tonic and kinetic components of the evoked …

The Japanese Journal of Physiology

17, pp.415-428, 1967

TONIC AND KINETIC COMPONENTS OF THE

EVOKED ELECTROMYOGRAM

Teruo NAKAYAMA AND Tetsuro HORT

Department of Physiology, Nagoya University School of Medicine

The existence of the red and pale striated muscles has long been known.

In his detailed work on the extensor muscles, DENNY-BROWN has shown the

mode of participation of the red and pale muscles into various reflex activities,such as the tonic neck and labyrinthine reflex, the stretch reflex and the

crossed extensor reflex3, 4). The red or slow muscle has a lower threshold in

the postural reflexes. The discharge frequency of the tonic motor unit was

lower than that of the phasic motor unit1). The fact that the superficial

component of the muscle is rapidly contracting and the deep component isslowly contracting was confirmed in the flexor muscles9) as well as in the

extensor muscles3, 4).

Granit and his co-workers classified the alpha motoneuron into phasic andtonic types10). The phasic motoneurons give larger spike potentials in the

ventral root filament and respond to a sustained muscle twitch with one or

two discharges. The post-tetanic potentiation was observed only on the tonic

motoneurons. These two types of alpha motoneurons were separated also in

the crossed extensor and the pinna reflexes11). Intracellular recording of the

alpha motoneurons revealed that the tonic motoneuron has a longer after-

hyperpolarization, the duration of which is inversely proportional to the con-

duction velocity of the motor axons6). ECCLES et al. concluded that the tonic

and kinetic components innervate 'slow' and 'fast' muscles, respectively.

In clinical electromyography, the spike discharge of large amplitude re-

corded by a concentric needle electrode is often referred to as the 'kinetic

spike'. Needless to say, the amplitude of the EMG is greatly modified in

volume conductor by various factors such as, geometric configuration of the

electrode, distance between electrodes and active muscle fibers and so on.

Statistical treatment of the discharge interval of the motor units has shownthat there are two types of unit discharges and these were supposed to be

'kinetic' and 'tonic' activities19).

The present study arose from a simple observation that in a tendon jerk,

Received for publication November 21, 1966

中山昭雄,堀哲郎

415

416 T. NAKAYAMA AND T. HORI

the magnitude of the response was not proportional to the peak-to-peak

amplitude of the electromyogram. The analysis of the monosynaptically in-

duced action potential of the gastrocnemius muscle has proved that the H-wave

is a vector summation of the kinetic and the tonic muscular activities.

METHOD

The staff of the Department, including authors, acted as subjects. A stimulatingdisk electrode, 8mm in diameter, was placed to the popliteal fossa over the tibial nerve.An indifferent electrode, 8x8cm, was fixed to the medial side of the knee. Stimuluswas an isolated square pulse, 0.5 to 1 msec in duration and 15 to 50 volt in intensity.Two recording disk electrodes, 8mm in diameter, were placed on the medial or lateralhead of the gastrocnemius along the run of the muscle fibers. A bipolar recording wasmade either by surface or by concentric needle electrodes. The cathode ray oscilloscopewas triggered 24 msec after stimulation so that the evoked electromyogram could beobserved in detail. In some experiments, H-waves were added electronically by anaveraging computer, simply to confirm that the changes of wave form were not due topossible instability of the response. The knee jerk was manually elicited using thehammer with a built-in microswitch which closes on tapping and triggers the sweep ofthe CRO.

For stimulation of the dorsal root filaments, cats were tracheotomized and de-cerebrated at the intercollicular level under ether introductory anesthesia. Laminec-tomy was made between Li and L7 and the cavity thus exposed was filled by warmliquid paraffin. The dorsal root filaments were cut (Si to L5), the central end of whichwas stimulated by an isolated rectangular pulse, 0.1 to 0.5 msec in duration and 100 mVto 30V in intensity. The gastrocnemius-soleus muscles were roughly isolated from thesurrounding tissue and the Achilles tendon was fixed to the strain-gauge myograph.The lumbar vertebrae, the femur and the ankle were fixed firmly to the frame ofanimal board. Two small holes were made on the skin over the muscle belly and werefilled with the electrode jelly. The recording electrode was a small silver plate of2x2mm. For stimulation of the ventral root filament, cats were anesthetized by chlo-ralose in a dosis of 80mg per Kg body weight.

RESULTS

The magnitude of response and the amplitude of the H-wave. It is well knownthat the tendon jerk is augmented during inspiration. The peak-to-peak

amplitude of the H-wave of the gastrocnemius, however, was found to be

rather reduced when the stimulus was delivered to the subject at the top ofinspiration. The amplitude was reduced by about 20% in inspiration and the

reduction was observed more or less at any stimulus intensities tested. These

counter results provided a turning point to do the present study.The amplitude of the H-wave is also modified by the postural changes of

the subjects. The magnitude of the response is larger when the subject is

lying on the recorded side, while the amplitude of the H-wave is larger when

lying on the opposite side. The mechanical response is larger in ankle flexion,

while the H-wave is larger in ankle extension. The finding that the magnitude

EVOKED ELECTROMYOGRAM 417

TABLE 1.

The amplitude of H-wave of the gastrocnemius muscle and the magnitude

of mechanical response in human subject under various conditions.

of the mechanical response is not proportional to the amplitude of the H-wave

was further confirmed in the cat. FIG.1 shows the electromyogram and the

tension curve of the cat's gastrocnemius after stimulation of the dorsal root

filament. The stimulus intensity was 2V in A and 3V in B. The tension

developed was naturally larger in B, but the peak-to-peak amplitude of the

action potential was larger in A. Thus, the amplitude of the muscle action

potentials is not always proportional to the mechanical response. Another

FIG.1. Surface electromyogram and tension curve of the cat's

gastrocnemius muscle to stimulation of the dorsal filament. Stimulus.intensity was 2V in A and 3V in B, and was given at the start of

each traces.


significant feature to be pointed out is that the wave form is quite different

in the two records and the peak latency of the upward deflection is shorter

in B. These findings suggest that the increase of the stimulus intensity brings

about a participation of a neural mechanism which is not activated in A.

Further comment on this figure will be made in the discussion.

Form of the H-wave. With a given electrode position, the form of the H-wave

was uniform if the stimulus intensity was constant. In a lower range of

stimulus intensities, in which only the afferent fibers of the tibial nerve were

stimulated13), the amplitude of the H-wave was roughly proportional to the

stimulus intensity. In a moderate range, motor axons were stimulated and

the gastrocnemius gave a direct response (M-wave) as well as a H-wave. Ina higher range, the H-wave was inhibited by the antidromic impulses while

the M-wave was augmented in proportion to the stimulus intensity. These

observations were first made by MAGLADERV16) and reconfirmed in this study.

Basically, the H-wave is expected to have tetra-phasic deflections, which are

typical in a bipolar recording of the conductive action potential in the volume

conductor, but actually it is very of ten superimposed by a small notch. FIG.2

Ftc.2. Human surface electro-

myogram of the quadriceps femoris

in the knee jerk.

is a record taken from the quadriceps femoris in the knee jerk. In the upward

deflection following the initial downward deflection, a notch can be seen which

is less clear in the upper and more distinct in the lower record. The wave

form changed more or less with the electrode position, but the notch which

appeared a few msec later than the first deflection was noted in most records.

The configuration of the H-wave of the gastrocnemius was quite similar to

that of the response of the quadriceps femoris in the knee jerk.

Stimulation of the ventral root filament. FIG.3 shows the action potentials

of the cat's gastrocnemius after stimulation of the corresponding ventral fila-


FIG.3. Electromyogram of the

cat's gastrocnemius to stimulation of

the ventral filament. Stimulus inten-

sity was increased as indicated.

ment. At the stimulus intensity of 100 mV, the triphasic action potential was

recorded with a latency of 3 msec. This latency did not change even with

increased stimulus intensity. The notch appeared when the stimulus intensity

was increased to 200 mV. At the stimulation of 500 mV, both the first and

second downward deflections were augmented. This made the maximum res-

ponse of the gastrocnemius in this case, because a further increase of stimulusintensity did not alter the wave form. Thus, FIG.3 indicates that as far asthe motor axons are stimulated, the short latency component of the H-wave

has a lower threshold than the long latency component which gives rise to

the notch.

Stimulation of the dorsal root filament. The central end of the S1 dorsal rootfilament was stimulated at various intensities (FIG.4). At 2V, the latency

was 5.7 msec and at 5V it was 5 msec. The amplitude was increased but the

latency remained unchanged at 10V. The latency reduced suddenly to 3 msec

and the first downward deflection appeared at the intensity of 20V. Further

increase of stimulus intensity did not change the latency. The result shows

that the rapid component of the compound action potential has a higher

threshold than the slow component in the stimulation of the dorsal filament.

420 T. NAKAYAMA AND T. IIORI

FIG.4. Electromyogram of the cat's gastrocnemius to stimulation of the

dorsal filament. Stimulus intensity was increased as indicated.

FlG.5. Action potentials of the

motor fiber (upper trace) and the

EMG of the gastrocnemius (lower

trace) to stimulation of the dorsal

filament.

FIG.5 was recorded from the muscle nerve (upper trace) and the gastro-

cnemius (lower trace) in response to the stimulation of the S1 dorsal filament.

The nerve action potential has two peaks suggesting that the short and long

latency components have their own motor fibers which are different in con-

duction velocity.

Post-tetanic potentiation. The S1 dorsal root filament was stimulated at the

frequency of 500 cps for 10 sec and then the monosynaptic evoked potential of

the gastrocnemius was recorded at an interval of 20 to 30 see (FIG.6). The

response to the test stimulus was increased more than twice 20 sec after the

tetanic stimulation and declined with a lapse of time. In this case, the effect

EVOKED EL, ECTROMYOGRAM 421

FIG.6. rost-tetanic potentiation. Tetanic stimulation (500 cps) was

given to the S1 dorsal filament for 10 sec and 20 sec later the test stimuluswas given at the interval of 20 to 30 sec. The left figure shows the elec-tromyogram of the cat's gastrocnemius and the right illustrates increased

peak-to-peak amplitude of the muscle action potential after tetanization.

of the PTP lasted for 3 min. The downward deflection of the control action

potential is not uniform, that is, the deflection is made of two components

although the notch is not clearly seen in this record. The component aug-

mented by tetanic-potentiation is the second peak of the downward deflection

which is made by the slow component mentioned above.

Hacares in muscular actirilies. FIG.7 shows the H-wave in various muscular

activities in man. In A, the gastrocnemius was relaxed and the surface elec-

trode did not pick up any activitiy. In B, the subject was requested to keep

the gastrocnemius in a weak postural tonus, during which the surface elec-

tromyogram showed activities of about 5ƒÊV. C was taken while the gastro-

cnemius was in a maximum voluntary contraction. The amplitude of the H-

wave is large in C and small in B. The upward deflection was steepest in C

and less in B. The peak latency of the H-wave is short in C and long in B.

The notch mentioned previously is observed clearly in A, but less in B and

absent in C.

Changes of the H-wave are illustrated in more detail in FIG.8. The

stimulus intensity was increased in the order of A, B and C as seen in the

size of the M-wave. The subject made a voluntary contraction of the gastro-

cnemius in C. In each recording, the H-wave was expanded both in the X

and Y axis on the second beam of the dual beam oscilloscope, as is shown in

the right half of the figure. In this figure, the notch appeared in the down-

ward deflection. A and B show a similar wave form but the amplitude is


muscular activities H-waves

FIG.7. Muscular activities and H-waves. The left figures show

activities of the gastrocnemius, during which II-wave was recorded

as shown on the right side. A: at rest, 13: in weak postural tonus,

C: in maximum voluntary contraction. Stimulus intensity was con-

stant.

FIG.8. M- and H-waves of the gastrocnemius muscle in man to stimu-lation of low (A), medium (13) and high (C) intensity. In C, the subjectmade maximum voluntary contraction of the gastrocnemius. The portionsof the H-wave of the left figure were expanded on both X and Y axis andwere represented on the right hand sidle.


reduced in B. This is apparently due to the fact that the monosynaptic res-

ponse was inhibited to some extent by the antidromic volley of the motoraxon which was fired by an intense stimulation. In C, the peak latency of

the upward deflection was short and the notch was not observed. It seems

that the H-wave, in this case, is composed of the short latency component

only and the long latency component is completely abolished. The reason for

which will be mentioned in the discussion. In all of the three records the

peak latency of the first downward deflection was the same, as is shown bythe dotted line. These results may suggest that the H-wave is a summation

of two components: the first downward deflection is caused by a rapid com-

ponent and the notch, the second downward deflection, is made by the sum-mation of a slow component.

Discharge of the muscular unit and the H-ware. The monosynaptic reflex

responses of the gastrocnemius muscle to stimulation of the tibial nerve were

recorded simultaneously by surface and concentric needle electrodes in human

AB C

D

FIG.9. Simultaneous recording of the action potential

from the gastrocnemius muscle to stimulation of the tibial

nerve. Upper trace was recorded by a concentric needle

electrode and the lower trace was recorded by surface elec-

trodes. CRO was triggered 21 msec after stimulation.


subjects. In each record of FIG.9, upper traces show the activity of theneuromuscular units. In A and B, the latencies of the upper traces are the

same as those of the H-wave; the initial downward phases of the upper traces

are followed by a rapid spike, the onsets of which fairly coincide with the

notch of the H-waves. The initial downward phases seem to be caused by

current spread from the remote component which has a short latency and the

spike is the activity of the motor unit near the tip of the needle electrode.In C, the upper trace lacks the initial downward phase and the response begins

coincidently with the notch as indicated by the dotted line. In D, by contrast,the latency of the large spike of the upper trace was the same as that of the

H-wave. The unit discharges in C and D must make the long and shortlatency components, respectively. The former was more easily recorded when

the needle electrode was inserted into the relatively deep layer of the muscle,

while the latter was recorded mostly from the superficial part of the muscle.

DISCUSSION

The rapid component of the H-wave mentioned in the "Results" has ashort latency and a low threshold resulting from the stimulation of the ven-

tral root filament. This tells us definitely that the rapid component represents

a kinetic activity. ECCLES et al. has shown that the motor axon of the kinetic

motoneuron has a lower threshold and a rapid conduction velocity6). The

slow component must be a tonic activity. GRANIT et al. differentiated the

tonic motoneuron from the phasic motoneuron by the fact that the former is

potentiated by tetanic stimulation10). The lower threshold of the slow com-

ponent from the stimulation of the dorsal root filament is well understood inthe light that the tonic motoneuron receives a more dense projection of the

Group 1 afferent5). There is no doubt that the H-wave is induced by the

stimulation of the Group la afferent16). Bipolar recordings of the conductiveaction potential in the volume conductor usually give tetra-phasic waves, the

third and fourth deflections are often less clear. Indeed, the surface recording

of the electromyogram makes one of the recordings from the volume conduc-

tor and fundamentally is not different from the recording made by the con-

centric needle electrode. Both the kinetic and tonic muscular units give tetra-

phasic deflections but with different latencies. There are some motoneuronswhich show an intermediate character in their after-hyperpolarization and in

conduction velocity6), but statistically a-motoneurons are considered to be dif-

ferentiated into two categories. The vector summation of these two is ex-

pected to turn in a variety of wave forms. The notch may appear on thefirst deflection or on the second deflection depending mainly on the relative

position of the electrodes in respect to the active muscle fibers. The peak-to-

peak amplitude is reduced if the upward deflection due to the tonic activity


FIG.10. Vector summation

of the tonic and kinetic action

potential makes the H-wave.

is cancelled by the downward deflection of the kinetic activity (See FIG.10).

On this basis, the reason is well understood why an increased intensity of

stimulus often results in a decreased amplitude of the H-wave. Thus, theamplitude of the H-wave can not be a measure of the muscular activity.

Based on these considerations, it can be said that the kinetic activity isincreased if the peak latency of the upward deflection becomes short. In-

creased activity of the tonic components is manifested by the increase of the

second downward deflection, which, however, may in some cases be cancelledby an upward deflection of the kinetic component simultaneously activated.

Such being the case, one may think that the amplitude of the H-wavewas decreased by chance during inspiration. However, the fact that this

reduction of amplitude is always observed, regardless of the position of the

recording electrodes on the muscle, needs another explanation. Respiratory

movement is known to modify various body functions, such as a tendon jerk14),

cutaneous sensations18)and so on, possibly due to the spread of the respira-

tory neuronal activities of the medulla to the surrounding reticular formation.

Augmentation of the tendon jerk in inspiration seems to be brought about byan increased activity of the tonic components. Tonic muscles give a slow but

large tension curve, while the kinetic muscles develop a rapid but small ten-

sion2,6,8). The reduction of the amplitude of the H-wave in inspiration is now

understood as follows: the tonic activity of the gastrocnemius motoneurons is

increased and gives a large mechanical reflex response, but the kinetic activity

is inhibited reciprocally. The action potential of the tonic muscle fibers as

recorded by the surface electrode is smaller than that of the kinetic fibers,

426 T. NAKAYAMA AND T. HOR1

possibly because the tonic fibers exist rather in a deep layer of the muscleand the action potential of the kinetic muscle fiber itself may be large. The

decrease of the kinetic muscle action potential, therefore, decreased the am-

plitude of the H-wave, regardless of the increase of the tonic activity.The same explanation may apply to the decreased amplitude of the H-

wave in lying on the recorded side. Inhibition of the kinetic activity andfacilitation of the tonic activity have been pointed out by one of the authors

in the postural and labyrinthine reflexes17). In the ankle flexion, tonic moto-

neurons of the gastrocnemius are facilitated by the increased number of im-

pulses from the primary endings and cause an augmented reflex contractionof the muscle. The decrease of the H-wave in the ankle flexion seems to be

due to the decreased activity of the kinetic motoneurons. The H-wave was

inhibited also in a weak postural tonus. The fact that the kinetic activity

is inhibited in this condition, which is manifested in FIG.7, suggests that the

physiological influences from the higher level upon the spinal motoneuron maybe reciprocal between tonic and kinetic neurons.

FIG.8 shows that the kinetic component is activated and the tonic activity

is inhibited during the voluntary maximum contraction of the gastrocnemius.

Although the exact mechanism of this phenomenon is not fully clarified, the

following three possibilities may be taken into consideration. An antidromic

volley of the motor axon may be blocked by the natural orthodromic impulses

to the muscle, so that the monosynaptic response is elicited in this reflex arc.

Statistically, the blocking of the antidromic volley has to take place twice asoften in the kinetic motor axon, because the maximum rate of discharge in

voluntary contraction is 30 to 60 and 10 to 20 impulses per sec in the kinetic

and tonic motor fibers, respectively11). Consequently, the tonic activity is sub-

jected to a greater extent to the antidromic inhibition. The second possibilityis that in the maximum voluntary contraction, the kinetic motoneurons are

activated, which in turn inhibit the tonic motoneuron via the RENSHAW

cens7,12,15). The third explanation is that the higher influences to the spinal

motoneuron may be reciprocal between the kinetic and tonic activities. Dur-

ing the voluntary maximum contraction, the kinetic activities may be facilit-

ated while the tonic neurons may be inhibited.

From the practical point of clinical electromyography, the present study

offers a unique method to identify whether the unit subjected is kinetic or

tonic. In simultaneous recording of the evoked electromyogram by surface

and concentric needle electrodes, the kinetic unit has the same latency asthe H-wave and the tonic one discharges coincidently with the notch of the

H-wave.


SUMMARY

1. The peak-to-peak amplitude of the H-wave of the gastrocnemius muscle

was inhibited in inspiration, in lying on the recorded side and in an ankle

extension, while the magnitude of the mechanical response was augmented.

2. The form of H-wave is not tetra-phasic, but is very often superimposed

by a small notch suggesting that the H-wave is composed of two components.

3. The long latency component has a lower threshold to stimulation of the

dorsal root filament and potentiated by tetanic stimulation.

4. The short latency component has a lower threshold to stimulation of the

ventral root filament and augmented during voluntary contraction.

5. Some muscular units have a same latency with the H-wave and others

fire coincident with the appearance of the notch.

6. The short and long latency component is the kinetic and tonic activities,

respectively.

7. The H-wave is the vector summation of these two activities, so that the

peak-to-peak amplitude can not be a measure of the machanical response.8. H-waves in various state of muscular activities were discussed from the

standpoint of tonic and kinetic activities.

The authors wish to express their thanks to Dr. K. TAKAGI for his reading the

manuscript.

REFERENCES

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tonic and kinetic components of the evoked …

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