deep-seated nerves (e.g., sciatic nerve or cervical root stimulation).

Figure 2-1 Supramaximal stimulation of a peripheral nerve during a motor nerve conduction study (median nerve stimulating at the wrist while recording abductor pollicis brevis). With a subthreshold stimulus of 3.6 mA (top response), none of the fibers were stimulated and no response was evoked. With a higher stimulus of 8.6 mA (second response), few fibers are stimulated and a low-amplitude compound muscle action potential (CMAP) is recorded. A further increase in the current to 12.4 mA (third response) reveals a larger CMAP that is still submaximal. A 17.4 mA stimulus results in a maximal CMAP (fourth response). This can only be confirmed after increasing the stimulus intensity by 20–25% (supramaximal stimulus of 22 mA, fifth response) and evoking a CMAP that is identical to the maximal CMAP. With maximal and supramaximal stimulations, all nerve fibers are stimulated.

Recording Electrodes and Techniques

Surface electrodes are most often used for nerve conduction recordings. Surface recording electrodes are often made as small discs that are placed over the belly of the muscle or the nerve (Figure 2-2). The advantages of surface recording are that the evoked response is reproducible and changes only slightly with the position of the recording electrode. Also, the size (amplitude and area) of the response is a semiquantitative measure of the number of axons conducting between the stimulating and recording electrodes.

Figure 2-2 Belly-tendon recording of compound muscle action potential. The settings are for peroneal motor conduction study recording the extensor digitorum brevis and stimulating distally at the ankle. Note that the active electrode (G1) is over the belly of the muscle while the reference electrode (G2) is over the tendon. The ground electrode is placed nearby.

With motor conduction studies, the active recording electrode is placed over the belly of the muscle that correlates with the endplate zone. This ensures that muscle activity at the moment of depolarization is recorded as soon as the nerve action potential has arrived at the endplate. Ring electrodes are convenient to record the antidromic sensory potentials from hand digital nerves over the proximal and distal interphalangeal joints (Figure 2-3). These ring electrodes could act as stimulation points with orthodromic recording from hand digits.

Figure 2-3 Ring electrodes used in recording sensory nerve action potential (SNAP). The settings are for antidromic median SNAP recording index finger.

Needle recording is also possible but is less popular and reserved for situations where the recording sites are deep-seated muscles or nerves. Needle recordings are also useful to improve the recording from small atrophic muscles or a proximal muscle not excitable in isolation. In contrast to surface recording, needle electrode recording registers only a small portion of the muscle or nerve action potentials and the amplitude of the evoked response is extremely variable and highly dependent on the exact location of the needle. Hence, amplitude and area measurement are not reproducible which renders this technique not clinically valuable such as in assessing conduction block or estimating the extent of axonal loss (see below).

Recording Settings and Filters

Filters are set in the recording equipment to reject low- and high-frequency electrical noise. Low-frequency (high-pass) filters exclude signals below a set frequency, while high-frequency (low-pass) filters exclude signals above a certain frequency. Filtering results in some loss or alteration of the signal of interest. For instance, as the low-frequency filter is reduced, more low-frequency signals pass through, and the duration of the recorded potential increases slightly. Likewise, as the high-frequency filter is lowered, more high-frequency signals are excluded, and the amplitude of the recorded potential usually decreases. Hence, all potentials should be obtained with standardized filter settings, and only compared to normal values collected using the same filter settings. The recommended low and high filter settings for motor conduction studies are 10 Hz and 10 kHz, respectively. The high-frequency filter is set lower for sensory nerve conduction studies than for motor nerve conduction since high-frequency noise (>10 kHz) commonly obscures high-frequency sensory potentials. For sensory conduction studies, the low- and high-frequency filters settings are typically 20 Hz and 2 kHz.

The amplifier sensitivity determines the amplitude of the potential. Overamplification of the response truncates the response, which results in false measurements of evoked response amplitude and area, while underamplification prevents accurate measurements of the takeoff point from baseline. Typically, sensory studies are recorded with a sensitivity of 10–20 μV/division and motor studies with a sensitivity of 2–5 mV/division.

Recording Procedure

A prepulse preceding the stimulus triggers the sweep on a storage oscilloscope. A stimulus artifact occurs at the beginning of the sweep, and serves as an indicator of the time when the shock occurred from which point latencies are measured. Digital averaging is a major improvement in recording low-amplitude responses by eliminating artifacts and noise. Signals time-locked to the stimulus summate at a constant latency and appear as an evoked potential, distinct from the background noise. The signal-to-noise ratio increases in proportion to the square root of the trial number. For example, four trials give twice as big a response as a single stimulus, whereas nine trials give three times the amplitude. Modern instruments digitally indicate the latency and amplitude when the desired spot on the waveform is marked.

Sensory Nerve Conduction Studies

Sensory NCSs are performed by stimulating a nerve while recording the transmitted potential from the same nerve at a different site. Hence, SNAPs are true nerve action potentials. Antidromic sensory NCSs are performed by recording potentials directed toward the sensory receptors while orthodromic studies are obtained by recording potentials directed away from these receptors. Sensory latencies and conduction velocities are identical with either method, but SNAP amplitudes are higher in antidromic studies and, hence, more easily obtained without the need for averaging techniques. Since the thresholds of some motor axons are similar to those of large myelinated sensory axons, superimposition of muscle action potentials may obscure the recorded antidromic SNAPs. These volume-conducted muscle potentials often occur with mixed nerve stimulation or may result from direct muscle co-stimulations. Fortunately, SNAPs can still be measured accurately in most cases because the large-diameter sensory fibers conduct 5–10% faster than motor fibers. This relationship may change in disease states that selectively affect different fibers. In contrast to the antidromic studies, the orthodromic responses are small in amplitude, more difficult to obtain, and might require averaging techniques (Figure 2-4).

Figure 2-4 Antidromic and orthodromic median sensory nerve action potentials. The response in (A) is antidromic, i.e., stimulating the wrist and recording the index finger. The response in (B) is orthodromic, i.e., stimulating the index and recording at the wrist. Note that the peak latencies are comparable while the antidromic response is much larger in amplitude than its orthodromic counterpart.

SNAPs may be obtained by (1) stimulating and recording a pure sensory nerve (such as the sural and radial sensory responses), (2) stimulating a mixed nerve while recording distally over a cutaneous branch (such as the antidromic median and ulnar sensory responses), or (3) stimulating a distal cutaneous branch while recording over a proximal mixed nerve (such as the orthodromic median and ulnar sensory studies). The active recording electrode (G1) is placed over the nerve and the reference electrode (G2) is positioned slightly more distal with antidromic recordings or slightly more proximal with orthodromic techniques. The distance between G1 and G2 electrodes should be fixed (usually at about 3–4 cm), since it has a significant effect on SNAP amplitude. The SNAP is usually triphasic with an initial small positive phase, followed by a large negative phase and a positive phase. Several measurements may be recorded with sensory NCSs (Figure 2-5):

Figure 2-5 Antidromic median sensory nerve action potential stimulating wrist while recording middle finger revealing commonly measured parameters including a shock (stimulation) artifact.

Sensory conduction velocity may also be calculated after a distal and a proximal stimulation and measurement. For example, the median sensory SNAPs are obtained at the wrist and elbows and the conduction velocity is measured as follows:

Motor Nerve Conduction Studies

Motor NCS is performed by stimulating a motor or mixed peripheral nerve while recording the CMAP from a muscle innervated by that nerve. The CMAP is the summated recording of synchronously activated muscle action potentials. The advantage of this technique is a magnification effect based on motor unit principles: Stimulation of each motor axon results in up to several hundred muscle action potentials with this number depending on the innervation ratio (number of muscle fibers per axon) of the examined muscle.

A belly-tendon recording is a typical electrode placement to obtain a CMAP: a pair of recording electrodes are used with an active lead (G1) placed on the belly of the muscle and a reference lead (G2) on the tendon (see Figure 2-2). Both active and reference electrodes locations are an essential determinant of the CMAP size, shape, and latency. The propagating muscle action potential, originating near the motor point and under G1, gives rise to a simple biphasic waveform with an initial large negative phase followed by a smaller positive phase. With incorrect positioning of the active electrode away from the endplate, the CMAP will show an initial positive phase that corresponds to the approaching electrical field of the impulses from muscle fibers toward the electrode. Similar initial positivity is also recorded with a volume-conducted potential from distant muscles activated by anomalous innervation or by accidental spread of stimulation to other nerves.

Whenever possible, the nerve is stimulated at two or more points along its course. Typically, it is stimulated distally near the recording electrode and more proximally to evaluate its proximal segment. Several measurements are evaluated with motor NCSs (Figure 2-6):

5. Conduction velocity. This is a computed measurement of the speed of conduction and is expressed in meters per second (m/s). Measurement of conduction velocity allows the comparison of the speed of conduction between different nerves and subjects, irrespective of the length of the nerve and the exact sites of stimulations. Also, motor conduction velocity reflects the pure speed of the largest motor axon and, in contrast to distal and proximal latencies, does not include any neuromuscular transmission time nor propagation time along the muscle membrane. Motor conduction velocity is calculated after incorporating the length of the nerve segment between distal and proximal stimulation sites. The nerve length is estimated by measuring the surface distance along the course of the nerve and should be more than 10 cm to improve the accuracy of surface measurement. Motor conduction velocity is calculated as follows:

Figure 2-6 Median motor nerve conduction study revealing commonly measured parameters following distal (top) and proximal (bottom) stimulations.

Mixed Nerve Conduction Studies

Mixed NCSs are done by stimulating and recording from nerve trunks with sensory and motor axons. Often, these tests are done by stimulating a nerve trunk distally and recording more proximally, since the reverse is often contaminated by large CMAP that obscures the relatively low-amplitude MNAPs. In situations where the nerve is deep (such as the elbow or knee), the MNAP may be very low in amplitude or unelicitable, due to considerable tissue interposing between the nerve and recording electrode. Hence, these studies are not popular in clinical practice and are restricted to evaluating mixed nerves in distal nerve segments, such as in the hand or foot during the evaluation of carpal tunnel syndrome and tarsal tunnel syndrome, respectively (Figure 2-7).

Figure 2-7 Mixed nerve action potential. This is a median palmar response stimulating the mixed median nerve in the palm and recording orthodromically the median nerve at the wrist.

Segmental Stimulation in Short Increments

Routine NCSs are often sufficient to localize the site of lesion in entrapment neuropathies. However, during the evaluation of a focal nerve lesion, inclusion of the unaffected segments in conduction velocity calculation dilutes the effect of slowing at the injured site and decreases the sensitivity of the test. Therefore, incremental stimulation across the shorter segment helps localize an abnormality that might otherwise escape detection. More precise localization requires moving the stimulus in short increments along the course of the nerve while keeping the recoding site constant. This procedure is often labeled inching (or actually centimetering) since 1 cm increment is a common distance measurement. The large per-step increase in latency more than compensates for the inherent measurement error associated with stimulating multiple times in short increments. The analysis of the waveform usually focuses on sudden changes in latency values or abrupt drop in amplitude.

The inching technique is particularly useful in assessing patients with carpal tunnel syndrome, ulnar neuropathies at the elbow or wrist, or peroneal neuropathy at the fibular neck. For example, with stimulation of a normal median nerve in 1 cm increments across the wrist, the latency changes approximately 0.16–0.21 ms per cm from midpalm to distal forearm. A sharply localized latency increase across a 1 cm segment indicates a focal abnormality of the median nerve.

Physiologic Variabilities

Temperature. Nerve impulses propagate slower by 2.4 m/s or approximately 5% per degree Celsius as the limb cools from 38 to 29°C. Also, cooling results in a higher CMAP and SNAP amplitude and longer duration probably because of accelerated and slowed Na⁺ channel inactivation. Hence, a CMAP or SNAP with high amplitude and slow distal latency or conduction velocity should be highly suspicious of a cool limb (Figure 2-8).

Figure 2-8 The effect of temperature on antidromic median sensory nerve action potential stimulating at the wrist and recording the index finger. Response obtained with a skin palm temperature of (A) 33.5∞C and (B) 29.5∞C. Note that cool limb results in a SNAP with slower onset and peak latencies and higher amplitude.

To reduce this type of variability, skin temperature is measured with a plate thermistor that correlates linearly with the subcutaneous and intramuscular temperatures. If the skin temperature falls below 33 to 34°C, it is necessary to warm the limbs by immersion in warm water. Warming packs or a hydroculator can also be used, particularly in bedridden or intensive care unit patients. Adding 5% of the calculated conduction velocity for each degree below 33°C theoretically normalizes the result. However, such conversion factors are based on experience with healthy individuals and do not apply to patients with abnormal nerves.

Age. Nerve conduction velocities are slow at birth since myelination is incomplete. They are roughly one-half the adult value in full-term newborns and one-third that of term newborns in 23- to 24-week premature newborns. They reach adult values at 3–5 years. Then, motor and sensory nerve conduction velocities tend to slightly increase in the arms and decrease in the legs during childhood up to 19 years. With aging, conduction velocities slowly decline after 30–40 years of age, that the mean conduction velocity is reduced about 10% at 60 years of age.

Aging also causes a diminution in SNAP and CMAP amplitudes, which decline slowly after the age of 60 years. This affects SNAP amplitudes more prominently, that normal upper limb SNAP amplitude drops up to 50% by age 70, and lower limb SNAPs in healthy subjects above the age of 60 years are low in amplitude or unevokable. Hence, absent lower extremity SNAPs in the elderly must always be interpreted with caution, and are not necessarily considered abnormal without other confirmatory data.

Height and nerve segments. An inverse relationship between height and nerve conduction velocity suggests that longer nerves generally conduct slower than shorter nerves. For example, the nerve conduction velocities of the peroneal and tibial nerves are 7–10 m/s slower than the median and ulnar nerves. This cannot be explained entirely by the small reduction in temperature of the legs as compared with the arms. Possible factors to account for the length-related slowing include abrupt distal axonal tapering, progressive reduction in axonal diameter, or shorter internodal distances. For similar reasons, nerve impulses propagate faster in proximal than in distal nerve segments. Hence, adjustments of normal values must be made for individuals of extreme height, which is usually no more than 2–4 m/s below the lower limit of normal.

Anomalies. Anomalous peripheral innervations may mislead the electrodiagnostic physician and occasionally lead to erroneous diagnosis and treatment. There are several anomalous peripheral innervations that are important to recognize since they have a significant effect on NCS.

Figure 2-9 Martin-Gruber anastomosis with evidence of prominent median to ulnar anastomosis recording hypothenar muscle (ADM). The figure shows an ulnar motor conduction study recording hypothenar muscle (ADM), stimulating the ulnar nerve at the wrist (A), below elbow (B) and above elbow (C). It also reveals the response following stimulating the median nerve at the wrist (D) and the elbow (E).

Figure 2-10 Martin-Gruber anastomosis with evidence of prominent median to ulnar anastomosis recording first dorsal interosseous muscle. The figure shows an ulnar motor conduction study recording first dorsal interosseous muscle, stimulating the ulnar nerve at the wrist (A), below elbow (B) and above elbow (C). It also reveals the response following stimulating the median nerve at the wrist (D) and the elbow (E).

Figure 2-11 Martin-Gruber anastomosis with evidence of median to ulnar anastomosis recording thenar muscle in a patient with moderate carpal tunnel syndrome. The figure shows a median motor conduction study recording abductor pollicis brevis (A, distal; B, proximal). Note the slowing of the distal latency (7.1 ms, N < 4.0 ms) which is compatible with carpal tunnel syndrome. There is a spuriously rapid conduction velocity with a larger proximal thenar CMAP exhibiting a positive dip (arrow).

Figure 2-12 Accessory deep peroneal nerve anomaly shown while performing a peroneal motor conduction study recording extensor digitorum brevis. The distal stimulation at the ankle (A) results in a CMAP that was lower in amplitude that the proximal response following knee stimulation (B). Stimulation behind the lateral malleolus yielded a CMAP (C). Note that the summation of the CMAPs at (A) and (C) were higher than the CMAP at (B).

Figure 2-13 Prominent accessory deep peroneal nerve anomaly. Note here that the distal CMAP was extremely low in amplitude (A) while the proximal CMAP is higher (B). Similar to Figure 2-12, stimulation behind the lateral malleolus yielded a relatively large CMAP (C). However, in this example, most fibers were directed to the extensor digitorum brevis through the accessory deep peroneal nerve, leaving only a few to travel through the main trunk of the deep peroneal nerve.

Temporal dispersion and phase cancellation. The CMAP, evoked by supramaximal stimulation, represents the summation of all individual muscle action potentials directed to the muscle through the stimulated nerve. Typically, as the stimulus site moves proximally, the CMAPs slightly drop in amplitude and area and increase in duration. This is caused by temporal dispersion where the velocity of impulses in slow-conducting fibers lags increasingly behind those of fast-conducting fibers as conduction distance increases. With dispersion, there is also a slight positive/negative phase overlap and cancellation of MUAP waveforms. The final result of temporal dispersion and phase cancellation is a reduction of CMAP amplitude and area and prolongation of its duration.

Physiological temporal dispersion affects the SNAP more than the CMAP. This is related to two factors. First is the disparity between sensory fiber and motor fiber conduction velocities. The range of conduction velocities between the fastest and slowest individual human myelinated sensory axons is almost double that of the motor axons (25 m/s versus 12 m/s). This results in more dispersion of individual action potentials and leads to more prominent phase cancellation. The second factor is the difference in duration of individual unit discharges between nerve and muscle. With short-duration biphasic sensory spikes, a slight latency difference could line up the positive peaks of the fast fibers with the negative peaks of the slow fibers and cancel both. In longer duration motor unit potentials, the same latency shift would only partially superimpose peaks of opposite polarity, and cancellation would be less of a factor (Figures 2-14 and 2-15).

Figure 2-14 Temporal dispersion and phase cancellation of two surface-recorded motor unit potentials at distal and proximal sites. This can be translated into many similar biphasic potentials, which contribute to the compound muscle action potential (CMAP).

(Reproduced from Kimura J et al. Relation between size of compound sensory or muscle action potentials, and length of nerve segment. Neurology 1986;36:647–652, with permission.)

Figure 2-15 Temporal dispersion and phase cancellation of two surface-recorded single-fiber sensory potentials at distal and proximal sites. This can be translated into many similar biphasic potentials, which contribute to the sensory nerve action potential (SNAP).

(Reproduced from Kimura J et al. Relation between size of compound sensory or muscle action potentials, and length of nerve segment. Neurology 1986;36:647–652, with permission.)

Intertrial variability. Principal factors contributing to an intertrial variability include errors in determining surface distance and in measuring latencies and amplitudes of the recorded response. A slight shift in recording site results in significant amplitude variability. NCSs are more reproducible when done by the same examiner, because of the significant degree of inter-examiner variability.

Common Sources of Error

Several major pitfalls in NCS may result in erroneous measurements, calculations, and conclusions. These are usually due to technical errors related to a large obscuring stimulus artifact, increased background electrical noise, submaximal stimulations at distal or proximal sites or both, spread of the stimulating current to a nerve not under study, eliciting an unwanted potential from distant muscles, misplacement of recording or reference electrodes, or errors in the measurement of nerve length and conduction time.

Motor Units and Muscle Fibers

The motor unit consists of a single motor neuron and all the muscle fibers it innervates. The number of muscle fibers innervated by a single motor axon is the innervation ratio, which is variable ranging from 3 to 1 for extrinsic eye muscles to several hundreds to 1 for limb muscles. A low ratio occurs in muscles with greater ability for fine gradations of movement, and is typically found in the extraocular, facial, and hand muscles.

Muscle fibers are classified based on their mechanical properties and resistance to fatigue. Based on the speed of the actin–myosin reaction and the Ca²⁺-dependent activation and relaxation regulatory systems, muscle fibers are either slow or fast. They are also either fatigue-resistant with higher mitochondrial content, or fatigable. Hence, muscle fibers are usually labeled as type I (slow and fatigue-resistant), type II A (fast and fatigue-resistant), or type II B (fast and fatigable) fibers (Table 2-1). All muscle fibers of each individual motor unit are of one specific type. The distribution of muscle fibers of a single motor unit within a muscle is wide with considerable overlap among the territories of motor units.

All muscle fibers in one motor unit discharge simultaneously when stimulated by synaptic input to the lower motor neuron or by electrical stimulation of the axon. Based on the “size principle,” the smallest motor neurons are activated first with larger motor neurons recruited later with progressive increase in force. This order of recruitment correlates with the functional properties of the motor units, i.e., the small motor units are slow and fatigue-resistant and are activated first and for longer periods of time than the large motor units that are fast and fatigable and recruited later and for shorter periods of time.

Principles

The skeletal muscle fiber has a resting potential of 90 mV, with negativity inside the cell. These fibers, as well as neurons and other excitable cells, generate action potentials when the potential difference across the plasma membrane is depolarized past a specific threshold. This follows an “all-or-none” rule, which means that increasing the stimulus does not change the shape of the action potential. The generation of an action potential reverses the transmembrane potential, which then becomes positive inside the cell. An extracellular electrode, as used in needle EMG, records the activity resulting from this switch of polarity as a predominantly negative potential (usually triphasic, positive–negative–positive waveforms). However, when recording near a damaged region, action potentials consist of a large positivity followed by a small negativity.

The needle EMG study is an essential component of the EDX evaluation. It provides an efficient and rapid mean of testing the electrical activity of motor units in a widespread number of muscles. The selection of muscle to be sampled is based on the working and differential diagnoses as determined by the clinical manifestations and NCS findings. The accessibility of the muscle, the ability to activate it, and the degree of pain associated with needle insertion particularly in children and anxious adults also play a role in that choice.

Concentric and Teflon-coated monopolar needle electrodes are equally satisfactory in recording muscle potentials, with few appreciable differences (Table 2-2). Though monopolar needles are less painful, they require an additional reference electrode nearby which often results in greater electrical noise due to electrode impedance mismatch between the intramuscular active electrode and the surface reference disk.

Table 2-2 Difference Between Monopolar and Concentric Needle Electrodes

Techniques

Knowledge of the anatomy of muscles is a prerequisite for needle EMG. This includes their exact location, segmental and peripheral innervations, and activation maneuvers. The electromyographer first identifies the needle insertion point by recognizing the proper anatomical landmark of the sampled muscle. The initial insertion of the needle electrode should occur when the muscle is relaxed and not contracted since this is less painful. Needle EMG evaluation is performed in three steps:

Oscilloscope sweep speeds of 10 ms per division bests define spontaneous and voluntary activities. A 50 μV/division sensitivity is the usual amplification for the evaluation of insertional and spontaneous activities, while 200 μV/division is used for analysis of voluntary motor activity.

Insertional and Spontaneous Activity

Normal Insertional and Spontaneous Activity

Brief bursts of electrical discharges accompany insertion and repositioning of a needle electrode into the muscle, slightly outlasting the movement of the needle, and usually not lasting more than 300 ms. Insertional activity appears as a cluster of positive or negative repetitive high-frequency spikes, which make a crisp static sound over the loudspeaker.

At rest, muscle is silent. It is, however, noisy in the motor endplate region (the site of neuromuscular junctions), which is usually located near the center of the muscle belly. Two types of normal endplate spontaneous activity occur together or independently: endplate spikes and endplate noise.

Endplate spikes. These are intermittent spikes and represent discharges of individual muscle fibers generated by activation of intramuscular nerve terminals irritated by the needle. Their characteristic irregular firing pattern distinguishes them from the regular-firing fibrillation potentials (Figure 2-16). The waveform of endplate spike is also distinguished by its initial negative deflection since the generator of the potential is usually underneath the needle’s tip. Endplate spikes fire irregularly at 5–50 impulses per second, and measures 100–200 μV in amplitude, and 3–4 ms in duration. They have a cracking sound on the loudspeaker, imitating “sputtering fat in a frying pan.”

Figure 2-16 Endplate spikes. Note the irregular firing pattern and the biphasic morphology with an initial negative deflection that separates this from the brief spike form of fibrillation potentials. (Compare the waveforms in this figure with those in Figure 2-18.)

Endplate noise. The tip of the needle approaching the endplate region frequently registers recurring irregular negative potentials, 10–50 μV in amplitude and 1–2 ms in duration (Figure 2-17). These potentials are the extracellularly recorded miniature endplate potentials that, in turn, are nonpropagating depolarizations caused by spontaneous release of acetylcholine quanta. Endplate potentials produce a characteristic sound on loudspeaker much like a “seashell held to the ear.”

Figure 2-17 Endplate noise. Note the low-amplitude, high-frequency and predominantly negative potentials (A). These may be seen in conjunction with the endplate spikes (B).

Abnormal Spontaneous Activity

Fibrillation potentials. Fibrillation potentials are spontaneous action potentials generated by recently denervated muscle fibers. They often are triggered by needle insertion and persist more than 3 seconds after the needle movement stops. Fibrillation potentials typically fire in a regular pattern at a rate of 1–30 impulses per second. They produce a sound reminiscent of the sound caused by “rain on the roof” or “the tick/tock of a clock.” They consist of one of two types of waveforms with distinctive morphologies (positive waves and brief spikes), which likely reflect the relation between the position of the needle electrode and the muscle fiber.

1. Positive waves have an initial positivity and subsequent slow negativity with a characteristic sawtooth appearance (Figure 2-18). It is likely that the needle mechanically deforms the muscle fiber, and the action potential that move toward the damaged part of the muscle fiber is incapable of propagate further. This accounts for the positive wave morphology and absence of negative spike.

2. Brief spikes are usually triphasic with initial positivity (Figure 2-19). They range from 1 to 5 ms in duration and are 20–200 μV in amplitude when recorded with a concentric needle electrode. If the needle electrode is placed near the endplate zone, brief spikes fibrillation potentials may resemble physiologic endplate spikes with an initial negativity. Although often seen together, positive sharp waves tend to precede brief spikes after nerve injury, possibly because they can be triggered by the insertion of a needle in already irritable muscle membrane.

Figure 2-18 A positive waveform of fibrillation potentials shown in raster form. Note that the discharge frequency is quite regular but decreases slightly and steadily starting the third trace.

Figure 2-19 A brief spike form of fibrillation potential shown in raster form. Note that the discharge is brief in duration, triphasic with an initial positivity and a regular rate.

Fibrillation potentials are seen following muscle denervation that occurs with motor axon loss lesions to the anterior horn cells of the spinal cord, root, plexus, or peripheral nerve. Fibrillation potentials appear after 1–2 weeks of acute denervation but do not become full till after 3 weeks after nerve injury. They disappear late in the course of denervation when muscle fibers become reinnervated or fibrotic and severely atrophied. Hence, fibrillation potentials may be absent in very acute or chronic denervation.

Fibrillation potentials are also commonly encountered in necrotizing myopathies, such as the inflammatory myopathies, critical illness myopathies and muscular dystrophies. This is likely due to segmental necrosis of muscle fibers, leading to effective denervation of the distant segments as they become physically separated from the neuromuscular junction. Also, damage to the terminal intramuscular motor axons, presumably by the inflammatory process, may also result in muscle fiber denervation. In disorders of the neuromuscular junction such as myasthenia gravis or botulism, fibrillation potentials are rare. They are best explained by a chronic neuromuscular transmission blockade, resulting in “effective” denervation of muscle fibers.

Fibrillation potentials are graded from 0 to +4 as follows: 0, no fibrillation potentials; +1 persistent single trains of potentials (>2–3 seconds) in at least two areas; +2, moderate number of potentials in three or more areas; +3, many potentials in all areas; +4, abundant spontaneous potentials nearly filling the oscilloscope. This conventional grading is semiquantitative since the density of fibrillation potentials represents only a rough estimate of the extent of denervated muscle fibers.

Fasciculation potentials. Fasciculation potentials are spontaneous (involuntary) discharges of a motor unit. They originate from the anterior horn cell or motor axon anywhere along its length. Fasciculation potentials fire randomly and irregularly, with variable waveform morphology, and much slower firing rate than voluntary MUAPs. They may be associated with a visible muscle twitch and, rarely, in slight movement of a small joint in the fingers of toes. When abundant, fasciculation potentials give a “popping corn” sound on the loudspeaker.

Fasciculation potentials are encountered most commonly in motor neuron diseases, but are seen also in radiculopathies, entrapment neuropathies, peripheral polyneuropathies, and the cramp-fasciculation syndrome. They are seen also in tetany, thyrotoxicosis, and overdose of anticholinesterase medication. In addition, they may occur in healthy individuals, and there is no reliable method of distinguishing “benign” from “malignant” fasciculation potentials except that the fasciculation potentials in motor neuron disease tend to fire slower, are more complex, and less stable. Most importantly, benign fasciculation potentials are not associated clinically with weakness and wasting, or with other electrophysiologic signs of denervation including fibrillation potentials and neurogenic MUAP changes (Figure 2-20).

Figure 2-20 Fasciculation potentials recorded, in raster mode, from the vastus lateralis in a patient with motor neuron disease. In (A) the sweep speed is set at 20 ms/division while in (B) it is set at a long sweep speed of 200 ms/division. Note that the morphology of the potentials is of motor units but with extreme variability in configuration among the individual discharges and their irregular firing pattern. Individual fasciculation potential may recur irregularly (arrows and arrowheads in (A)).

Complex repetitive discharges. A complex repetitive discharge is often referred to as CRD and was formerly known as bizarre repetitive discharge. It is a composite waveform that contains several distinct spikes and often fires at a constant and fast rate of 30 to 50 Hz. Occasionally, the discharge frequency is slow or extremely fast, ranging from 5 to 100 Hz. The individual CRD ranges from 50 μV to 1 mV in amplitude and up to 50–100 ms in duration. It remains uniform from one discharge to another, a feature that helps distinguishing it from myokymic discharge (Figure 2-21). CRDs typically begin and cease abruptly. On loudspeaker, CRD produces a noise that mimics the sound of a “machine.” Pathophysiologically, CRD results from the near synchronous firing of a group of muscle fibers that communicates ephaptically. One fiber in the complex serves as a pacemaker, driving one or several other fibers so that the individual spikes within the complex fire in the same order as the discharge recurs. One of the late-activated fibers re-excites the principal pacemaker to repeat the cycle. The chain reaction eventually blocks resulting in abrupt cessation. CRDs are abnormal discharges but rather nonspecific since they accompany a variety of chronic neurogenic as well myopathic disorders. They may also be found in the iliopsoas or cervical parapsinal muscles of apparently healthy individuals, probably implying a clinically silent neuropathic process.

Figure 2-21 Complex repetitive discharge recorded from the deltoid muscle in a patient with chronic C6 radiculopathy. Note that the complex (circled) is stable and remains exactly the same between discharges with a constant firing rate. In (A) the discharge is shown as a triggered rastered form and in (B) the five rasters are superimposed. Note that the complex superimposes perfectly reflecting its uniform configuration.

Myokymic discharges. Myokymic discharge is defined as groups of motor unit potentials that fire repetitively in a quasi-rhythmical fashion with intervening period of silence. The burst composed of about 2–15 spikes with frequent variability in the number of spikes per discharge (Figure 2-22). The intraburst frequency is about 30–40 Hz, while the interburst frequency is much slower and ranges from 1 to 5 Hz, which gives myokymia the sound of “marching soldiers” on the loudspeaker. Clinically, myokymic discharges often give rise to sustained muscle contractions, which have an undulating appearance beneath the skin (bag of worms). Myokymic discharges probably originate ectopically in motor fibers and decrease in intensity with progressively distal nerve blocks. They may be amplified by increased axonal excitability, such as after hyperventilation-induced hypocapnia.

Figure 2-22 Myokymic discharge shown in a raster mode with a long sweep speed of 200 ms/division. Note that the number of potentials often changes from one burst to another, varying in this example from one to four potentials. Note also the relatively slow interburst frequency of about 2 Hz while the intraburst frequency is about 18–20 Hz.

Myokymic discharges may be restricted to focal areas such as the in face with brainstem glioma or multiple sclerosis, a single extremity with radiation plexopathy, or the thenar eminence with carpal tunnel syndrome. They also may be generalized as encountered in association with gold toxicity or the syndrome of continuous motor unit activity (Isaac syndrome) (Table 2-3).

Table 2-3 Causes of Myokymic Discharges

Focal
Facial	Limb	Generalized
Multiple sclerosis Brainstem tumors Syringobulbia Bell’s palsy Guillain-Barré syndrome Basilar invagination Cerebellopontine angle tumor Cardiac arrest Hydrocephalus Lymphocytic meningitis

Radiation plexopathy (brachial or lumbosacral)

Carpal tunnel syndrome

Ulnar neuropathy

Chronic radiculopathy

Spinal stenosis

Guillain-Barré syndrome

CIDP^*

HNPP^†

Thyrotoxicosis

Thymoma

Guillain-Barré syndrome

Gold intoxication

Penicillamine

Timber rattlesnake poisoning

* CIDP = chronic inflammatory demyelinating polyneuropathy.

† HNPP = hereditary neuropathy with liability to pressure palsy (tomaculous neuropathy).

Neuromyotonic discharges. Neuromyotonic discharges are extremely rare discharges in which motor units fire repetitively at high frequency (150–250 Hz), either continuously or in recurring decrementing bursts, producing a “pinging sound” on loudspeaker (Figure 2-23). The discharge continues during sleep, and diminishes in intensity with progressively distal nerve blocks, implicating the entire axon as the site of generation. The syndrome of continuous motor unit activity (Isaac syndrome) which may have an autoimmune etiology, with the target antigen likely being peripheral nerve potassium channels, is often associated with neuromyotonia and myokymia. Other conditions associated with neuromyotonia include anticholinesterase poisoning, tetany, and chronic spinal muscular atrophies.

Figure 2-23 Neuromyotonic discharge. Note the decrementing response. The top is recorded with a long sweep speed of 100 ms/division while the insert is at a regular sweep speed of 10 ms/division. Note the very high frequency (150–250 Hz) repetitive discharge of a single motor unit.

(Reproduced from Preston DC, Shapiro BE. Electromyography and neuromuscular disorders. Boston, MA: Butterworth-Heinemann, 1998, with permission.)

Myotonic discharges. Like fibrillation potentials, myotonic discharges appear either as a sustained run of sharp positive waves or brief spikes (Figure 2-24). Positive sharp waves are initiated by needle insertion injuring muscle membrane, whereas the brief spikes tend to occur at the beginning of slight volitional contraction. Both types of discharges typically wax and wane in amplitude (range = 10 μV–1 mV), and frequency (range = 20–150 Hz), which gives rise to a characteristic noise over the loudspeaker, simulating a “dive-bomber” or an “accelerating–decelerating motorcycle or chain saw.”

Figure 2-24 Myotonic discharge recorded with a sweep speed of 100 ms/division. The arrow depicts the time of needle insertion that triggers the discharge from a muscle fiber. Note the waxing and waning of both amplitude and frequency.

(Reproduced from Preston DC, Shapiro BE. Electromyography and neuromuscular disorders. Boston, MA: Butterworth-Heinemann, 1998, with permission.)

Myotonic discharges may occur with or without clinical myotonia in the myotonic dystrophies, myotonia congenital, and paramyotonia congenita. They may also accompany acid maltase deficiency, colchicine myopathy, myotubular myopathy, and hyperkalemic periodic paralysis (Table 2-4).

Table 2-4 Common Causes of Electrical Myotonia

Motor Unit Action Potential Morphology

The motor unit action potential (MUAP) is the sum of the extracellular potentials of muscle fiber action potentials of a motor unit. The waveform is dictated by the inherent properties of the motor unit and the spatial relationships between the needle and individual muscle fibers. The extracellularly recorded MUAP, recorded along the length of the muscle fibers and away from the endplate region, has a triphasic waveform (Figure 2-25). The initial positive deflection represents the action potential propagating towards the electrode. As the potential passes in front of the electrode the main positive–negative deflection is recorded. When the action potential propagates away from the electrode the potential returns to the baseline. Slight repositioning of the electrode causes major changes in the electrical profile of the same motor unit. Therefore, one motor unit can give rise to MUAPs of different morphology at different recording sites. If the electrode is placed immediately over the endplate area, the initial positive defection will not be recorded and the potential will have a biphasic waveform with an initial negative deflection.

Figure 2-25 Relative average durations and amplitudes of some MUAPs seen in myopathic and neurogenic disorders.

(Reproduced from Daube J. Needle electromyography in clinical electromyography. Muscle Nerve 1991;14:685–700, with permission.)

Amplitude. MUAP amplitude is the maximum peak-to-peak amplitude and ranges from several hundred microvolts to a few millivolts with a concentric needle, and is substantially greater with a monopolar needle. At a short distance between the recording electrode and the potential generators (muscle fibers), the MUAP has a short rise time and high amplitude with a “crisp” or “sharp” sound on the loudspeaker. In contrast, the MUAP recorded from distant muscle fibers has a long rise time and a low amplitude that sounds “dull” or “muffled” on the loudspeaker. For example, the MUAP amplitude decreases to less than 50% at a distance of 200–300 μm from the source and to less than 1% a few millimeters away. Therefore, only a small number of individual muscle fibers located near the tip of the recording electrode determine the amplitude of an MUAP (probably less than 20 muscle fibers lying within a 1 mm radius of the electrode tip). In general, amplitude indicates muscle fiber density and not the motor unit territory. High MUAP amplitude, when isolated, is considered a nonspecific abnormality except when it is significantly increased (more than twice the upper normal limit); then, it indicates a neurogenic process.

Duration. MUAP duration reflects the electrical activity generated from most muscle fibers belonging to a motor unit. Muscle potentials generated more than 1 mm away from the electrode contribute to the initial and terminal low-amplitude portions of the potential. The duration also indicates the degree of synchrony among many individual muscle fibers with variable length, conduction velocity, and membrane excitability. MUAP duration is a good index of the motor unit territory and is the parameter that best reflects the number of muscle fibers within a motor unit. A shift in needle position has much less effect on MUAP duration than amplitude. The duration is measured from the initial deflection away from baseline to the final return to baseline, and normally varies from 5 to 15 ms, depending on the sampled muscle and the age of the subject. In normal subjects, large muscles tend to have long-duration MUAPs and MUAP duration increases with age after the sixth decade.

Long-duration MUAPs are the best indicators of reinnervation. They occur with increased number or density of muscle fibers, or a loss of synchrony of fiber firing within a motor unit as seen with lower motor neuron disorders. These MUAPs may also show high amplitude (see Figure 2-25). In contrast, short-duration MUAPs often have low amplitude and are indicators of muscle fiber loss as seen with necrotizing myopathies.

Phases. An MUAP phase constitutes the portion of a waveform that departs from and returns to the baseline. The number of phases equals the number of negative and positive peaks extending to and from the baseline, or the number of baseline crossings plus one. Normal MUAPs have four phases or less, though about 5–15% of MUAPs in distal muscles have five phases or more, and this may be up to 25% in proximal muscles, such as the deltoid, iliacus, and gluteus maximus. Increased polyphasia is an abnormal yet nonspecific MUAP abnormality since it is encountered in myopathies as well as in neuropathies. An increased number of polyphasic MUAPs suggests a desynchronized discharge, loss of individual fibers within a motor unit, or temporal dispersion of muscle fiber potentials within a motor unit. Excessive temporal dispersion, in turn, results from differences in conduction time along the terminal branch of the nerve or over the muscle fiber membrane. After severe denervation when the newly sprouting axons only reinnervate few muscle fibers, the MUAP may also be polyphasic with short duration and low amplitude (“nascent” MUAP).

Some MUAPs have a serrated pattern with several turns or directional changes without crossing the baseline; this also indicates desynchronization among discharging muscle fibers. Satellite potential (linked potential or parasite potential) is a late spike of MUAP, which is distinct, but time locked with the main potential. It implicates early reinnervation of muscle fibers by collateral sprouts from adjacent motor units.

Motor Unit Action Potential stability

Motor units normally discharge semirhythmically, with successive potentials showing nearly identical configuration due to firing of all muscle fibers of the motor unit during every discharge. The morphology of a repetitively firing unit may fluctuate if individual muscle fibers intermittently block within the unit. This instability may be evident in neuromuscular junction disorder, such as myasthenia gravis, the myasthenic syndrome, or botulism. Also during reinnervation such as motor neuron disease, subacute radiculopathy, or polyneuropathy, the newly formed endplates are immature and demonstrate poor efficacy of neuromuscular transmission. This results in unstable MUAP waveforms with moment-to-moment MUAP variability (Figure 2-26). The MUAP instability disappears when reinnervation is complete and well established and helps to distinguish between a subacute and chronic neurogenic process.

Figure 2-26 Unstable polyphasic motor unit action potential with a satellite potential. Both the main component of the potential (solid arrow) and the satellite potential (dashed arrow) are unstable. This complex potential is triggered upon using a trigger, delay line and a raster mode. Note the extreme variation in the morphology of the unit and its satellite potential between subsequent discharges.

Motor Unit Action Potential Firing Patterns

During constant contraction, a healthy individual initially excites only 1–2 motor units semirhythmically. The motor units activated early are primarily those with small, type I muscle fibers. Large, type II units participate later during strong voluntary contraction. Greater muscle force brings about not only recruitment of previously inactive units, but also more rapid firing of already active units, both mechanisms operating simultaneously.

The firing rate of the motor unit equal to the number of MU discharges in a one second time interval, and is measured in hertz (Hz). When several MUAPs are discharging they superimpose, which makes MUAP identification and firing rate analysis difficult requiring automated methods. When one or two MUAPs are firing, such as during minimal voluntary effort or when there is marked decrease in the number of MUAPs firing, this analysis become quite easy. The firing rate may be estimated manually by freezing a 100 ms epoch and multiplying the number of discharges of an MUAP by 10 to obtain a one second epoch. For example, a motor unit appearing twice in a 100 ms sweep has a firing rate of 2 × 10 = 20 Hz. The multiplication factor can be adjusted depending on the analyzed epoch, being 5 for a 200 ms epoch and 2 for a 500 ms epoch (Figure 2-27). Another way of calculating the firing rate of a motor unit is by dividing 1000 by the time interval between successive MUAP discharges in ms. For example, a firing rate of a unit with an interval of 50 ms is 20 Hz.

Figure 2-27 A slightly increased duration motor unit action potential firing rapidly. The sweep speed is set at 20 ms/division, resulting in an epoch of 200 ms. The firing rate is 5 × 5 = 25 Hz.

Motor unit firing is a dynamic process that involves a balance between the number of motor units recruited and their firing rate. With minimal contraction, one MUAP is first recruited and its firing rate when it begins to discharge is called its onset frequency. When the subject gradually increases the force of contraction, the motor unit firing rates increases slightly and eventually a second motor unit is recruited. Recruitment frequency is defined as the firing frequency just before the time an additional unit is recruited. In normal muscles, the onset frequency varies between 6 and 10 Hz while the recruitment frequency ranges between 8 and 15 Hz, and the reported ranges for healthy individuals and those with neuromuscular disorders overlap considerably. Recruitment ratio is the average firing rate divided by the number of active units. This ratio should normally not exceed 5, for example, three units each firing less than 15 impulses per second. A ratio of 10, with two units firing at 20 impulses per second each, indicates a pathologic lower motor neuron process.

Activation is the central control of motor units that allows an increase in the firing rate and force. Failure of descending impulses also limits recruitment, although here the excited motor units discharge more slowly than expected for normal maximal contraction. Thus, a decreased number of voluntary MUAPs with a slow firing rate (poor activation) is a feature of an upper motor neuron disorder (such as stroke or myelopathy) but may be seen with volitional lack of effort (such as due to pain, conversion reaction, or malingering). This stands in sharp contrast to a fast firing rate associated with a disorder of the lower motor neuron (decreased recruitment).

With greater contraction, many motor units begin to fire rapidly, making recognition of individual MUAPs difficult, hence the name interference pattern. This is assessed by its sound on the loudspeaker and the number of spikes and their amplitude. The interference pattern depends on the descending input from the cortex, number of motor neurons capable of discharging, firing frequency of each motor unit, waveform of individual potentials, and phase cancellation. An incomplete interference pattern may be due to either poor activation or reduced recruitment. Recruitment may be assessed during maximum contraction by examining the interference pattern, or during moderate levels of contraction by estimating the number of MUAPs firing for the level of activation. Evaluating MUAPs during maximal effort is most valuable in excluding mild degrees of decreased recruitment.

In myopathy, the motor unit pool produces a smaller force per unit than a normal pool. These usually low-amplitude, short-duration MUAPs must be recruited instantaneously to support a slight voluntary effort in patients with moderate to severe weakness. Early recruitment refers to the greater than expected number of discharging MUAPs for the force of contraction. With early recruitment, a full interference pattern is attained at less than maximal contraction, but its amplitude is low because fiber density is decreased in individual motor units. In advanced myopathies with severe muscle weakness and atrophy (such as in advanced muscular dystrophy), loss of muscle fibers may be so extensive that whole motor units effectively disappear, resulting in a decreased recruitment and an incomplete interference pattern, mimicking a neuropathic recruitment.