J. Physiol. (1976), 259, pp. 531-560 With 14 text-figurew Printed in Great Britain

531

STRETCH REFLEX AND SERVO ACTION IN A VARIETY OF HUMAN MUSCLES

BY C. D. MARSDEN, P. A. MERTON AND H. B. MORTON From the National Hospital, Queen Square, London WC1N 3BG, the Physiological Laboratory, Downing Street, Cambridge CB2 3EG, and the University Department of Neurology, Institute of Psychiatry and King's College Hospital, de Crespigny Park, London SE5 8AF

(Received 22 January 1976) SUMMARY

1. In the long flexor of the thumb the latency of the stretch reflex and of other manifestations of servo action is some 45 msec, roughly double the latency of a finger jerk. 2. Tendon jerks are feeble or absent in the long flexor of the thumb even in subjects with brisk long-latency stretch reflexes in this muscle. This, and other facts, suggests that the nervous mechanism of the tendon jerk is different from that of the stretch reflex. 3. A muscle that has feeble tendon jerks may show a late component in the response to a tendon tap, with a latency similar to that of the longlatency stretch reflex. 4. On the hypothesis that the excess latency of the stretch reflex over that of a tendon jerk is because the stretch reflex employs a cortical rather than a spinal arc, the excess would be expected to be larger in magnitude for the long flexor of the big toe and smaller for the jaw closing muscles. This is confirmed. 5. An alternative hypothesis that the long latency of stretch reflexes in thumb and toe is because they are excited by slow-conducting afferents is made improbable by the finding that stretch reflexes with an equal or greater excess latency are also found in proximal arm muscles. 6. The long-latency stretch reflex in proximal muscles was seen most distinctly in a healthy -subject who happened to have feeble or absent tendon jerks. In ordinary subjects there is often a large, short-latency, presumably spinal component of the stretch reflex in proximal muscles; and short-latency responses to halt and release are also seen. The significance of this spinal latency servo action in proximal muscles remains to be explored. 7. The Discussion argues that the available data on conduction time to

532 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON and from the cerebral cortex are compatible with the hypothesis that the long-latency component of the stretch reflex uses a transcortical reflex arc, and that none of the experiments described in the present paper are inimical to this view. INTRODUCTION

An earlier paper (Marsden, Merton & Morton, 1976) described servo-like responses in the long flexor of the thumb and gave some of their properties. A singular feature of these responses was their uniformly long latency relative to the tendon jerk time in forearm muscles. The finger jerk latency is about 25 msec and is presumably a measure of the time round the simple monosynaptic spinal reflex arc in the fastest afferent and efferent fibres. Servo responses take roughly twice as long as this. There are plenty of possible reasons why this might be; mechanical lags in soft and compliant tissues are likely to contribute, while, on the nervous side, servo responses might, for example, use polysynaptic spinal pathways; or alternatively slowly conducting 'secondary' spindle afferents, which are believed to contribute to the spinal stretch reflex (Matthews, 1972; McGrath & Matthews, 1973; Kirkwood & Sears, 1974, 1975) might be dominant in these conditions, instead of the fast-conducting primary spindle afferents which excite tendon jerks. A -more radical hypothesis is that servo responses have a long latency because they employ a supraspinal stretch reflex arc, with extra time needed for conduction to and from the brain. This possibility seems first to have been suggested by Hammond (1960) to explain the long latency of the stretch responses he discovered in his pioneer work on the human biceps. Later, Phillips (1969), impressed by the existence of a fast pathway for primary spindle afferents to the cerebral cortex and a fast monosynaptic corticospinal pathway back to hand motoneurones in the baboon, wondered whether there might be a stretch reflex in primates via the cerebral cortex. In this paper we give evidence that the nervous mechanism of servo action is different from that of the tendon jerk, so that it does indeed require a special explanation. The idea of a transcortical servo loop in man is attractive for a number of reasons (Marsden, Merton & Morton, 1972, 1973a), but it is difficult to get positive evidence in favour of it. We can, however, follow out some of the consequences of the theory and test them to see if it survives. Some of the results have already been published in preliminary form (Marsden, Merton & Morton, 1973b, 1975).

SERVO ACTION IN VARIOUS HUMAN MUSCLES

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METHODS The general technique for recording, in one experimental run, the responses of a muscle to unexpected stretch, halt or release in the course of a series of voluntary tracking movements were the same as in the earlier paper on the thumb (Marsden et al. 1976). The resultant superimposed integrated electromyographic records we call 'tulips'. The only modifications required in the equipment for use on muscles other than the thumb flexor were in the arrangements for taking the pull of the muscle in use to the low-inertia electric motor that opposed it and applied perturbations during the movement. For the great toe little had to be done, for that of the two principal subjects C.D.M. and P.A.M. could be got with some little trouble into the clamp intended for the thumb. The long flexor works on the terminal phalanx and, when this flexed, the pad of the great toe bore on the thumbstick in the ordinary way. To be at a convenient height the subject sat on a high table. For leading off the electromyogram of the flexor hallucis longus one electrode was 3 cm behind and 3 cm above the medial malleolus and the other 6 cm above the lateral malleolus behind the fibula. For the jaw closing muscles, masseter and temporalis, the subject rested his upper teeth in a groove on a horizontal bar fixed to the frame. A lever 5 cm long carried on the motor spindle in place of the thumbstick pushed the lower jaw downwards by bearing on the lower teeth. When the contact arm was against the backstop, the teeth were about 4 cm apart. The subject's task was to close his teeth at a smooth rate. The muscles are strong and the inertia of the jaw high, compared to the thumb or toe, so the largest possible motor currents had to be employed to get reasonable rates of stretch. One recording electrode was over the zygoma, 6 cm in front of the auditory meatus; the electrode for masseter was 4 cm vertically below this one, and that for temporalis was 4 cm above. For the infraspinatus a pulley of diameter 6 cm, used as a winch drum, was fixed to the motor spindle in place of the thumbstick. A length of flexible steel cable was anchored to the pulley, taken round it for a turn and then run off to the subject's wrist, where it ended in a loop. The subject sat on the board carrying the motor with his back to the motor and his right forearm held horizontally across his abdomen. The palm of the hand was vertical, facing backwards, with fingers lightly flexed. The loop of wire went round the wrist at the level of the heads of the radius and ulnar. It was prevented from cutting into the skin by an incomplete band of aluminium shaped to fit the bone heads. Both the band and the wire loop were held in place by surgical tape. The wire to the pulley passed close to the subject's left iliac crest. The demanded movement was a smooth rotation of the near-vertical humerus, carrying the wrist away from the body as in a backhand stroke at tennis. This movement employs the infraspinatus muscle. As a fulcrum the medial epicondyle of the right humerus rested in a cup carried on the main frame. To avoid moving the display cathode ray tube, used for tracking, which was now behind the subject, he viewed it in a mirror. One recording electrode was 3 cm from the medial edge of the scapula and 4 cm below the spine, the other was 4 cm lateral to the first and 3 cm below the spine. In a few experiments a bipolar needle electrode, inserted between these sites, was employed. With the largest motor current (17 A) the tension in the wire was 3-4 kg (35 N). When this was suddenly applied the wire extended slightly and the pull compressed the skin at the wrist. These various sources of give cause an initial step, lasting some 5 msec, to be seen in some displacement records of stretch reflexes, e.g. Fig. 9 B. For pectoralis the motor was to the right of the subject and the movement was adduction of the humerus, held slightly forward so that the elbow could pass some

534 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON way across the abdomen. The same pulley and wire were used. In some experiments the subject sat, the elbow was fully flexed with the forearm held to the upper arm by a strap and the pull was taken by hitching the wire loop over the medial epicondyle (protected with surgical tape) and the head of the ulnar. In other runs the subject stood with his elbow extended and the wire loop took the pull around the wrist at the level of the heads of the ulnar and radius with a wrist band, etc, as for infraspinatus. The palm of the hand faced away from the motor. One recording electrode was 6 cm from the mid line at the level of the second rib and the other electrode 4 cm lateral to the first in the direction of the fibres of the pectoralis major. For biceps the subject sat facing the equipment with the pulley in front of his right shoulder. His upper arm sloped straight forwards and downwards to rest on a board, which was an extension of the board with the motor on it. The olecranon was prevented from moving forwards by a wooden chock fixed to the board. When the contact arm on the motor spindle was against the backstop, the elbow was flexed roughly to a right angle. The palm of the hand faced the shoulder. The wire loop to the pulley was round a wristband at the level of the heads of the ulnar and radius. The task was smooth flexion of the elbow. Electrodes 4 cm apart were applied over the belly of the biceps. Tendon jerks were elicited using a hammer with a microswitch in it for triggering the recording sweep. The striking face was a light plastic member hinged to the hammer body that had to move back about 1 mm to open the switch in the body of the hammer. The light plastic member came to the end of its travel immediately afterwards. By mounting an old gramophone pick-up on the striking face it was ascertained that the interval between the pick-up first touching the skin and the operation of the microswitch was about a millisecond with blows of average violence, as used for eliciting jerks. This was confirmed by striking the thumbstick (held stationary) with the bare hammer and observing the delay between the first rise of force, signalled by the force transducer on the thumbstick, and the time of opening of the microswitch. A computer programme, using a continuously running memory, which allowed events before the trigger pulse from the microswitch to be inspected, was used for this measurement. A delay of a millisecond or so between first contact and the opening of the microswitch corresponds to a velocity of about 1 m/sec for the head of hammer, which is reasonable. When the hammer struck the thumbstick more slowly longer intervals were observed. It is of interest that varying the rate of the hammer blow over a wide range did not observably alter the latency of a finger jerk, measured from the time of opening of the microswitch, although the interval between first contact with the skin and the opening of the switch must have altered by several milliseconds. This suggests that there is insufficient inertia in the hinged plastic member to stretch the muscles. The opening of the microswitch corresponds closely with the moment when the full weight of the hammer comes behind the blow and this apparently is what counts. In another method of eliciting finger and thumb jerks, the tip of the digit was flicked by the experimenter snapping his middle finger (Hoffmann's reflex). To trigger the recording sweep at the moment of contact, electrodes were applied to the hands of both the experimenter and the subject and a trigger pulse was obtained when a circuit was completed by the experimenter's finger touching the subject, whose digit was lightly smeared with electrode jelly. The latency of finger jerks obtained in this way was 2-3 msec longer than when the hammer was used and the latency was measured from the opening of the microswitch. It would thus be similar to the latency of a finger jerk from a slow hammer blow, if the start were to be taken from the time of first contact of the hammer with the skin. It is not obvious which measure should be taken as the true latency of the jerk.

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535

Because it is invariant with hammer velocity over the ordinary clinical range of velocities and is easily measured, we give the figures obtained with the hammer in this paper, unless otherwise noted. If it is preferred to measure latencies from first contact with the skin, 1-3 msec must be added to our figures. The arguments based on them are not affected. Subject. Most experiments were performed, as in the earlier paper, on two of the authors, but in addition we had two experimental sessions with a special subject, L.B.W., whose tendon jerks were almost absent. He was a Cambridge medical student aged 20 at the time of the investigations. At about the age of 15 he had been found to have no tendon jerks at a routine school medical examination. This was confirmed by ordinary testing in 1972, but later a flicker of a jerk in biceps was seen with intense Jendrassik-type reinforcement, another jerks being absent on similar clinical testing. With electrical recording, small finger jerk action potentials were seen without a visible mechanical twitch, and jerk potentials were also detected in infraspinatus with reinforcement. The biceps jerks were also recorded electrically. The records from these three muscles are shown in Figs. 1, 8, 11 and 13. The jerk latencies are normal, so there can be no abnormality in either sensory or motor conduction velocities. Pupillary responses to light and accommodation were normal, ruling out the full-blown Holmes-Adie syndrome. The subject had no motor or sensory symptoms, he took part in games successfully, played the flute and appeared in every way healthy. RESULTS

Flexor pollwic longu8 In previous writings (and in Fig. 1B of this paper) we compare the unexpectedly long latency of a tulip in flexor pollicis longus (40-50 msec) with the latency of a finger jerk (20-25 msec) recorded through the same electrodes, taking the jerk latency as an estimate of the spinal monosynaptic reflex time for muscles at that level in the forearm. There is no hint of a response in the tulip at tendon jerk latency, and this is true even with high initial loads (e.g. Fig. 3 of this paper and figs. 13, 14 and 15 of Marsden et at. 1976) which are known from the work of Upton, McComas & Sica (1971) to potentiate spinal monosynaptic reflexes. Our estimate of the time to and from the spinal cord has now been checked in both the principal subjects by recording F waves, through electrodes over flexor pollicis longus, to maximal stimulation of the median nerve at the elbow. The latency of the F wave plus the latency of the direct action potential evoked by the shock gives a measure of twice the motor conduction time from the cord to the muscle which (as is known from comparison of H reflex and F wave latencies in other sites) approximates to the reflex conduction time.

The reason for using the finger jerk for our primary comparison is that finger jerks are simple to obtain and record, whereas a tendon jerk in the thumb flexor itself is conspicuously difficult to elicit, in fact previously we thought it impossible. We return to the question of thumb jerks later but we wish now to make the point that this very difficulty in evoking thumb jerks even by extending the terminal phalanx as rapidly as possible, suggests at once that 'tulips', in which the rates of stretch are much less,

536 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON are (quite apart from their long latency) not likely to be based on the same reflex arc as the tendon jerk. Further evidence of the same tendency is that normal tulips are seen when not only the thumb jerk but all clinical tendon jerks are effectively absent. The special subject L.B.W., who was A

0

B

/0

250 msec Fig. 1. Servo responses in the long flexor of the thumb, contrasted with finger jerks. A, in subject L.B.W. (2 March 1974). B, in subject P.A.M. (3 March 1974). For each subject, tendon jerks (each the average of thirty-two raw action potentials, i.e. not rectified or integrated) are shown above the 'tulips' as insets, the amplification for L.B.W. being 8 times greater than for P.A.M. The main records in the upper half in A and in B are superimposed rectified and integrated electromyograms of the response of the muscle to an unexpected halt, stretch or release in the course of a smooth flexion movement, compared with a control. Initial force, in both cases, 540 g (5 3 N). Each trace is the average of thirty-two trials (four successive experiments each of 8 trials of each variety). Such records are referred to as 'tulips'; for further details see Marsden et al. (1976). The traces below are the corresponding records of angular displacement of the terminal phalanx of the thumb, taken simultaneously with the electromyograms. The timing lines are at the time of imposition of perturbations, at 50 msec later, and also at the tendon jerk latency (22 msec for L.B.W. and 25 msec for P.A.M.). The peak to peak amplitude of the first component of the tendon jerk (the component starting at 22 msec) in L.B.W. is 73 1V; the amplitude in P.A.M. is 800 ,itV. Tendon jerks were elicited in the ordinary clinical manner. The subject lightly flexed his fingers against the experimenter's fingers and the experimenter then struck his own fingers with the tendon hammer. The displacement and integrated electromyogram calibrations apply to both sets of records. The time scale is common to all the records, including the tendon jerks. The tendon jerk recording sweeps are plotted to start at the time of imposition of perturbations in the tulips.

~ An

SERVO ACTION IN VARIOUS HUMAN MUSCLES 537 almost without tendon jerks (see Methods), gave normal tulips from his long thumb flexor. A careful comparison of his thumb tulips with a series done under precisely similar conditions in P.A.M. (all of whose ordinary clinical tendon jerks are normal) is shown in Fig. 1. The two are very similar, so the presence or virtual absence of all tendon jerks makes no obvious difference to thumb tulips. A

0

B/

40

250 msec

Fig. 2. The relatively constant latency of the stretch reflex in the long flexor of the thumb with different rates of stretch. A, in subject C.D.M.; two different currents used to produce different rates of stretch (17 November 1974). B, in subject P.A.M., 'slugged' and 'unslugged' stretches compared (17 November 1974). Initial force, in both cases, 540 g (5.3 N). In each set the top pair of traces are the integrated electromyograms, the middle pair are the rectified and smoothed electromyograms (with zero base lines drawn in) and the bottom pair are displacement records, showing in each case fast and slow stretches. In each trial the three variables were recorded simultaneously. Each trace shown is the average of eight trials. Eight fast stretches and eight slow stretches were presented in succession, without controls. In B, the response to the slowed stretch is the smaller and later record. The timing lines are at the time stretch starts and 40 msec later. The time and displacement calibrations apply to both sets of records. The calibration bar for the top traces is equal to 10 ,W . sec for A and 5 /zV . sec for B. For the rectified electromyogram the calibration bar is equal to 200 #eV for A and 100 1sV for B.

No doubt the long latency of a tulip, relative to a tendon jerk, does owe something to the fact that stretch is applied much more abruptly in the case of a jerk; but this factor turns out to be less important than might be expected. The most immediate indication of this is that in a tulip the latency of the stretch reflex component is approximately the same as the

538 0. D. MARSDEN, P. A. MERTON AND H. B. MORTON latency of the response to the halt, which can be regarded as a stretch of zero velocity (see, for example, Fig. 3). In confirmation of this, Fig. 2 shows the remarkably similar latency of the stretch reflex to two velocities of stretching in C.D.M. and P.A.M., records which are in every way typical. In the case of P.A.M. where the slow stretch was produced by 'slugging' the rate of rise of motor current with a condenser, the lag in starting the stretch is reflected in a small increase in reflex latency. (In the earlier paper also (Marsden et al. 1976) it was shown in fig. 15B that High force

Slugged

]A

Unslugged

4

Low force

Slugged

Unslugged

10

Fig. 3. The relatively constant latency of 'slugged' and 'unslugged' tulips in the long flexor of the thumb. The lower half of the Figure shows records made at the standard low initial force, roughly 120 g (1-2 N) at the pad of the thumb (see Marsden et al. 1976). Each trace is the average of eight, with 'random cyclic' presentation of perturbations and controls. Tulips, rectified electromyograms and displacement records for the slugged condition are shown in the upper row with those for the unslugged condition in the row below. Timing lines at 50 msec after the imposition of perturbations. The top half of the Figure shows the same thing with the initial force 4-5 times greater. The displacement calibration applies throughout. There are separate electrical calibrations for the upper and lower sets of records. The sweep time is 250 msec. The records also demonstrate change of gain in proportion to load (see Marsden et al. 1976). Subject P.A.M. (10 October 1972).

SERVO ACTION IN VARIOUS HUMAN MUSCLES 539 even greatly slowed stretches gave reflex responses that were not greatly delayed or diminished in size.) In a full tulip, we have made a careful comparison of the latencies at both low and high forces when the tulips were obtained in the ordinary way and when the 0 47/,F condensers normally used to blunt the rate of change of current in the stretch and release trials had been removed (Fig. 3). The longest latency was with the 'slugged' tulip at the low force, but it was only some 10 msec longer than the shortest latency, which is in the 'unslugged' tulip at the higher force, although the displacement records show that the start of the perturbations was much sharper without the slugs. Thus, within the range so far used, the rapidity of onset of the perturbations does not closely govern the latency of a tulip. However, if stretch reflexes are elicited with faster and faster stretches, the response does eventually begin earlier; but what appears to be happening here is that a new component is coming in in front of the ordinary stretch response seen in a conventional tulip. This is suggested by Fig. 4A and B, which give (on a fast time base) the stretch responses to four different rates of stretch in C.D.M. The appearance is of a component in all four responses at 40 msec, with another component coming in earlier at the fastest rate of stretch. (In subject P.A.M. all the responses are smaller and the early component is difficult to distinguish.) On the provisional interpretation of the late component as a cortical, or, at any rate, a supra-spinal reflex, the earlier component in C.D.M. would presumably represent a spinal response. With this possible interpretation in mind we tried to see whether we could remove the spinal component by rendering the motoneurones partially refractory by a preceding tendon jerk. Fig. 4C shows that this can apparently be done. It gives the superimposed results of three experiments in which stretch reflexes to the fastest stretch were compared with responses (labelled S + J) in which a finger jerk had been elicited 30 msec before the thumb stretch. As can be seen, the tendon jerk removes the early component and leaves only the late component at 40 msec. Further evidence relevant to this point is given later in the section on double tendon jerks. There are two alternative interpretations of this experiment. It is observed that flicking the pad of the thumb, in the manner to obtain a tendon jerk by the method of Hoffmann, is seldom successful, but not infrequently when the thumb is flicked the index and other fingers will respond with a jerk. Conversely flicking the index or middle fingers -will often give a jerk in the thumb. Hence the early component seen after rapid stretch of the thumb in the machine may in fact be in finger flexors, rather than in flexor pollicis longus. If, on the other hand, it is in flexor pollicis longus, the motoneurones of this muscle may equally well be excited and rendered refractory by the finger jerk. In either case, then, the finger jerk will involve the relevant motoneurones. The distinction is not important for present purposes. We are only concerned to show that the early component, in whatever muscle it is occurring, can be removed by a preceding finger jerk, to reveal the late component in flexor pollicis

540 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON longus uncontaminated in fast stretches. Analogous results are given later on infraspinatus in subject L.B.W. For comparison Fig. 4D gives the reflex response to fast extension of the terminal phalanx of the index finger, a muscle known, in this subject, to have a brisk finger jerk. Stretch of the flexors of the index finger gives a response which we identify as a finger jerk, the start of which corresponds in time closely with the early response seen in the thumb records in B and C: It thus supports the proposed interpretation of the latter.

I0r4 A

B

C

p-

D

I

100 msec

Fig. 4. For legend see facing page.

9

SERVO ACTION IN VARIOUS HUMAN MUSCLES

541

The long flexors of the middle and ring fingers Although finger jerks are easily obtained in both C.D.M. and P.A.M., tulips closely similar to those obtained from the thumb, with no hint of a response at jerk latencies, have been recorded from the ring finger of C.D.M. and the middle finger of P.A.M. (Fig. 5). Long latency tulips are, therefore, not confined to muscles with feeble or absent tendon jerks. The purpose of the experiments described up to now is to establish that the long latency of a tulip in the thumb or in the fingers, about double that of the tendon jerk, is a genuine phenomenon, not to be written off in terms of mechanical lags. Earlier responses to rapid stretch can be obtained, with ease in the fingers, with difficulty (or not at all) in the thumb, but they are probably of a different origin from the responses seen in a tulip, which appear at the same latency in muscles with and without tendon jerks.

Flexor hallucis longus If the excess latency of a thumb tulip over that of a spinal tendon jerk is to be attributed to the time taken for impulses to travel to the brain and back, the excess should be longer for muscles whose spinal motoneurones are further from the brain than those of the hand muscles, and shorter for those whose motoneurones are in the brain. We accordingly looked at tulips from the long flexor of the big toe and from the jaw muscles. Fig. 4. Reflex responses in subject C.D.M. to stretch at various rates in the long flexor of the thumb and in the long flexor of the index finger. Sweep duration 100 msec. Initial force 450 g (4.4 N) throughout. A, records of angular displacement of the terminal phalanx of the thumb during stretch at 4 different rates numbered 1-4. At the faster rates the contact arm on the motor spindle (see Marsden et al. 1976) hits the backstop and bounces. Stretch starts at the beginning of the sweep but the increased current is only left on for 50 msec, which is why the thumb begins to flex again midway. Each trace is the average of eight trials. B, the electrical responses, correspondingly numbered, from flexor pollicis longus, with the usual leads. The electromyogram has been rectified and smoothed with a time constant of 3 msec. The timing lines are 25 and 40 msec after the time of imposition of stretch (16 September 1972). (C, responses in flexor pollicis longus to stretch at the fastest rate shown in A. Each trace, as usual, is the average of eight trials. In three runs the stretch was preceded by a finger jerk and in three it was not. The records with the finger jerk are labelled S + J. The finger jerk was elicited 30 msec before the start of the sweep by striking a 12 in. ruler held against the tips of the subject's fingers, with his hand clamped in the equipment in the usual way (17 September 1972). D, a record from the long flexor of the index finger during rapid extension of the distal phalanx. The middle phalanx was held in the clamp. The displacement record was similar to the fastest shown in A (the experiment was performed immediately before that shown in A and B).

542 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON The big toe takes the place of the thumb in the equipment, as described in Methods. Tulips, however, are not so easily obtained. It needs a good deal of practice to track smoothly with the toe. To start with it moves in irregular jerks no matter how hard the subject tries to move it smoothly. In addition, it may well be that, even when reasonable tracking has been achieved, training is necessary to develop the responses seen in a tulip.

250 msec

Fig. 5. Tulips from the ring and middle fingers. Initial force 120 g (1.2 N). A, subject C.D.M.; the middle phalanx of the ring finger was held in the clamp and the movement was flexion of the terminal phalanx. Recording electrodes were 4 cm apart on the flexor in the upper part of the forearm. Seven runs, with eight trials of each kind, were done and averaged; thus each trace is the average of fifty-six trials (5 March 1972). B, subject P.A.M., middle finger; in this case the proximal phalanx was clamped. The clamp was moved backwards, towards the subject, so that the pad of middle finger bore on the thumbstick. The electrodes were 4 cm apart over the flexor of the middle finger in the forearm. Four runs were done, so each trace is the average of thirty-two trials (15 September 1972). The time base for both sets was 250 msec. The displacement calibration gives the angular movement of the terminal phalanx of the ring finger, but for the middle finger the total angular movement of the interphalangeal joints was less than the calibration indicates, because the proximal joint was now behind the axis of the motor. The upper calibration bar is equal to 10 ,sV. sec for A and 0 8 sV. sec for B.

This is clearly not the case with the thumb; but possibly the thumb is to be regarded as trained to start with. At all events it took many hours of work to get tolerable tulips from the big toe. The results for C.D.M. and P.A.M. are given in Fig. 6. The latencies, from the time of imposition of perturbations, are about 75 msec in C.D.M. and 90 msec in P.A.M. No tendon jerks were ever reliably obtained by striking or flicking the

SERVO ACTION IN VARIOUS HUMAN MUSCLES 543 great toe itself in either subject, a finding which, as in the case of the thumb, strongly suggests that the tulip is not based on the same nervous pathway as a tendon jerk. The spinal reflex times for muscles at that level were estimated by striking the ball of the foot with the tendon hammer to elicit an ankle jerk and recording the resulting reflex response through the same electrodes A

B

500 msec

Fig. 6. Tulips in the long flexor of the big toe, contrasted with ankle jerks. Time base 500 msec. A, in subject P.A.M.; the record shown is the average of nine runs each with sixteen trials of each variety, so each trace is the average of 144 trials (26 July 1972). B, in subject C.D.M., the average of six runs giving ninety-six averaged for each trace (29 July 1972). Initial force, in both cases, 400 g (3-9 N). The ankle jerk action potentials are shown as insets; the start of the sweep is placed above the time of imposition of perturbations in the tulips. Each jerk action potential is the average of eight. The mean peak to peak height is 480 #sV for P.A.M. and 380 1sV for C.D.M. The timing lines are at the time of imposition of perturbations and at the ankle jerk and tulip latencies (45 and 90 msec in P.A.M.; 38 and 75 msec in C.D.M.). The time and displacement calibrations apply throughout. The integrated electromyogram calibration bar is equal to 10 sV. sec for A and 5 WV. sec for B.

used for the tulips. The figures were 38 msec for C.D.M. and 45 msec for P.A.M. As a precaution the time to and from the cord was also estimated from the H reflex and the F wave produced by stimulating the medial popliteal nerve behind the knee, with generally concordant results. The H reflex latency was 36 msec in C.D.M. and 45 msec in P.A.M. The ankle

C. D. MARSDEN, P. A. MERTON AND H. B. MORTON jerk latencies give excess times for the tulip over the tendon jerk of 37 msec for C.D.M. and 45 msec for P.A.M. - decidedly longer than the figures for the thumb. The recorded jerks are shown as insets in Fig. 6. Jaw muscles The modifications to the apparatus necessary to study servo responses in masseter and temporalis during jaw closure have been described in Methods. Smooth tracking is not so difficult to achieve as it is with the 544

A

B

IL!

125 msec

Fig. 7. Tulips in the jaw closing muscles, contrasted with jaw jerks. Time base 125 msec. A, subject P.A.M., electrodes over temporalis; the average of four runs giving thirty-two trials to each trace (30 July 1972). B, subject C.D.M., electrodes over masseter; the average of nine runs giving seventytwo trials to each trace (30 July 1972). Initial force, in both cases, 200 g (2-0 N). The action potentials of the jaw jerks have been rectified and integrated and are shown as insets; for the jerk in A the trace is the average of eight and the electrical gain is the same as for the tulip; for B the trace is the average of thirty-two and it is plotted at 4 times the gain for the tulip. In this experiment perturbations were applied at the start of the sweep. The time calibration applies throughout. The displacement calibration, which also applies to both sets, is in millimetres of separation of the upper and lower teeth. The electrical calibration is equal to 1 isV. sec for A and 2 #V. sec for the tulip in B.

big toe. Tulips obtained on P.A.M. and C.D.M. are shown in Fig. 7. In these experiments the sweep lasted 125 msec, and perturbations were applied at the start. The latencies of the tulips are about 14 msec in P.A.M. and 12 msec in C.D.M. Jaw jerks were elicited in the conventional clinical manner. The latencies were about 8 msec in P.A.M. and 7 msec in C.D.M. From these figures we see that the excess latencies for the tulips over the

SERVO ACTION IN VARIOUS HUMAN MUSCLES

545 jaw jerks were some 6 msec in P.A.M. and 5 msec in C.D.M. Jaw jerks, recorded through the same electrodes as the tulips, are also shown as insets in Fig. 7. The diphasic waves of the jerks have, in this instance, been rectified and integrated in the same manner as the tulip records, to assist comparison of latencies. Lamarre & Lund (1975) describe burst-like responses in masseter to halting during jaw closure, occurring at jaw jerk latencies. Our integrated halt records, however, rise smoothly, with no evidence of an early burst. This discrepancy is a matter for further investigation; it may be relevant that in P.A.M. in particular, the jaw jerk, recorded electromyographically, was feeble or often absent, as it is clinically in many normal people.

Sensory evoked responses Using the methods and electrode placements of Giblin (1964) we measured the latencies of the cortical evoked responses - an important check for the transcortical theory. In C.D.M., stimulating the median nerve at the elbow, the time to the peak of the first negative going wave (Giblin's 'initial negative') was 16 msec, a normal value. With the same stimulus the latency of the muscle action potential from the usual electrodes over flexor pollicis longus was 3 msec, giving an estimate for the conduction time from muscle to cortex of 19 msec. For P.A.M. the corresponding figures were 17 msec and 4 msec, a total of 21 msec. Doubling these conduction times to give estimates of the time from the muscle to the cortex and back we obtain 38 and 42 msec. Both these figures are less than the observed latencies of the stretch reflex and the tulip in the two subjects and the difference of 4 msec accords with the fact P.A.M. is taller and leaner than C.D.M. They tally roughly with the longer latency often observed in tulips and in the stretch reflex in P.A.M. as compared with C.D.M. (see e.g. Marsden et at. 1976, fig. 7 and fig. 15C). For the leg, stimulating the medial popliteal nerve behind the knee, C.D.M. gave 34 msec to the first positive going peak of the evoked response, a normal value, and 7 msec for the muscle action potential latency (with the usual electrode positions at the ankle), a total of 41 msec. The figures for P.A.M. were 39 msec and 8 msec, total 47 msec. The double figures giving the estimated transcortical times are therefore 82 and 94 msec. The difference between these two (12 msec) fits well with the observed difference in the latency of the tulips in C.D.M. and P.A.M., about 15 msec (Fig. 6), but the absolute values are rather greater than the observed latencies of the tulips (75 and 90 msec). In C.D.M. the onset of the evoked response was at 25 msec (in agreement with Giblin); a calculation based on this would have reduced the estimated transcortical loop time to 64 msec; but the onset was not clear-cut in the records from P.A.M. and so could not be used for a comparison. 20

PHY 259

546 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON We conclude that, broadly speaking, both for arm and leg, the evoked response data do not conflict with the tulip latencies in the two subjects and are generally consistent with the transcortical hypothesis.

Infraspinatus The results for the toe, thumb and jaw have confirmed that the excess latency of a tulip over the latency of a tendon jerk is related to the distance of the motoneurones in question from the brain, but, as it so happens, in each case with the muscles we have used the latency of the tulip is roughly double the jerk latency. An alternative interpretation of the results is, therefore, that tulips, like tendon jerks, are spinal, but employ more slowly conducting afferents than tendon jerks, e.g. the spindle secondary endings. To investigate this possibility we looked at the proximal muscles in the arm. If the excess latency is due to conduction to and from the brain it should, on the present assumptions, remain the same for muscles close to the spinal cord as it is for distal muscles. On the other hand if the excess latency is due to the use of slowly conducting afferents it should diminish for proximal muscles in proportion to the diminution in jerk latency. In the event the answer obtained is not straightforward because proximal arm muscles give early responses which, from their latency, are almost certainly of spinal origin. Spinal responses identified as tendon jerks were seen by Hammond (1960) when he stretched biceps. For our purposes a muscle as close to the spinal cord as possible was desired. Most experiments have been done on infraspinatus, in which the tendon jerk latency was about 13 msec, half the latency of a finger jerk. Jerks were elicited by flexing the elbow to a right angle and striking the wrist with a tendon hammer in such a manner as to rotate the humerus on its long axis and stretch infraspinatus. Tulips from infraspinatus in three subjects are shown in Fig. 8. Details of the task are given in Methods. In C.D.M. (Fig. 8A) there is a response to stretch at about 15 msec (i.e. close to the tendon jerk latency) followed by a second and larger increase of activity at 40 msec. The responses to halt and to release are also both accentuated at about 40 msec. In P.A.M. (Fig. 8B) the response to stretch at about 15 msec is much larger and is not clearly marked off from what follows, but the main halt and release responses are at the longer latency. In L.B.W., the subject with exiguous tendon jerks, there is almost no response before a brisk stretch reflex at 40 msec (Fig. 8 C). These results suggest that the tulip responses in infraspinatus are in two components, a spinal component at roughly tendon jerk latency and a late component which would correspond to the servo responses in the long flexor of the thumb.

SERVO ACTION IN VARIOUS HUMAN MUSCLES A

547

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Fig. 8. Tulips in infraspinatus, contrasted with 'tendon' jerks. A, subject C.D.M., records from a concentric needle electrode (see Methods), the average of three runs giving twenty-four trials to each trace (27 January 1974). B, subject P.A.M., surface electrodes (see Methods), the average of four runs giving thirty-two trials to each trace (3 March 1974). CT, subject L.B.W., surface electrodes, the average of six runs giving forty-eight trials to each trace (2 March 1974). Rectified and smoothed records are given as well as integrated. Initial force in wire 700 g (6-9 N) for all three subjects. The 'tendon' jerks are shown as insets, on the same time base, with the start arranged to coincide with the time of imposition of perturbations in the tulips. The jerk action potential in A is the average of eight and the peak to peak height is 380 1sV; in B it is the average of eight and the height is 730 1sV; in C it is the average of sixty-four and the height of the first component is 90 /aV. The timing lines are at the time of imposition of perturbations and 13 and 40 msec later. The integrated electromyogram calibration equals 2 sV. sec for A, 4 #aV. see for B and 10 #sV . see for C. The rectified electromyogram calibration equals 50 1sV for A, 100 ,#V for B and 250 1sV for C. The time and angular displacement calibrations are common to all the sets. The displacement is given in degrees of rotation of the humerus about its long axis.

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548 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON Further experiments on subject L.B.W. gave support to this interpretation. In an experiment in which all the trials were stretches, his responses showed two components to start with, but the early component soon became enfeebled (Fig. 9A). Two runs later in a continuous sequence he gave an almost pure response at 40 msec (Fig. 9B).

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Fig. 9. Stretch reflexes in infraspinatus and flexor pollicis longus in subject L.B.W. The muscles were stretched in the usual way by reversing the motion during a smooth tracking movement or, in the case of the thumb, by extending the terminal phalanx while the subject was holding the thumb flexed against a resistance. Sweep duration 250 msec, with stretches applied at 50 msec. Timing lines are at the moment of stretch and 40 msec later. The electrical records on the right are rectified and smoothed electromyograms, with zero base lines drawn in. In each run four successive averages of eight trials were recorded, without controls, to give the four traces shown. A, infraspinatus, the first run performed. Initial force in wire 200 g (2.0 N). The subject was exceeding the correct rate of tracking. The first two averages show a small response at a latency of about 15 msec, in front of the main response at 40 msec. To be compared with Fig. 4B. B, infraspinatus, the third run in the same experiment as A. Only the long latency response starting at 40 msec is seen. C, flexor pollicis longus, showing stretch responses at the same latency as those in infraspinatus. Initial force 540 g (5 3 N). Tulips in this muscle and finger jerks recorded at the same session in this subject are shown in Fig. lA (2 March 1974).

SERVO ACTION IN VARIOUS HUMAN MUSCLES

549

If the late component at 40 msec in infraspinatus, seen with greater or less clarity in all three subjects, can be equated with the stretch reflex in the thumb then any hypothesis that it depends on a spinal reflex utilizing slowly conducting afferents becomes very implausible. If (as would be the case if the slow afferent conduction velocity was the same as for the thumb) the latency of the late component in infraspinatus had been reduced in proportion to the reduction in jerk latency it would have been some 25 msec, rather than 40 msec. So that clearly is ruled out, and to account for a latency of 40 msec in terms of even slower afferents would require unrealistically low velocities. Thus, if the motor conduction time is taken as half the jerk latency, i.e. as 6-5 msec, afferent conduction time would be 33-5 msec, implying that the fastest afferents involved conducted at 33-5 . 65 5 times slower than the motor fibres. On the other hand the results are compatible with the view that the excess latency of the late component over the tendon jerk is roughly the same for the thumb and shoulder muscles, about 25 msec. It may, in fact, be rather greater for infraspinatus than for flexor pollicis longus. Thus Fig. 9 C shows that the latency of a stretch reflex in the thumb of L.B.W. is practically the same as in his infraspinatus, whereas on the simplest expectations of the transcortical hypothesis it ought to be longer by the difference in jerk latencies (about 12 msec) plus a millisecond or two because the motoneurones of flexor pollicis longus are two or three spinal segments further from the brain than those of infraspinatus. Other instances of greater excess latencies than expected will be met with later.

While these results can be regarded as supporting the transcortical hypothesis for the stretch reflex in the thumb they do, however, require important modifications of our views in the case of proximal muscles. In normal subjects there is a substantial component at spinal latency which is elicited by rates of stretch that cannot be regarded as unphysiological. Thus, during stretch in the experiments of Fig. 8 the hand moves at roughly 50 cm/sec. The interpretation of the tendon jerk as 'an accidental overload condition of a nervous pathway' (Hammond, Merton & Sutton, 1956) only produced by rates of stretch greater than encountered in ordinary life must be regarded as suspect. (It might still be correct, for there is no guarantee that the spinal latency responses seen in infraspinatus are monosynaptic, as the tendon jerk almost certainly is. An attempt to augment small early responses to stretch in the long thumb flexor of P.A.M. by vigorous reinforcement proved unsuccessful.) It follows that the answer to the question 'Is the human stretch reflex cortical, rather than spinal?' (Marsden et al. 1973a) must be 'only in part' as regards infraspinatus. And it is not only the responses to stretch itself that show two components, for early release responses are clearly to be seen in the infraspinatus in C.D.M. (Fig. 8A) and early halt responses, as well as releases, will be described later in biceps. Thus the whole tulip, at any rate in proximal muscles, probably has two components, identified provisionally as spinal and cortical on our working hypothesis.

550

C. D. MARSDEN, P. A. MERTON AND H. B. MORTON

Pectoralis major The tendon jerk latency in pectoralis major (12 msec) is similar to that in infraspinatus, but fewer experiments have been done with this muscle because the mechanical arrangements proved less satisfactory. The movement used was adduction of a near-vertical upper arm as described in Methods. If the elbow was flexed to reduce the moment of inertia for movement at the shoulder and the wire loop that led to the motor pulley was hitched over the medial epicondyle, tulips with an early component were obtained. One from C.D.M. is given in Fig. 10A and others (with a smaller first component) from P.A.M. will be illustrated in a subsequent paper. With the elbow extended and the pull taken by the wire round the distal ends of the radius and ulnar, tulips without an early component were obtained both in P.A.M. (Fig. 10B) and in C.D.M. (not illustrated). These results are consistent with the view that there are two components in pectoralis major, as there are in infraspinatus; that the first component is velocity sensitive, as it is, for example, in the digits (Fig. 4), and is lost when the experiment is done with the elbow extended, because then the extra compliance and increased moment of inertia slow the initial rate of extension of the pectoralis. To elicit tendon jerks the experimenter pressed his thumb on the tendinous end of the muscle, near its insertion into the humerus, and struck his thumb with the hammer. If the muscle is struck at this point directly with the hammer a jerk is seen, but in this jerk the muscle fibres are excited directly, not reflexly, and the action potential recorded at a distance has a slow take-off and a latency longer than that of a tendon jerk. (Falsely brief latencies may be obtained for similar reasons for the ankle jerk and for other muscles if ill-directed blows are struck with a hard hammer.)

A simple modification of the above arrangements is of interest as showing the servo in action in almost natural conditions. In this experiment the hand was fully supinated, the elbow extended and the movement was adduction of the pendant arm across the trunk. The thumb was somewhat flexed and the wire from the motor pulley was hitched round the pad of the thumb. No clamps or supports were employed at all. To exert force on the wire both the thumb flexors and the pectoralis had to contract (and no doubt other muscles too). Electrodes were applied to both flexor pollicis longus and pectoralis major. Tulips were recorded from both muscles simultaneously (Fig. 10C). Although the system was even more compliant than before and no special attempt was made even to steady the subject's trunk, good tulips were obtained both of which had a latency of about 40 msec. (This similarity of latency implies a greater

SERVO ACTION IN VARIOUS HUMAN MUSCLES 551 'excess latency' for pectoralis than for flexor longus, as already seen in infraspinatus.) The task approximates to a number of normal acts, such as tugging at a dog on a lead, and the result shows that servo assistance would be immediately available in such circumstances. Looked at from A

B

C

250 msec Fig. 10. Tulips in pectoralis major, contrasted with tendon jerks. A, subject C.D.M., the tulip is the average of three runs, giving forty-eight trials to each trace (31 March 1973). B, subject P.A.M., the average of five runs, giving eighty trials to each trace (5 May 1973). Tendon jerks on the same time base are given as insets. Each is the average of eight raw action potentials. The peak-to-peak height is 530 1WV in A and 360 ,uV in B. The timing lines are at the time of imposition of perturbations (or at the start of the tendon jerk recording sweep) and 12 and 40 msec later. Rectified and smoothed electromyograms were available for A only. C, subject P.A.M.; simultaneously recorded tulips in pectoralis major (above) and in flexor pollicis longus (below); details in text. The calibration of angular displacement, which applies to all pectoralis records, is in degrees of rotation at the shoulder. The calibration bar for the tulips is equal to 5 #uV. see for A, 30 sV . see for the pectoralis tulips in B and C and 8 1sV. see for the thumb tulip in C. For the tulips, the initial force in the wire was 700 g (6-9 N) in each case.

this point of view we see that it may be no coincidence that the responses in pectoralis do not anticipate those in the thumb; if they did, an undesirable 'whiplash' element might be introduced to the detriment of the thumb. Biceps brachii The experiments on biceps confirm the original results of Hammond (1960) and our own results on infraspinatus and pectoralis. Experimental

552 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON details are given in Methods. Both C.D.M. and P.A.M. (Fig. IlA and B) have a large early stretch component in the tulip with a hint of an early release response and an early halt in C.D.M. L.B.W. gives nothing at all before 50 msec, a clearer result even than his infraspinatus tulip (Fig. 8 C). Hammond's figure for the stretch reflex in biceps was 45 msec. Tendon jerks, elicited by conventional methods, had a latency close to 15 msec in A

B

C

0 15

50

250 msec

Fig. 11. Tulips in biceps brachii, contrasted with tendon jerks. The layout is as for Fig. 8. Timing lines at 0, 15 and 50 msec from the imposition of perturbations. A, subject C.D.M.; the tulip is the average of five runs, giving forty trials to each trace (4 February 1973). B, subject P.A.M.; three runs giving twenty-four trials to each trace (4 February 1973). C, subject L.B.W.; a single run of eight trials averaged for each trace (11 December 1973). The peak-to-peak amplitude of the tendon jerk action potentials (each the average of eight) is 840 ,pV for C.D.M., 1-7 mV for P.A.M. and (with intense reinforcement) 160 ,V for L.B.W. The various calibrations apply to all three sets of records. Displacement is in degrees of rotation at the elbow joint. The initial force in the wire was 700 g (6-9 N) for each subject.

all three subjects. Biceps has the advantage over the shoulder muscles that the mechanical conditions are better defined. With the wire round a wristband fitted closely to the ends of the radius and ulnar, the compliance presented to the motor is small and the mechanical lag before the muscle is extended in a stretch reflex is likely to be brief.

SERVO ACTION IN VARIOUS HUMAN MUSCLES

553

Flexor pollicis brevis An alternative approach to the problem of slowly conducting afferents is to look at a muscle distal to flexor pollicis longus instead of at proximal muscles. Excellent tulips can be obtained from electrodes over flexor pollicis brevis in the thenar eminence simply by carrying out the usual movements of thumb flexion without applying the clamp to the proximal phalanx. Such tulips will be illustrated in a later paper in connexion with another question. (It is not guaranteed, of course, that, of the short thenar muscles, only flexor pollicis is involved.) Tulips can be recorded simultaneously from the short and the long flexor and the difference of latency

under identical conditions thereby measured. A

B

250 msec

Fig. 12. Comparison of stretch reflex latencies in flexor pollicis longus and flexor pollicis brevis. Simultaneous tulips were recorded from electrodes in the usual position over flexor longus, and from a pair of electrodes 4 cm apart at the ulnar border of the thenar eminence over flexor brevis. Only the averaged rectified responses to stretch are displayed. Initial force, in both cases, 540 g (5-3 N). A, subject C.D.M.; superimposed records of stretch reflexes from the two muscles, each the average of eight runs of eight trials each (4 October 1975). B, subject P.A.M.; each record is the average of four runs of eight trials (30 September 1975). In each case the plotting gain has been chosen so that the reflex responses are roughly the same size. In both cases the later responses are from the thenar electrodes. The mean levels have also been adjusted so that the initial parts of the records superimpose. The calibration bar equals in A, 250 /fY for the record from flexor longus and 125 flV for flexor brevis; in B it equals 50 1V for both records. In the event the answer obtained was equivocal. The difference in motor conduction time for the two muscles was obtained by stimulating the median nerve at the elbow and simultaneously recording the action potentials of the two muscles. For both subjects, with the particular electrode placings in use, this time was 3-5 4 0 msec. For a reflex response using fast spindle afferents the difference in reflex time should be approximately double this interval, i.e. 7-8 msec. In C.D.M. a check on this figure was obtained in one experiment in which tendon jerk action potentials were recorded simultaneously in the short and long flexors when the top of the thumb was struck with a hammer; the difference in latency was 8 msec (30 msec as against 22 msec). In P.A.M. the same answer was obtained if the motor latency recorded from electrodes over flexor brevis was measured by stimulating the ulnar nerve at the elbow, so it would make no difference if the 'flexor brevis' reflex responses were really in ulnar-supplied thenar muscles. In both subjects several series of simultaneous full tulips were recorded, but for comparison of latencies the rectified electromyograms of the stretch responses gave

554 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON the sharpest take-off and attention was concentrated on them. Fig. 12A gives the results for the best series on C.D.M. The latency difference is about 8 msec. In another series the next day, however, the latency difference appeared to be about 13 msec; and in two series on P.A.M., of which Fig. 12B is one, the difference was also about 13 msec. The results thus lean towards the slow afferent rather than the transcortical hypothesis. We are not inclined to give much weight to this. The differences we are trying to measure are at the limit of the technique. It is also clear that the excess latency of the stretch reflex over the tendon jerk is not constant for different muscles of the cervical enlargement, as we have already drawn attention to for the results on L.B.W. in Fig. 9 and for the simultaneous tulips on P.A.M. in Fig. lOC. In these cases the excess is greater for muscles proximal to flexor pollicis longus; here it may be slightly greater for a distal muscle. A

B

12 40 250 msec Fig. 13. Jerk responses in infraspinatus in subject L.B.W. The arrangements were the same as for obtaining tulips except that the subject did not track but held the arm in a steady position against a pull of 200 g (2.0 N) by the wire on the wrist. Responses were elicited by striking the dorsum of the wrist with a hammer. The records shown are raw electromyograms (not rectified or integrated) on a 250 msec sweep. A, four single sweeps above, with their average below. B, the same, but before each record was made the subject 'reinforced' vigorously. The records are not the same as those shown in the inset of Fig. 8C, but were made on the same occasion (2 March 1974). The timing lines are at 12 and 40 msec. The sweep was triggered when the hammer struck the wrist.

Double tendon jerks In muscles which in healthy subjects give tendon jerks only with difficulty, such as flexor pollicis longus, and in other muscles in the subject L.B.W., who had very feeble or absent jerks all round, a blow with a tendon hammer may elicit a late response in the muscle in addition to or

SERVO ACTION IN VARIOUS HUMAN MUSCLES 555 instead of a response at the normal jerk latency. This has already been illustrated without comment for finger jerks (Fig. 1 A) and for infraspinatus jerks in L.B.W. (Fig. 8C). The late response is at the time of the hypothetical cortical stretch reflex. The most instructive instance of the phenomenon was given by L.B.W. in infraspinatus. When he arranged himself as if to do a tulip experiment, with his forearm stationary but exerting a small steady force on the wire round his wrist by contracting infraspinatus, striking the dorsum of the B

A

1 10 UVI

C

D

125 msec

Fig. 14. Double tendon jerks from the distal phalanx of the thumb. The electrodes were in the usual position over flexor pollicis longus and single action potentials were recorded raw. A and B, selected responses to hammer blows in C.D.M. A, four superimposed records showing large early responses. B, four records with large late responses (2 August 1975). C and D, similar records in P.A.M. but using the Hoffmann technique of flicking the thumb, instead of the hammer (6 July 1975). The calibrations apply throughout.

wrist with the hammer gave a response consisting solely of a diphasic action potential at 40 msec (Fig. 13A), the same latency, that is, as the stretch reflex in that muscle. With intense Jendrassik-type reinforcement, but otherwise without change in the conditions or in the weight of the hammer blows, a small electrical response was seen at tendon jerk latency (Fig. 13B) but the late response at 40 msec was still present and was not altered in size by the reinforcement. This is taken as clear evidence for two components of different mechanism in the response to stretch. In subjects C.D.M. and P.A.M. double jerks were frequently seen when attempting to record tendon jerks from flexor pollicis longus. For this purpose the proximal phalanx was firmly held by the experimenter and the distal phalanx was slightly flexed, either by natural elasticity or by a minimal voluntary contraction of the long flexor. Two forms of stimulus have given results: either a glancing blow from a rapidly moving tendon hammer or a flick from the experimenter's middle finger (Hoffmann's technique, see Methods). Visible reflex jerks of the thumb, such as are easily obtained by flicking other digits, were never seen when we were

556 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON recording with mechanical stimulation of the thumb; but they were seen very occasionally at other times in C.D.M. when flicking his thumb, and they are not uncommon in some people. Since flicking the thumb often causes a reflex twitch in other digits there is no guarantee that the diphasic action potentials we record after striking or flicking the thumb are, in fact, in flexor pollicis longus (anything in the way of a heavy blow to the thumb is apt to move the wrist and give obvious reflex responses in other flexor muscles). The earliest electrical responses to striking the thumb with the hammer had a latency, both in C.D.M. and P.A.M., about 2 msec longer than finger jerks recorded through the same electrodes at the same session, i.e. about 24 msec for the 'thumb' jerk in C.D.M. and 27 msec in P.A.M. Four selected early jerk action potentials of this type from C.D.M. are shown in Fig. 14A. Fig. 14B gives four records from the same series selected for their large second components, which are at about 50 msec. In P.A.M. late components were not in evidence when the hammer was used, but they were seen with the Hoffmann flick. Fig. 14C gives four superimposed early jerks, with a latency of about 30 msec (as mentioned in Methods, the Hoffmann method gives longer latencies than the hammer) to be contrasted with the almost isolated late responses from the same series in Fig. 14D. Their latency, again about 50 msec, is clearly more variable than that of the early responses. Double responses to striking the terminal phalanx of the thumb with the hammer were also seen very clearly (in flexor pollicis brevis?) with electrodes on the thenar eminence, the latencies of the two components being 30 and 60 msec (subject C.D.M.). In general the larger the early component the less likely it was to be followed by a late response. This was very obvious with ankle, knee and biceps jerks in healthy subjects, which never, in our experience, showed a second component. It is also of interest that in subject L.B.W. late components were absent from his biceps jerks (Fig. 11 C), the only tendon jerk in him that gave a visible mechanical twitch of the muscle. We conclude that a tendon jerk may have two components and when it does they very probably have pursued different reflex pathways. A large early component militates against a late component. The late component we identify provisionally with the stretch reflex seen with stretch at slower rates, in tulips, etc. The fact that a sharp blow that gives rise to a tendon jerk may also produce a long-latency reflex which is at roughly the same time as the stretch reflex seen in a tulip is an additional argument against the possibility that mechanical lags are a significant element in the long latency of a tulip.

SERVO ACTION IN VARIOUS HUMAN MUSCLES

557

DISCUSSION

A principal object of the experiments described in the present paper was to see whether the transcortical theory of the human stretch reflex would stand up to two tests that might have invalidated it. On the whole it does stand up, with the important proviso that in proximal arm muscles there is an additional early component which almost certainly is spinal in origin. The identification of the late, supposedly cortical component in proximal muscles is strongly supported by the results obtained on one apparently completely healthy subject who had absent or very feeble tendon jerks. The relative importance of the early and late components of servo action in proximal muscles in ordinary life cannot be assessed as yet. There is no hint that our special subject is not as nimble in every way as his contemporaries, and yet he is presumably lacking almost all spinal latency servo action. Likewise in the experiment of Fig. 10C on subject P.A.M. in which the conditions most mimicked those of an everyday muscular act, the responses in pectoralis were wholly long-latency. On the other hand large spinal-latency stretch responses were seen in infraspinatus with quite modest rates of arm movement and early components in other elements of the tulip were discernible in both infraspinatus and biceps. So it seems likely that the spinal components will prove to have a real function in man. The human tendon jerk may well not have been put there, as we at one time suspected, to test the faith of physiologists. Nevertheless, as we have argued at several places in this paper, the tendon jerk does behave differently from the long-latency stretch reflex and must have a different mechanism; so that the distinction between tendon jerk and stretch reflex which we drew in an earlier paper (Marsden et al. 1973 a) is to be maintained. When it was first applied to the human results the transcortical theory was on the defensive as regards the time available. For the long thumb flexor, 40 msec does not seem a generous allowance for conduction to the cortex and back. But these worries have now been set at rest. MilnerBrown, Girvin & Brown (1975) stimulated the exposed human motor cortex with single shocks and recorded minimum latencies of 17-22 msec for electrical responses from thenar muscles in the hand. With stronger stimuli the latencies were 1-2 msec less. Allowing for the fact that motor conduction time to electrodes over flexor pollicis longus is 3-4 msec less than to thenar muscles, we roughly estimate efferent conduction times from cortex to forearm as 14 msec for C.D.M. and 17 msec for P.A.M. If the latencies of the cortical sensory evoked responses (see Results) are used to give the approximate sensory conduction times (19 and 21 msec), it is seen that there is plenty of time for a transcortical loop. Indeed MilnerBrown et al. point out that there may even be time for a transcortical

558 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON

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SERVO ACTION IN VARIOUS HUMAN MUSCLES 559 stretch reflex employing Group II (secondary) spindle afferents. The relevant figures for flexor pollicis longus and other muscles are summarized in Table 1. (The motor conduction times from cortex to flexor hallucis longus are approximate values based on Pagni, Ettore, Infuso & Marossero (1964), who obtained latencies of 26-33 msec from electrodes over tibialis anterior when stimulating the internal capsule). Further discussion of the transcortical theory is deferred until future papers dealing with the effect of peripheral anaesthesia and of clinical lesions of the pathway. The longlatency stretch reflex in the thumb is abolished by lesions of the dorsal column, of the internal capsule and of the sensorimotor cortex, which do not necessarily alter the tendon jerks in the arm. Preliminary accounts of this work have appeared (Marsden, Merton & Morton, 1971, 1972; Adam, Marsden, Merton & Morton, 1976). C.D.M. and P.A.M. express their thanks to Dr W. A. Cobb in whose department of Clinical Neurophysiology at the National Hospital the experiments were done. Financial support was received by C.D.M. from the Bethlem Royal and Maudsley Hospitals Research Fund and by P.A.M. from the Department of Trade.

REFERENCES

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