446
J. Physiol. (I956) I33, 446-455
A COMPARISON OF FLEXOR AND EXTENSOR REFLEXES
OF MUSCULAR ORIGIN
BY M. G. F. FUORTES AND D. H. HUBEL
From the Department of Neurophysiology, Walter Reed Army Institute of Research,
Walter Reed Army Medical Center, Washington 12, D.C.
(Received 10 April 1956)
Whereas extensor muscles of decerebrate mammalian preparations usually
present both phasic and tonic reflex contraction to stretch (Liddell & Sherrington, 1925), flexor muscles present phasic stretch reflexes only (Asayama, 1916).
Under anaesthesia or during spinal shock (Creed, Denny-Brown, Eccles,
Liddell & Sherrington, 1932, p. 51), tonic stretch reflexes are lost while phasic
responses are maintained. Extensor and flexor muscles then respond in
a similar way to applied stretch. The present research was undertaken with the
purpose of identifying the processes responsible for this difference between
flexor and extensor pathways. This appeared to be a convenient way of
approaching an understanding of the central events which underlie the
development of sustained reflex responses.
METHODS
The experiments were performed on thirty-two acutely decerebrate cats. Decerebration was
carried out under deep ether anaesthesia and additional anaesthetic was administered during the
subsequent surgical procedure if required. In all cases the experiments were performed after
recovery, as judged by restoration of such anaesthetic-sensitive reflex movements as flexor
withdrawal, extensor thrust, contralateral extensor reflex, etc. The lumbar enlargement of
the spinal cord was exposed and appropriate ventral roots were severed on one side near
the point of passage through the dura. Records were taken from L7 or S1 ventral roots or
from one of their filaments, with neighbouring ventral roots cut to prevent antidromic invasion.
The branches of the ipsilateral hamstring and gastrocnemius nerves were severed and their
proximal stumps were used for stimulation. Stimulation and recording were carried out in the
conventional way in most experiments, but in some a train of stimuli was used for conditioning
and a subsequent single shock for testing. This was done by using the first pulse of a doublechannel stimulator (Attree, 1950) as a gate for another stimulator supplying the train of
conditioning shocks, and the second pulse as a test stimulus (Fig. 1).
RESULTS
Responses to repetitive stimulation
In previous work (Alvord & Fuortes, 1953, fig. 8) it was found that in decerebrate preparations repetitive stimuli to extensor muscle afferent fibres
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FLEXOR AND EXTENSOR REFLEXES
insufficient to evoke reflex firing of extensor motoneurones when delivered at
a low frequency might evoke sustained firing if applied at higher frequencies.
It was noted that the firing evoked in this way was similar to that elicited in
the same motoneurones by sustained stretching of the muscle.
Fig. 1. Block diagram of stimulation arrangement when trains of conditioning stimuli were used.
Stimulator A provides two impulses separated by a variable delay: the first of these serves as
a gate for a single-channel stimulator B which provides a train of stimuli used for conditioning; the second provides the test stimulus. Below is shown a record led off from a small
filament of S I ventral root. A train of eight stimuli is used for conditioning one branch of the
hamstring nerve. The following test shock is applied to the second branch.
As illustrated in Fig. 2, different features are typical of flexor muscular
responses. A flexor motoneurone responds to single-shock stimulation of
a flexor muscular nerve with the discharge of a single impulse occurring after
monosynaptic delay (Lloyd, 1943; Alvord & Fuortes, 1954). With weak
repetitive shocks applied at a low frequency (e.g. 0.5/sec-1/sec) a response will
occur to some of the stimuli. Increase of stimulus strength causes an increase
in the ratio of number of reflex impulses to number of stimuli (probability of
firing) until eventually the motoneurone responds to each stimulus. If
frequency of stimulation is now increased (its strength being unchanged) this
ratio decreases. For a moderate increase of frequency (say from 1/sec to
2/sec) responses occur to some of the stimuli throughout the period of stimulation. At higher frequencies (10/sec-100/sec) the motoneurone responds only to
the first stimulus or to the first few stimuli, and usually no further impulses
break through even if the stimulation is maintained for a long time (Fuortes,
1954 c). While the greater effectiveness of the first stimulus is particularly
obvious for higher frequencies of stimulation, it is also often observed for slow
stimulation rates such as 0.5-1/sec, where the first of the stimuli usually evokes
PHYSIO. CXXXIII
29
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M. G. F. FUORTES AND D. H. HUBEL
a response even if probability of firing is quite low for the stimuli following the
first.
If frequency of stimulation is set at a high value (e.g. 100/sec) and the
voltage is gradually increased from zero, no firing at all results even if the final
voltage reaches or exceeds values which are effective in producing a response
when the stimulation is applied abruptly (Fig. 3).
Fig. 2. Reflex firing of a single motoneurone in response to stimuli to one branch of the hamstring
nerve. Records taken from a thin filament of a peripherally cut ventral root. Strength of
stimulation constant throughout; frequency 1, 10, 100/sec as indicated by artifacts. Time
1 sec.
These results are analogous to the findings obtained with flexor reflexes
evoked by stretch by Asayama (1916), who observed that flexor muscles react
with a short-lasting contraction to a pluck or to an abrupt stretch but do not
respond to a gradual increase in tension.
As noted in previous work (see, for example, Fuortes, 1954 b), sustained
responses are sensitive to many types of damage. Because of this it was
considered important to show that the unsustained character of flexor
muscular reflexes is not the consequence of the general factors which indiscriminately depress sustained responses. Fig. 4 illustrates the results obtained
in one of the experiments done for this purpose. A ventral root filament
containing axons of extensor and flexor units was selected for recording.
A flexor motoneurone contained in this filament responded to stimulation of
one branch of the hamstring nerve in the usual manner: it responded to all
shocks if these were delivered at 1/sec, but only to the first if stimulated at
10/sec or 100/sec. In contrast, extensor units in the same filament failed to
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449
FLEXOR AND EXTENSOR REFLEXES
respond to stimuli applied to one branch of the gastrocnemius nerve at 1/sec or
10/sec but readily responded if the frequency was raised to 100/sec.
In other experiments (Fig. 5) it was observed that flexor motoneurones which
respond only initially to repetitive stimulation of muscular nerves may present
sustained firing on stimulation of skin nerves or receptors.
A
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B
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..
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Fig. 3
Fig. 4
Fig. 3. Repetitive stimulation at 250/sec of one branch of hamstring nerve (lower beam), record
taken from a small filament of S 1 ventral root (upper beam). A, Stimulation applied abruptly;
B, intensity of stimulation gradually increased to a final value equalling that of A. Time 1 sec.
Fig. 4. Responses of flexor (A) and extensor (B) motoneurones to repetitive stimulation of
hamstring and gastrocnemius nerves respectively: all records taken within a short time from
a ventral root filament containing one unit responding to hamstring and a few units responding
to gastrocnemius nerve stimulation. Stimuli at 1, 10 and 100/sec indicated by artifacts.
Time 1 sec.
A
Fig. 5. Reflex firing of a motoneurone recorded from a ventral root filament and evoked by
stimulation of one branch of hamstring nerve at 10/sec in A and by pinching the skin of the
ipsilateral hindlimb in B. Time 1 sec.
29-2
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M. G. F. FUORTES AND D. H. HUBEL
These results show that the early failure of flexor reflexes of muscular origin
is not due to inherent inability of the preparation to produce sustained responses,
as is the case in anaesthetized preparations; and also, that it is not a necessary
feature of the flexor motoneurone. Rather, abrupt and unsustained responses
are a property of flexor muscular reflex pathways.
The different responses of flexor and extensor muscular pathways to repetitive stimulation show that volleys from flexor nerves contribute a condition
which tends to prevent firing, whereas volleys from extensor nerves result in
accumulation of a change which tends to facilitate a reflex response.
Excitability changes after one or more stimuli
In contrast with this conclusion derived from experiments employing
repetitive stimulation, previous results obtained by testing excitability
changes evoked on a motoneurone pool by a single impinging volley (Lloyd,
1946) have shown no differences between extensor and flexor pathways. This
finding was not confirmed in preparations such as the unanaesthetized
decerebrate, presenting unsustained reflexes of flexor but well-sustained
reflexes of extensor muscles.
The excitability cycle following a subliminal conditioning shock was determined in two ways: by recording from a large number of ventral root fibres and
measuring the height of the reflex spike resulting from the synchronous firing
of many units ('composite recording'), and by recording from a single motoneurone, determining its probability of firing in response to a given test shock
at various times after conditioning.
Typical results obtained with the first method are shown in Fig. 6. If
a conditioning shock subliminal for reflex activation is applied to a flexor
muscular nerve, the reflex spike elicited by a subsequent larger test shock to
the same or to another closely allied nerve is increased for some 15 msec, but
later is considerably decreased for a period which may greatly exceed 1 sec. In
extensor muscular reflex pathways the early facilitation may be more prolonged
but the subsequent depression is absent, or at least less pronounced. This is
only true in preparations presenting well-sustained extensor reflexes: if these
are unsustained (as happens under anaesthesia, spinal shock, surgical damage,
or under other circumstances escaping experimental control), then strong
depression is observed also in extensors.
The difference in properties of flexor and extensor muscular reflexes is
emphasized if a train of stimuli rather than a single stimulus is used for
conditioning (Fig. 1). With trains of 5 to 12 shocks delivered in a period of
50-75 msec, it was observed that in flexor reflex pathways facilitation reaches
a maximum after the first, second, or sometimes third stimulus, and then
decreases sharply. Conversely, facilitation builds up progressively in extensor
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451
FLEXOR AND EXTENSOR REFLEXES
pathways so that the effectiveness of a test stimulus is increased maximally
towards the end of the train. This is illustrated with composite recording in
Fig. 7.
As with single conditioning shocks, the difference between flexors and
extensors was evident only if extensor reflexes were well-sustained in experiments employing composite recording. Even in only moderately rigid preparations, however, a conspicuous difference was found between flexor and
A
I
0
B
C
D
0
50
100
msec
D
50
100
msec
Fig. 6. Amplitude of reflex spike recorded from a whole ventral root and evoked by stimuli
applied at different times after a subliminal conditioning shock. The horizontal line in each
record indicates the average height of response to test shock alone. Conditioning and test
stimuli applied to the same branch of the hamstring nerve in A and separate branches in C;
to the same branch of the gastrocnemius nerve in B, and separate branches in D.
extensor units selected for typical unsustained activity on the one hand and
for typical sustained activity on the other. Examples of the course of probability of firing of such units during and following conditioning with a train
of impulses are given in Fig. 8. Fig. 9 shows the course of probability of firing
following trains of different lengths, illustrating its decrease with increasing
train length for flexor pathways, as contrasted with its increase in the case of
extensors.
Consistent with these results, it was found that when the strength of the
train of conditioning stimuli was raised until it barely succeeded by itself in
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452
M. G. F. FUORTES AND D. H. HUBEL
exciting a flexor motoneurone, this discharged after one of the first three
stimuli (see Eccles & Rall, 1951), while extensor motoneurones discharged
after the last stimulus (Fig. 10).
A
A
1229 24 1410
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t-
08
.i
13 1110
I
21 10
3
I
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10
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B
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0
_ _. .A_
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20 30 40 50 60 msec
B
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8
i10
15
2
30
40
50
60
70 msec
15 15
15 15 1515 15 15 15 171515
cO
00
00
0
0
0
0
5
0.
0
60 msec
10 20 30 40 50 60 70 msec
3
40 50
Fig. 7
Fig. 8
Fig. 7. Amplitude of reflex spike recorded from a whole ventral root and evoked by stimuli
applied at different times during and after a subliminal (conditioning) train of shocks,
indicated by the vertical lines. The horizontal line in each record represents the average
height of response to test shock alone. Conditioning and test stimuli applied to the same
branch of the hamstring nerve in A and of the gastrocnemius nerve in B.
Fig. 8. Probability of firing of a single motoneurone in response to a test shock applied during and
after a subliminal (conditioning) train of stimuli. Probability of firing is expressed as the
ratio of number of responses obtained to number of stimuli at each time interval. The number
of applied stimuli at a given interval is indicated by the figure above each point. Probability
of firing in response to a test shock alone is indicated by the horizontal line in A, and was zero
in B. A, Conditioning and testing stimuli applied to one branch of the hamstring nerve;
B, same preparation as A, stimuli to one branch of the gastrocnemius nerve.
0
10. 20
DISCUSSION
Prior to this study identical changes have been described as occurring in
flexor and extensor muscular reflex arcs following their activation. It is
important to note that those properties of muscular reflexes which are
identical in flexor and extensor pathways cannot include features relevant to
production of rhythmical firing, since rhythmical responses can be obtained in
extensor pathways only. Therefore care should be exerted in applying conclusions derived from the study of so-called monosynaptic reflexes (see
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FLEXOR AND EXTENSOR REFLEXES
Alvord & Fuortes, 1953, p. 303) to the interpretation of the events occurring
during the normal movements brought about by repetitive firing of each
activated motoneurone.
A
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......... .
A
3
a
b
_
3
5
0
E
0
0
.....
0
_-
a"00
40
20
60 msec
Time, 10 msec
Fig. lO
Fig. 9. Same experimental arrangement as Fig. 8. Testing stimulus delivered after the end of
conditioning trains of stimuli at 300/sec, the numbers besiide the curves indicating the number
of impulses in a conditioning train. A, Stimuli to one branch of the hamstring nerve; B, same
preparation as A: stimuli to one branch of gastrocnemius nerve. Probability of firing in
response to a test shock alone was one in A and zero in B.
Fig. lO. Impulses recorded from a thin ventral root filament of a decerebrate cat in response to
a train of stimuli adjusited to be just threshold for reflex discharge. In A stimuli were applied
to one branch of the hamstring nerve, and in B to one branch of the gastrocnemius.
Fig. 9
According to the results obtained in the present research, different features
of temporal summation characterize flexor and exrtensor reflexres of muscular
origin. Pathways capable of responding with rhythmical firing present
exrtensive abilities for temporal summation. In these pathways, the facilitatory
effect exrerted by repetitive impingement builds up to a steady level which, in
the absence of motoneurone firing, can be maintained for a long time. In some
conditions, the build-up of facilitation can progressively increase over a considerable fraction of a second, explaining the long latency between start of
stimulation and the first reflex response observed on occasion in previous and
in the present work (see Alvord & Fuortes, 1953, figs. 6, 7 A and 8).
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M. G. F. FUORTES AND D. H. HUBEL
In pathways responding with typically unsustained discharge to repetitive
stimulation, excitability reached a peak within a few msec and decayed
thereafter, even in the absence of a reflex response. Consistently, reflex firing
could be elicited in these pathways after short latencies only.
The present work does not reveal the nature and location of the processes
responsible for the contrasting features of flexor and extensor reflexes. In
a previous study on the effects of direct currents on flexor and extensor
motoneurones (Fuortes, 1954a), some difference was found between the two
types of cells, but this would be insufficient to justify the sharp difference
between their responses to repetitive afferent stimulation. Some other property of primary afferent terminals or of the central links activated by
muscular stimulation in the two cases is likely to play a more important role.
Even without commitment as to the cause of the different features of flexor
and extensor reflex responses, it can be stated that the observed correlations
between time-course of facilitation and ability to respond with rhythmical
firing justify the conclusion that temporal summation of a change fitting
Sherrington's definition of central excitatory state (Creed et al. 1932, pp. 31,
32) is necessary for production of rhythmical reflexes.
SUMMARY
1. Reflex responses of flexor motoneurones to stimulation of hamstring
nerve have been compared with responses of extensor motoneurones to stimulation of gastrocnemius nerve in decerebrate cats.
2. Whereas firing of extensor motoneurones is often more easily evoked by
high than by low frequency of stimulation, flexor motoneurones responding to
each shock when stimulation frequency is low respond only initially to stimuli
delivered at higher frequencies.
3. Following a single conditioning shock to the hamstring nerve, the reflex
response to a subsequent test shock is increased for a period of about 15 msec,
but later is considerably decreased. In extensor pathways, the early facilitation may be longer and the late depression is either less pronounced or altogether
absent.
4. With a train of conditioning stimuli, facilitation increases to an early
maximum and soon decays in flexor pathways, but it builds up more or less
gradually to a steady state in extensor pathways.
5. It is thought that the properties of temporal summation found in
extensor pathways are necessary for production of sustained rhythmical reflex
responses.
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FLEXOR AND EXTENSOR REFLEXES
455
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