Unloading Reflexes and the Silent Period

New Developments in Electromyography and Clinical Neurophysiology,

edited by J. E. Desmedt, vol. 3, pp. 589-602 (Karger, Basel 1973)

Studies of the Normal Human Silent Period

Β. Τ. SκΑκΑΝτ and R. R. YouNG
Department of Neurology, Harvard Medical School and Massachusetts General
Hospital, Boston, Mass.

The term `silent period' refers to a transitory, relative or absolute de-

crease of EMG activity, evoked in the midst of an otherwise sustained con-
traction. In man, the tonic background EIG activity is usually produced by
voluntary assumption of tension within a muscle. In animal studies, it has
been produced by the evocation of tonic reflex contraction, for example, as
the crossed extensor accompaniment of a prolonged flexor reflex. Though
periods of electrical silence in EIG activity are often seen in association with
intermittency of contraction, fatigue, tremor, clonus and so forth, the term
silent period (SP) should be reserved for reflex pauses following a stimulus
of some sort : an electrical shock to skin and peripheral nerve, a tendon tap
or other means of eliciting phasic reflex activity or sudden decreases in the load
against which the muscle is contracting.
The SP was discovered in man when HOFFMANN [1919] superimposed an
electrically induced twitch upon voluntary EMG activity. Its reflex nature
was quickly appreciated and over the years frequent attempts have been made
to interpret the SP in terms of contemporary physiological mechanisms
[DENNY-BROWN, 1928 ; GRANIT, 1955; MERTON, 1951, ANGEL, this volume]
with the explanations becoming more complex as knowledge of muscle
spindle, Golgi tendon organ and Renshaw cell behavior has increased. Sim-
ultaneously its behavior under various circumstances was used as a tool to
dissect even more complex motor phenomena such as posture [DENNY-
BRowN, 1928], normal control of movement [GRANIT, 1955; MERTON, 1951],
and certain pathological entities such as spasticity, rigidity and tremor.
ANGEL and STRUPPLER et al. [this volume] review the pathophysiology of these
latter conditions and the mechanisms responsible for the SP produced by
rapid unloading of a muscle during isometric contraction.
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Most studies have dealt with the SP produced by electrical stimulation of

peripheral nerves and the skin overlying them. Insufficient attention was paid
to the possible role played by activity that such stimulation would induce in
fibers other than muscle afferents and efferents. Because purely cutaneous
stimulation has recently been shown to produce a SP and because the SP has
always occupied such a central role in discussions of motor physiology, we
plan to review these new findings as well as other observations of the normal
behavior of the SP in an attempt to determine more precisely the role of
various central and peripheral factors influencing motoneurone excitability
in man.

Methods

Ten normal adult subjects were studied. BIG activity was recorded from adductor
pollicis, abductor pollicis brevis, abductor digiti quinti, biceps brachii, tibialis anterior,
soleus, masseter, and orbicularis oculí muscles, using concentric needle electrodes or
clip electrodes [CoPØ and Dwgs, 1964] and was photographed on moving paper or
with a Polaroid camera. Silent periods were evoked by electrical stimulation delivered
through DISH 13 Κ62 surface electrodes to the ulnar, median, superficial radial, medial
popliteal, posterior tibial, sural or facial nerves, or the skin overlying the motor point of
masseter or, through ring electrodes, to the digital nerves of the fingers. Stimuli were
square waves 0.1-1.0 msec in duration and of nominal amplitude 10-50 V led from a DISH
Multistim or from a Grass S88 stimulator through a special SIU 5 isolation unit capable of
300 V output. SP were recorded during an evenly sustained isometric background contraction
except in the case of orbicularis oculí where the tension produced is difficult to measure.
Background (0.5-1.0 kg) and twitch tension were recorded primarily from adductor pollicis
with the subject seated, the forearm supported and the hand fixed in a specially designed
splint. The proximal phalanx of the thumb was connected to a steel bar on which two
ceramic strain gauges (Ether 3A-1A 350Ρ) were cemented. These made up two arms of a
Wheatstone bridge circuit connected to a DC amplifier. Isotonic twitch contraction was
recorded by interposing a spring between the thumb and strain gauge. All experiments were
performed in a warm room (24-26 °C).

Results

As found by Mrnroi [1951], even a very small twitch is accompanied by

a recognizable SP (fig. 1 A and C), whereas a more characteristic, longer SP
follows a supramaximal shock to the ulnar nerve (fig. 1 B and D). With a
maximal twitch, the duration of SP ranged in different subjects from 100 to
120 msec as measured from the stimulus artifact; it was fairly constant in any
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 Studies of the Normal Human Silent Period 591

Ji kg

illmsec

Fig. 1. The effect of alterations in stimulus strength upon the SP in adductor pollicis.
A, B Isometric twitches. A Submaximal electric stimulus to the ulnar nerve. B Supramaxímal
stimulus. C, D Isotonic twitches (see methods). C Submaximal stimulus. D Supramaxímal
stimulus.

individual. Approximately 30 msec after the stimulus, the electrical silence is

broken by a synchronous potential, the F response of MAGLADERY and
MCDOUGAL [1950]. When the strength of stimulus was reduced (fig. 1 A and
C), voluntary potentials appeared in the midst of the SP at 50-80 msec after
the shock and occasionally between 30 and 50 msec. All these observations
were the same under isometric and isotonic recording conditions.
However, there is a difference between these two conditions in the dura-
tion of the SP with submaximal twitches. With isometric recording the dura-
tion is the same as with the maximal twitches described above, whereas with
isotonic twitch contractions the eventual resumption of voluntary activity
takes place 15-25 msec earlier (fig. 1 C).
A SP is also produced by reflex contractions (fig. 2A). In figure 2Β a
single electrical stimulus, subthreshold for motor fibers, was delivered at the
arrow to the medial popliteal nerve and the H-reflex response can be seen
with a latency of 30 msec. When this is repeated during a background con-
traction in soleus, the electrical silence (fig. 2A) begins with the arrival
of the H-reflex in the muscle rather than with the arrival of a direct muscle
(M) response as noted previously with stimuli above threshold for motor
fibres.
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ιιιιιilι
+

Fig.2. The SP in soleus produced by an H-reflex discharge is seen in A. The electrical

stimulus (arrow) to the medial popliteal nerve only activates IA afferents producing the
Η-reflex without a direct M response. The same stimulus without the background EMG
activity is seen in B. Calibrations are 100 msec and 500 0V.

Fig. 3. Each of these represents EMG activity of 5 superimposed sweeps. A Α SP

seen in the background voluntary contraction in abductor pollicis brevis following stimu-
lation of the median nerve at the wrist. B The response in orbicularis oculi following a
maximal stimulus to the facial nerve. Voluntary contraction of the same muscle is seen in D
while C represents superimposition of B and D. Note the very brief SP in C compared with
A. Stimuli are delivered at the arrows. Calibrations are 50 cosec for each, 2 mV for B, Cand D.

SP studies in man have usually been restricted to muscles in the hand or,
less often, the arm. Because muscles vary in anatomical configuration, size,
speed of contraction and concentration of muscle spindles, clues to the nature
of the SP may be obtained by studying it in a wide array of muscles. For ex-
ample, when stimulating the facial nerve (fig. 3 B) and recording the volun-
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 Studies of the Normal Human Silent Period 593

r
~

Fig.4. SP produced by cutaneous stimulation. A EMG of biceps brachii with stimu-

lation of the superficial radial nerve at the wrist. B The same stimulus produces an SP in
abductor pollicis brevis, and in C an SP in the latter muscle is produced by stimulation of
the digital nerves of the middle finger. Stimuli are delivered at arrows. Calibrations are
20 msec and 500 µ1.

tarily contracting orbicularis oculí (fig. 3 D), only a very brief and relative
electrical silence, lasting perhaps 30 msec, is seen (fig. 3 C). This is quite dif-
ferent from the SP in abductor digiti minimi (fig. 3A) or masseter [see SHA-
HANM and YOUNG, this volume, and STRUFPLER, STRUPPLER and AnAis, 1963]
under the same circumstances.
Supramaximal stimuli delivered to a mixed nerve, as in MERTON'S
studies [1951] or those reported here, have potential effects other than those
usually considered. In addition to producing impulses in motor fibers and in
at least the larger diameter muscle afferents (In and IB), such stimuli also
activate larger cutaneous fibers running in the mixed nerve. Fortunately, one
can stimulate such fibers in isolation in sensory nerves such as the superficial
radial at the wrist or digital nerves in the fingers, and such stimuli also pro-
duce a SP in the background voluntary contraction (fig. 4, 5). This cutaneously
evoked EMG silence is present from roughly 50-100 msec, after the stimulus
in the upper extremity and from 80-140 msec, after the stimulus in the leg.
There is also slight variation from muscle to muscle and nerve to nerve. This
SP is produced in muscles proximal (fig. 4A, C) as well as distal (fig. 4 Β) to the
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 SHAHAM/ŸOUNG 594

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Fig.5. A cutaneously evoked SP is seen with the same timing in each of a pair o;
antagonistic muscles. Simultaneous superimposed EMG recordings from solens on the
upper line of each par and from tibialis anterior on the bottom line. Ιn A and B voluntary
activity is present in soleus, and in C and D the activity is in tibialis anterior. In A and C the
stimulation is applied to the posterior tibial nerve at the medial malleolus, whereas in B and
D the sural nerve is stimulated at the lateral malleolus. The stimulus artifacts, as at arrows
in A, are clearly visible. Calibrations are 20 msec and 500 µV for one large division on the
graticule.

site of stimulation. Furthermore, it occurs at approximately the same time in

either of an antagonistic pair of muscles (fig. 5, compare Α with C, and B with
D) though the latency and duration varies in the same muscle depending on
which nerve is stimulated (compare Α and C with B and D). For example, the
SP begins sooner in gastrocnemius or tibialis anterior following a stimulus at
the ankle to sural nerve as compared with one to the tibial nerve (80 versus
100 msec). The SP in these muscles also has a longer duration with sural stimu-
lation because the return of voluntary activity takes place at about the same
time following the stimulus to either nerve.

Discussion

When a SP is produced by the method of MERTON [1951] used in this

study, the stimulus to the mixed nerve sets up two volleys of impulses, one of
which ascends to the spinal cord and the other descends to the muscle. The
ascending volley in motor fibers either results (a) in a collision of ortho- and
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 Studies of the Normal Human Silent Period 595

antidromic impulses somewhere in the motor axon between the cell body and
the site of stimulation if that motoneurone was active within plus or minus the
conduction time from cell body to stimulus site (of the order of 12 msec in the
case of stimulation at wrist), or (b) antidromic firing of the motoneurone if it
had not been active within plus or minus 12 msec of the stimulus. In addition,
the antidromic motor impulses which either collide central to the origin of the
recurrent axon collateral or invade the motoneurone would invade the col-
lateral to activate Renshaw-like cells, if such exist in man. Allowing for con-
duction centrally in motor fibers, for conduction peripherally again to the
muscle and assuming for the moment that the anterior horn cell will continue
to fire at rates of roughly 25/sec, it can be shown that electrical silence will
persist in the EMG from the arrival of the direct M response, some 3-4 msec
after a stimulus at the wrist, for the next 45-65 msec even if one ignores pos-
sible Renshaw effects. The `antidromic inhibition' described by RENSHAW
[1941] in the cat could not have an effect on the human EMG peripherally for
at least 30 msec after the stimulus ; this time allows for conduction centrally,
the onset of segmental inhibitory effects and the conduction peripherally of
impulses which arose just before the recurrent collateral inhibition began.
Therefore, the silence seen between the M and F responses (the latter occur-
ring some 30 msec after the stimulus) is explicable purely on the basis of
effects on conduction in motor axons and cannot be due to any changes in
CNS activity. If antidromic firing is avoided by using a stimulus below thre-
shold for motor fibers to produce a synchronous H-reflex, no Ell silence is
seen during the first 30 msec after the stimulus (fig. 2).
The effect of the ascending volley produced in sensory fibers by the stimu-
lation is more difficult to comprehend. The usual percutaneous stimulus
would be expected to activate Ia and In fibers from primary endings on the
spindle and Golgi tendon organs respectively, as well as large fibers from
joint receptors, cutaneous and subcutaneous structures, and so forth. Again,
allowing for conduction times, this volley of impulses could not produce an
EMG effect in less than 30 msec after the stimulus, which is the latency of the
H-reflex, taken to be the result of a volley in In fibers. This synchronous firing
of much of the motoneurone pool would also be expected to produce, via the
recurrent collateral pathway, considerable local Renshaw inhibition that would
tend to produce Ell silence for some time after the arrival of the H-reflex in
the muscle. Recent studies in the cat [RYALL, PIERCEY, PILOSA and GOLDFARB,
1972] have shown greater Renshaw cell activation following antidromic as
opposed to orthodromic monosynaptic activation of the motoneurone pool.
The effect of a volley in IB, joint or cutaneous fibers is less clear. Ιn the latter
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instance, at least, the SP produced (fig. 4 and 5) appears about 50 msec after
the stimulus at the wrist and persists for another 50 msec or so. In summary,
though the ascending volley in motor and sensory fibers may produce EMG
silence by Renshaw or other mechanism from 30-75 msec (see below) after
the stimulus, the first 30 msec of the SP is produced by peripheral antidromic
effects and tends, therefore, to be less noticeable or absent when the stimula-
tion of motor fibers is minimized or the conduction distance in them is shorter.
The next segment of the SP (from 30 to 50 or 60 msec after the stimulus)
occurs too soon to be explicable on the basis of cutaneous effects (50-100 msec)
or of effects produced by the volley descending from the site of stimulation to
the muscle. In the mechanical trace (fig. 1) the twitch begins 12-15 msec after
the stimulation or 9-12 msec after the arrival of the M response. Α certain
degree of extrafusal muscle contraction must occur before the spindles are
unloaded or the Golgi tendon organs begin to discharge. Though Iλ and IB
fibers are fast conducting, at least 30 msec must elapse in the case of human
hand muscles between any peripheral action and the appearance in the BIG
of increased or decreased activity related thereto. The effects of the descending
volley on the SP cannot be expected before 50-60 msec elapse after the stimu-
lus and the second segment of the SP must, therefore, be due to factors other
than the modification of proprioceptíve or cutaneous input produced by the
stimulus. The persistence in humans of only the first 50 msec of the SP in de-
afferented muscles [Sηληλντ and YouriG, unpublished] supports this hypo-
thesis and suggests that the initial volley in IB, joint and other fibers plays re-
latively little role in at least the first half of the SP. The factors responsible for
the silence between 30 and 50 or 60 msec must include antidromic collision
and motoneurone firing which could produce relative silence, as noted above,
up to 45 or 65 msec. One must also not forget possible effects of an antidromic
volley in Ia fibers into the spindles themselves [IλrrnΕws, 1964]. In addition,
a Renshaw effect, if present in humans, would be expected no earlier than
30 msec and would persist for at least the next 30 msec or so. Interestingly, if
weaker stimuli are used, few motor axons are stimulated, less Renshaw effect
would be expected, and under these conditions, a brief return of voluntary
action potentials can be seen (fig. 1) at 50 to 60 or more msec. The second
segment of the SP is probably due to a combination of some of the same peri-
pheral antidromic effects described in discussions of the first segment as well as
hypothetical Renshaw effects which may also spill over into the next segment.
The third segment of the SP also has a multifactoríal basis. In upper ex-
tremity muscles, at least, the role of the cutaneous afferents merit serious
consideration because, in isolation (fig. 4 and 5), they produce a SP between
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 Studies of the Normal Human Silent Period 597

50 and 100 msec after the stimulus. That interval comprises the latter half of
the usual SP (the third segment in our terminology), and since we know that
a single volley in radial nerve can produce it, we are forced to assume that a
volley in all the large cutaneous fibers in the ulnar or median nerve at the wrist
can also. HOFFMANN and associates described an SP in masseter following
cutaneous stimulation of the oral mucosa [HOFFMANN and TbNNIES, 1948]
and in gastrocnemius and soleus following an electrical stimulus to the skin
of the foot [HOFFMANN, SCHENCκ and TÖNMES, 1948] ; SCHEΝcκ and KOEHLER
[1949] soon found that the latter stimulus could also produce an SP in both
gastrocnemius and tibialis anterior. HAGBARTH [1960], using trains of noxious
stimuli, found excitation in one group of leg muscles (usually flexors but at
other times extensors, depending on the site of stimulation) and inhibition in
the antagonist group. These silent periods, though clearly of cutaneous origin,
were considered to be examples of reciprocal inhibition though at times no
actual reflex was seen in the muscles antagonistic to those where the SP was
seen. KUGELBERG, EKLUND and GRIMBY [1960], using the same techniques as
HAGBARTH, reported much the same findings, including the observation that
the SP began slightly before the associated reflex contraction. In addition to
reciprocal inhibition, KUGELBERG et al. used the term `ambivalent inhibition'
to describe the simultaneous SP in antagonistic muscles.
In 1961, LIBERSON reported that cutaneous stimulation could produce
an SP in many muscles — he cautioned against ignoring this factor — but sub-
sequent authors in their discussions of the physiology of the SP [HERMAN,
1969; HUFSCH/c r, 1966; MATTHEws, 1964] were apparently not aware of
the importance of cutaneous factors. HUG~ON [1967] and DELWAIDE, SCHWAS
and YOUNG [1971] also described a cutaneously produced SP. Once again,
physiological studies in man have demonstrated a new entity, the cutaneous
SP, the basic neurophysiology of which remains to be worked out. The timing
of the cutaneous SP (minimal latency in bulbar muscles with progressively
longer latencies when recording from proximal arm, hand and leg) supports
the contention that so-called `long loop reflexes' [EccLES, 1966; ΤΑΒοιuκονΑ
and SAx, 1969] may be involved, and other preliminary evidence suggests that
the ipsilateral cerebellar hemisphere is necessary for its presence. Because it
comes between 80 and 140 msec after stimulus in triceps surge, whereas the
usual SP is up to 100 or 120 msec long, less contamination of the latter with
cutaneous factors results, though an overlap is still present. Our impressions
are that stimuli supramaximal for motor fibers are required to produce a clear-
cut cutaneous SP and that lesser stimuli may tend to produce less cutaneous
effects as compared to proprioceptive. Studies with quantitative evaluations
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of stimulus current are needed. Nevertheless, supramaximal stimuli, such as

MERTON used, clearly produce cutaneous effects which cannot be ignored.
MERTON [1951, 1953] suggested that the latter half of the human SP was
related to a response of a `length servo' to an external disturbance causing
shortening of the muscle which unloaded spindles, reduced their discharge
(`spindle pause'), and thereby withdrew reflex excitation from motoneurones.
The subsequently postulated closed loop feedback circuit provided a mechan-
ism whereby the muscle could be set reflexly to any desired length, and it was
postulated that voluntary muscle activity is produced by such a servo with the
fusimotor fibers being the normal pathway for initiating voluntary contrac-
tion. This was an extremely fruitful hypothesis, giving rise as it did to the servo
loop theory of motor control with many subsequent physiological experi-
ments. However, since 1951 many studies, reviewed most recently by MAT-
THEWS [1964], ΒURκE [1971], and VALLBO and HAGBARTH [this volume] re-
quired the substitution of the concept of α-γ coactivation for MERTON's orig-
inal theory of γ-firing leading α-firing around the servo loop during voluntary
and other movements.
As noted above, the most constant period of electrical silence beginning
about 50 msec after the stimulus lasts 30 or 40 msec and can be seen as long as
there is any extrafusal contraction, whether isometric or isotonic (fig. 1).
Since this period of silence is present even with minimal isotonic contractions,
it may be related to modifications of the proprioceptive input dependent more
upon changes in length of muscle than in tension. The `pause' in In afferent
discharge with unloading of the muscle spindles during the rising phase of the
extrafusal twitch contraction which has been demonstrated in cats may, per-
haps, be present in man as well. If so, this pause would withdraw excitatory
input to the motoneurones during the time necessary to produce this part of
the SP. The physiology of human muscle spindles is totally unknown, apart
from recent data on afferent discharges in mixed nerves [HAGBARTH and
VALLBO, this volume], and though much has been ascribed to their function
and dysfunction in human health and disease, it is entirely speculative. Ana-
tomical information about human muscle spindles is extant, however ; no one
has found typical spindles in facial muscles [SHAιλνι and YouNG, this vol-
ume]. Therefore, the absence of the third segment of the SP in orbicularis oculi
at least supports our contention that it is related to changes produced in spindle
discharge by the superimposed twitch.
The first segment of the SP is present in facial muscles but, as in masseter,
it is slightly briefer than in more distal muscles (25 vs. 30 msec). The second
segment of the SP is less obvious or absent in facial and masseter muscles.
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Because of the shorter conduction distance, the antidromic effects discussed

above would be shorter-lived and would not spill over into the second seg-
ment. There is also some question in man [RAmµον y CAJAL, 1909] and ani-
mals [Pοξrξκ, 1965 ; Suit, 1969] as to whether recurrent collaterals and
Renshaw cells are present in masseter and other brain-stem motor nuclei. If
in man they are not, as suggested by PΕχΡDrn s and DELWMDE [this volume],
these findings in facial and masseter muscles would again support the hypo-
thesis that Renshaw inhibition plays some role in the second segment of the
SP. Muscle spindles have been demonstrated in masseter [COOPER, 1966] and
the third segment of the SP is present there but not in facial muscles. There
are, of course, other differences between facial and hand muscles, for example,
the thin sheet-like nature of the former, the difficulty in measuring tension in
the face and the shorter conduction distances and segregation of facial af-
ferents in the trigeminal nerve from efferents in the facial nerve. The presence
of a third segment of the SP in masseter and with weak isotonic contraction
distally, and the failure to produce an SP in the face even with stimulation of
both 5th and 7th cranial nerves [PENDERS, 1969] suggest, however, that the
most important difference lies in the absence of spindles in the face. The ab-
sence of the third segment of the SP in the face, therefore, might support our
hypothesis that the spindle pause plays a significant role in its origin.
To return to the peripheral limb musculature, an isometric twitch con-
traction of any amplitude or a maximal isotonic twitch produces an additional
15-25 msec of electrical silence compared with the SP produced by the sub-
maximal isotonic twitch described above. This last portion of the SP seems,
therefore, to be predicated upon the development of a certain tension within
the muscle, suggesting that tension receptors such as Golgi tendon organs
might be involved. MERTON [1951] felt it unlikely that tendon organs could
account for any part of the SP seen with small isometric contractions because
it was then thought that these receptors had relatively high thresholds for
activation by tension. HouK and HENNEMAN [1967] have shown in the cat,
however, that tendon organs are quite sensitive to tension developed by active
contraction of extrafusal fibers; for example, the contraction of a single fiber
that produces 0.1 g tension may cause inhibitory afferent activity in Is fibers
at the rate of 25/sec. Human tendon organs may discharge, therefore, in pro-
portion to tension developed by a muscle and, as far as timing goes, could
provide inhibitory input to account for much of the last half of the SP inclu-
ding the latter 20 msec or so. HIJFSCHMIDT [1966], for example, thinks that
Is input accounts for most of the SP. It was also shown that in cats, isotonic
contractions which merely shortened a muscle without producing much ten-
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Fig. 6. Schematic representation of factors presumably involved in SP (S-P where S is

the stimulus). The first 50-60 cosec (S-A) is related to various antidromic factors including
Renshaw recurrent inhibition. At A' the muscle spindles begin to be unloaded and the
Golgi tendon organs begin to be stimulated. At W the spindle pause ceases, and tendon
organ firing may carry on until P'. Voluntary activity resumes at P. Calibrations are 100 msec
and 1 kg.

sion resulted in a feeble tendon organ response [HouK and HUNNEMAN, 1967]
which might then fail (as in fig. 1 C) to produce the last 15-25 msec of the
SP. HERMAN [1969] reported no difference in the length of the SP in triceps
surge under isometric or isotonic conditions. He also found the SP duration
to persist for 175 to more than 200 msec, and we cannot account for this
discrepancy.
To account for the last half of the SP, at least the following factors must
be considered : poorly understood cutaneous input, particularly with electrical
stimuli supramaximal for motor fibers, muscle spindle unloading and Golgi
tendon organ activation. The first, though of little interest to neurophysio-
logísts, is clearly demonstrable in man, whereas the latter two have been ex-
tensively investigated in animal laboratories but remain terra incognita clini-
cally. The time relationships between stimuli and EMG response may be
difficult to visualize because of the delay around the loop from changes in
firing of muscle receptors, spinal modification of resultant input, increase or
decrease of motoneurone activity to eventual EMG changes. Figure 6 sche-
matically portrays hypothetical roles played by the spindle pause (A'—B') and
Golgi tendon organ activation (A'—P') in relation to the resulting EMG re-
sponses (A—B and B—P, respectively).
Clearly, multiple factors are involved in the SP, and it would be useful to
simplify them if possible. By the use of phasic reflex contractions (tendon jerk
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or H-reflex) to produce the muscle twitch, antidromic factors may be eli-

minated along with some though not all of the cutaneous factors because the
stimuli responsible for an H-reflex and, to a lesser extent, those producing
a tendon jerk also produce phasic cutaneous input. Using these reflexes, how-
ever, one may be left with Renshaw and Golgi tendon organ inhibitory ac-
tivity, a pause in excitatory afferents from spindle, as well as other mechanisms
yet to be described. Submaximal isotonic contractions could minimize tendon
organ activity but would introduce afferent input from joint receptors pro-
duced by the movement. The use of the unloading reflex to produce a SP
[ΑNGEL, this volume] eliminates the putative burst of Renshaw and Golgi
tendon organ activity, as well as other antidromic factors, but again adds
quick joint movement to complicate the issue. The rebuttal that joint move-
ment otherwise, during voluntary elbow flexion or passively during certain
biceps contractions, produces no SP does not convince one that input from
joint movement under different `command' circumstances (í. e., the unloading
reflex) may not affect the SP. Since MERTON's original hypothesis, the simpli-
fied servo theory of muscle contraction has had to be modified. Nevertheless,
its basic truth remains irrefutable — the subject attempts, using complicated
and not altogether conscious means, to do as instructed — to maintain a certain
prescribed muscular tension. If this tension is exceeded by the superimposition
of a twitch, a SP is required to allow the tension to fall to the preordained
level. When the subject is instructed to produce a maximal contraction, there
is no need for relaxation and only the early antidromic portion of the SP is
seen. What the subject has been instructed to do determines the result one
obtains, and differences in instructions account, at least in part, for the re-
ported variability in the results of SP studies.
The mechanisms responsible for this reflex regulation, including the
`command program' given to the subject by the experimenter and delivered
to the spinal cord from higher centers, and their ineffectiveness during maxi-
mal effort or quick phasic movements (which can break into the SP at any
time), remain to be delineated. In the future, when this has been done, ab-
normalities in the SP associated with disease states may be used to infer some-
thing about the pathophysiology of the disease itself (rigidity, spasticity, trem-
or, etc.). Meanwhile, we can only make correlations between clinical states
and findings observed, for example, in the SP or other reflex tests, in well con-
trolled studies.
We remain in the natural history stage of Clinical Neurophysiology.
Though it is difficult to resist the urge to jump to conclusions about mech-
anisms of human disease on the basis of comparison between a few human
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 SHAHANJ/YOUNG 602

studies under poorly defined conditions and reports from animal experiments
carried out under artificially simplified conditions, we must resist. We should
concern ourselves with gathering data of a type which will remain useful as
our understanding evolves.

Summary

Studies of the normal human SP produced in many different muscles by electrical

stimuli have been carried out under carefully controlled conditions to analyze factors
influencing motoneurone excitability in man. The first 50 msec of electrical silence appear
to be produced by antidromic effects in motor axons, including possible Renshaw inhibition
during the latter 20 cosec or so. The last 50-70 msec of the SP is associated with changes in
CNS activity produced by proprioceptive and _cutaneous input from the twitch or its
stimulus. Purely cutaneous input is shown to produce a SP from 50 to 100 or more msec
after a single large stimulus, and the occurrence of a SP cannot, therefore, be taken to
establish the existence of γ or other proprioceptive routes of motoneurone excitation. A
pause in muscle spindle afferent input may account for much of the second half of the SP
which is shown to be absent in facial muscles where spindles have not been seen. The last
20 msec of the SP, because it depends upon the degree of tension in the muscles, may relate
to Golgi tendon organ activity. The importance of the hitherto ignored cutaneous mechan-
isms of the SP is stressed to caution against premature and egregious extrapolation from
alterations in the SP in various pathological situations to explanations of even more complex
phenomena such as spasticity, rigidity and tremor. There is obviously a variety of excitatory
and inhibitory influences on spinal motoneurones, and it is important to include all these
factors in any comprehensive theory of muscle control in man.

Acknowledgement

This work was supported by a grant from Mrs. W. B. Lτ.ovn. We wish to thank Mr.
FREDERICK E. Balm, Medical Research Council, for his help in building the myograph.

Authors' address: Dr. B. T. SΗnηnνι and Dr. R. R. YouiG, Department of Neurology,

Massachusetts General Hospital, Fruit street, Boston, ΜΑ 02114 (USA)
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