subject who happened to have feeble or absent tendon jerks. In ordinary subjects there is often a

30 Pages·2005·2.92 MB·English

J. Physiol. (1976), 259,pp. 531-560 531
With 14text-figurew
Printedin Great Britain
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 CrespignyPark, LondonSE5 8AF
(Received 22January 1976)
SUMMARY
1. In the long flexor ofthe thumb the latency ofthe stretch reflex and
of other manifestations of servo action is some 45 msec, roughly double
the latency ofa finger jerk.
2. Tendonjerksarefeebleorabsentinthelongflexorofthethumb even
in subjects with brisk long-latency stretch reflexes in this muscle. This,
and other facts, suggests that the nervous mechanism ofthe tendon jerk
is differentfrom that ofthe stretch reflex.
3. A muscle that hasfeeble tendon jerks may show a late component in
the response to a tendon tap, with a latency similar to that of the long-
latency stretch reflex.
4. On the hypothesis that the excess latency of the stretch reflex over
thatofa tendonjerkis because the stretch reflex employs a corticalrather
than a spinal arc, the excess would be expected to be larger in magnitude
for the long flexor ofthe big toe and smaller for the jaw closing muscles.
This is confirmed.
5. An alternative hypothesis that the long latency ofstretch 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 signifi-
cance 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 componentofthestretchreflexuses atranscorticalreflex arc,
and that none of the experiments described in the present paper are
inimical to thisview.
INTRODUCTION
Anearlierpaper (Marsden, Merton & Morton, 1976) described servo-like
responsesinthelongflexorofthethumbandgavesomeoftheirproperties.
A singular feature of these responses was their uniformly long latency
relativetothetendonjerktimeinforearm muscles. Thefingerjerklatency
isabout25 msecandispresumably ameasureofthetimeround 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
tissuesare 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 ofthe 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 bythe existence ofafastpathway
forprimaryspindleafferentstothecerebralcortexandafastmonosynaptic
corticospinal pathway back to hand motoneurones in the baboon, won-
dered 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
actionisdifferentfromthatofthetendonjerk,sothatitdoesindeedrequire
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 ofit. We can,
however, follow out some ofthe consequences ofthe 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 533
METHODS
The general technique for recording, in one experimental run, the responses ofa
muscle to unexpected stretch, halt or release in the course ofa series ofvoluntary
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 inusetothelow-inertiaelectricmotorthatopposeditandappliedperturba-
tionsduringthemovement.
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
forthethumb. Thelongflexorworksontheterminalphalanxand,whenthisflexed,
the pad ofthe great toe bore on the thumbstick in the ordinary way. To be at a
convenientheightthesubjectsatonahightable.Forleadingofftheelectromyogram
of the flexor hallucis longus one electrode was 3cm behind and 3 cm above the
medial malleolus and the other 6 cm above the lateral malleolus behind the fibula.
Forthejawclosingmuscles, masseterandtemporalis, thesubjectrestedhisupper
teethinagroove onahorizontalbarfixedtotheframe.Alever5cmlongcarriedon
the motor spindle in place ofthe thumbstick pushed the lower jaw downwards by
bearing on the lower teeth. When the contact arm was against the backstop, the
teeth were about 4cm apart. The subject's task was to close his teeth at a smooth
rate. Themusclesarestrongandtheinertiaofthejawhigh, comparedto thethumb
ortoe, so thelargest possible motor currents had to be employed to getreasonable
rates ofstretch. One recording electrode was over the zygoma, 6 cm in front ofthe
auditorymeatus; theelectrodeformasseterwas 4cmvertically belowthis one, and
thatfortemporaliswas4cmabove.
Fortheinfraspinatus apulleyofdiameter 6 cm, used as awinch drum, was fixed
tothe motor spindle inplace ofthe thumbstick. Alength offlexible steel cable was
anchored to the pulley, taken round it for a turn and then run offto the subject's
wrist, where it ended in a loop. The subject sat on the board carrying the motor
withhisbacktothemotorandhisrightforearmheldhorizontallyacrosshisabdomen.
The palm of the hand was vertical, facing backwards, with fingers lightly flexed.
The loop ofwire went round the wrist at the level ofthe heads ofthe radius and
ulnar. It was prevented from cutting into the skin by an incomplete band of
aluminium shaped tofittheboneheads. Both thebandand thewireloopwereheld
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 thewrist awayfrom the bodyas in abackhand stroke at tennis.
Thismovementemploystheinfraspinatusmuscle.Asafulcrumthemedialepicondyle
oftherighthumerusrestedinacupcarriedonthemainframe. Toavoidmovingthe
display cathode ray tube, used for tracking, which was now behind the subject, he
viewed itinamirror. Onerecordingelectrode was 3cmfrom themedialedgeofthe
scapula and 4cm below the spine, the other was 4cm lateral to the first and 3cm
below the spine. In a few experiments a bipolar needle electrode, inserted between
these sites,wasemployed.
With the largest motor current (17A) the tension in the wire was 3-4kg (35N).
Whenthiswassuddenlyappliedthewireextendedslightlyandthepull compressed
theskinatthewrist. Thesevarioussourcesofgivecauseaninitialstep,lastingsome
5msec, to be seen in some displacement records of stretch reflexes, e.g. Fig. 9B.
For pectoralis the motor was to the right ofthe subject and the movement was
adduction ofthe humerus, held slightly forward so that the elbow could pass some
534 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON
wayacrosstheabdomen. Thesamepulleyandwirewereused. Insomeexperiments
the subject sat, the elbow was fully flexed with the forearm held to theupper arm
byastrapandthepullwastakenbyhitchingthewireloopoverthemedialepicondyle
(protected with surgical tape) and the head ofthe ulnar. In other runs the subject
stood with his elbow extended and the wire loop tookthe pull around the wrist at
the level ofthe heads ofthe ulnar and radius with a wrist band, etc, as for infra-
spinatus. Thepalmofthehandfacedawayfromthemotor. Onerecordingelectrode
was 6cm from the mid line at the level ofthe second rib and the other electrode
4cmlateraltothefirstinthedirection ofthefibresofthepectoralismajor.
For biceps the subject sat facing the equipment with the pulley in front of his
rightshoulder. Hisupper armsloped straightforwards anddownwards to rest on a
board,whichwasanextensionoftheboardwiththemotoronit. Theolecranonwas
prevented from moving forwards byawooden chock fixed to the board. When the
contact arm on the motor spindle was against the backstop, the elbow was flexed
roughlyto arightangle. Thepalmofthehandfacedtheshoulder. Thewireloopto
the pulleywas round awristband at thelevel ofthe heads oftheulnarand radius.
The taskwas smooth flexion ofthe elbow. Electrodes 4cm apartwere applied over
thebellyofthebiceps.
Tendonjerkswereelicitedusingahammerwithamicroswitch initfortriggering
the recording sweep. The striking face was a light plastic member hinged to the
hammerbodythathadtomovebackabout 1 mmto opentheswitchinthebodyof
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
operationofthemicroswitchwasaboutamillisecondwithblowsofaverageviolence,
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, signalledbytheforcetransducer onthe thumbstick, and the time ofopening
ofthemicroswitch. Acomputerprogramme, usingacontinuously runningmemory,
whichallowed eventsbeforethetriggerpulsefromthemicroswitch to beinspected,
wasusedforthis measurement. Adelay ofamillisecond or so between first contact
and the opening ofthe microswitch corresponds to a velocity ofabout 1 m/sec for
theheadofhammer,whichisreasonable. When thehammerstruckthethumbstick
moreslowlylongerintervalswereobserved.
It is ofinterest that varying the rate ofthe hammer blow over a wide range did
notobservablyalterthelatencyofafingerjerk, measuredfromthetime ofopening
ofthe microswitch, although the interval between first contact with the skin and
the opening ofthe switch must have altered by several milliseconds. This suggests
thatthereisinsufficientinertiain thehingedplasticmembertostretchthemuscles.
The opening ofthe microswitch corresponds closely with themomentwhenthefull
weight ofthe hammer comes behind the blow and this apparently is what counts.
In another method ofeliciting finger and thumb jerks, the tip ofthe digit was
flicked by the experimenter snapping his middle finger (Hoffmann's reflex). To
triggertherecordingsweepatthemomentofcontact, electrodeswereappliedtothe
hands ofboth 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
obtainedinthiswaywas 2-3mseclongerthanwhen thehammerwas used andthe
latencywasmeasuredfromtheopeningofthemicroswitch. Itwouldthusbesimilar
tothelatencyofafingerjerkfromaslowhammerblow,ifthestartweretobetaken
fromthetimeoffirstcontactofthehammerwiththeskin.
It is not obvious which measure should be taken as the true latency ofthe jerk.
SERVO ACTION IN VARIOUS HUMAN MUSCLES 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. Ifit is preferred to measure latencies from first
contactwiththeskin, 1-3msecmustbeaddedto ourfigures. The arguments based
onthemarenotaffected.
Subject. Most experiments were performed, as in the earlierpaper, on two ofthe
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
studentaged20atthetimeoftheinvestigations. Atabouttheageof15hehadbeen
found to have no tendon jerks at a routine school medical examination. This was
confirmedbyordinarytestingin 1972,butlateraflickerofajerkinbicepswasseen
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
latenciesarenormal, sotherecanbenoabnormalityin eithersensory ormotorcon-
duction velocities. Pupillary responses to light and accommodation were normal,
ruling out the full-blown Holmes-Adie syndrome. The subject had no motor or
sensorysymptoms,hetookpartingamessuccessfully, playedthefluteandappeared
ineverywayhealthy.
RESULTS
Flexorpollwic longu8
In previous writings (and in Fig. 1B of this paper) we compare the
unexpectedly long latency ofa tulip in flexor pollicis longus (40-50 msec)
with the latency ofa finger jerk (20-25 msec) recorded through the same
electrodes, taking the jerk latency as an estimate of the spinal mono-
synaptic reflex time for muscles at that level in the forearm. There is no
hintofa response in the tulip at tendon jerklatency, and this is true even
with high initial loads (e.g. Fig. 3 ofthis paper and figs. 13, 14and 15 of
Marsden et at. 1976) which are known from the work ofUpton, McComas
& Sica (1971) to potentiate spinal monosynaptic reflexes.
Our estimate ofthe time to and from the spinal cord has now been checked in
both the principal subjects by recording F waves, through electrodes over flexor
pollicislongus,tomaximalstimulationofthemediannerveattheelbow.Thelatency
ofthe F wave plus the latency ofthe direct action potential evoked by the shock
gives a measure oftwice the motor conduction time from the cord to the muscle
which (asisknownfromcomparison ofHreflexandFwavelatencies inothersites)
approximates tothereflexconductiontime.
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 itselfis conspicuously difficult to elicit, in fact previously we
thought it impossible. We return to the question ofthumb jerks later but
we wish now to make the point that this verydifficulty in evoking thumb
jerks even by extending the terminal phalanx as rapidly as possible,
suggests at once that 'tulips', in which the rates ofstretch are much less,
536 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON
are (quite apartfromtheirlonglatency) notlikelytobebasedonthesame
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 B
/0
0
250 msec
Fig. 1. Servo responses in the long flexor of the thumb, contrasted with
fingerjerks. A, in subject L.B.W. (2 March 1974). B, in subject P.A.M. (3
March 1974).Foreachsubject,tendonjerks (eachtheaverageofthirty-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
forP.A.M.
The main records in the upper half in A and in B are superimposed
rectified and integrated electromyograms ofthe response ofthe 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, 540g
(5 3N). Each trace is the average of thirty-two trials (four successive
experiments each of 8 trials ofeach 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.
Thetiminglines are atthe time ofimposition ofperturbations, at 50msec
later,andalsoatthetendonjerklatency (22msec forL.B.W. and 25msec
forP.A.M.).
The peak to peak amplitude ofthe first component ofthe tendon jerk
(the component starting at 22msec) in L.B.W. is 731V; the amplitude in
P.A.M.is800,itV.Tendonjerkswereelicitedintheordinaryclinicalmanner.
Thesubjectlightlyflexedhisfingersagainsttheexperimenter'sfingersand
the experimenter then struck his own fingers with the tendon hammer.
The displacement and integrated electromyogram calibrations apply to
bothsets ofrecords. The timescale iscommonto alltherecords, including
the tendonjerks. The tendon jerkrecording sweeps are plotted to start at
thetime ofimpositionofperturbationsin thetulips.
~~~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 ofhis 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 B/
40
0
250 msec
Fig. 2. The relatively constant latency of the stretch reflex in the long
flexor ofthe 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 subjectP.A.M., 'slugged' and 'unslugged' stretches
compared (17 November 1974). Initial force, in both cases, 540g (5.3 N).
In each set the top pair oftraces are the integrated electromyograms, the
middle pair are the rectified and smoothed electromyograms (with zero
baselines drawn in) andthe bottompairaredisplacementrecords,showing
in each case fast and slow stretches. In each trial the three variables were
recorded simultaneously. Each trace shown is the average ofeight 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
andlaterrecord. Thetiminglinesareatthetimestretchstartsand 40msec
later. Thetimeanddisplacement calibrations applyto both setsofrecords.
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
equalto 200#eVforA and 1001sVfor B.
No doubt the long latency ofa tulip, relative to a tendon jerk, does owe
something to the fact that stretch is applied much more abruptly in the
case ofa 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 asastretch of
zero velocity (see, for example, Fig. 3). In confirmation of this, Fig. 2
shows theremarkably similarlatencyofthe 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
Highforce
]A
Slugged
Unslugged
4
Lowforce
Slugged
Unslugged 10
Fig. 3. The relatively constant latency of'slugged' and 'unslugged' tulips
in thelongflexorofthe thumb. ThelowerhalfoftheFigure showsrecords
made at the standard low initial force, roughly 120g (1-2N) at the pad of
thethumb (seeMarsdenetal. 1976). Eachtraceistheaverageofeight,with
'randomcyclic'presentationofperturbationsandcontrols.Tulips,rectified
electromyograms and displacement records for the slugged condition are
shown in the upperrowwith those for the unslugged condition in the row
below. Timing lines at 50msec after the imposition ofperturbations. The
tophalfofthe Figure showsthesame thingwiththeinitialforce 4-5times
greater. The displacement calibration applies throughout. There are
separateelectrical calibrations fortheupperandlowersets ofrecords. The
sweep time is 250msec. The records also demonstrate change ofgain in
proportion to load (seeMarsden etal. 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,
althoughthedisplacement records showthat thestart oftheperturbations
was much sharper without the slugs.
Thus, within therangesofarused, therapidity ofonsetoftheperturba-
tions 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 componentis coming inin frontof the ordinary stretch response seen
in a conventional tulip. This is suggested by Fig. 4A and B, which give
(on afast timebase) the stretch responses to four differentrates ofstretch
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
earliercomponentinC.D.M. wouldpresumablyrepresentaspinalresponse.
With thispossible interpretation in mind we tried to seewhetherwe could
remove the spinal component by rendering the motoneurones partially
refractory by a preceding tendon jerk. Fig. 4C shows that this can appar-
ently 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 com-
ponent 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 ofthis experiment. It is observed that
flickingthepadofthe thumb, inthemannerto obtainatendonjerkbythemethod
ofHoffmann, is seldom successful, but not infrequently when the thumb is flicked
theindexandotherfingerswillrespondwithajerk. Converselyflickingtheindex or
middlefingers-will often give ajerk in the thumb. Hence the early component seen
after rapid stretch of the thumb in the machine may in fact be in finger flexors,
ratherthaninflexorpollicislongus.If,ontheotherhand,itisinflexorpollicislongus,
themotoneuronesofthismusclemayequallywellbeexcitedandrenderedrefractory
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
concernedtoshowthattheearlycomponent, inwhatevermuscleitisoccurring, can
beremovedbyaprecedingfingerjerk,toreveal thelatecomponentinflexorpollicis
540 C. D. MARSDEN, P. A. MERTON AND H. B. MORTON
longusuncontaminated infast stretches. Analogous resultsaregivenlater on infra-
spinatusinsubjectL.B.W.
Forcomparison Fig. 4Dgivesthereflexresponsetofastextension oftheterminal
phalanx ofthe index finger, amuscle known, in this subject, to have abrisk finger
jerk. Stretch ofthe flexors ofthe index finger gives a response which we identify
asafingerjerk,thestartofwhichcorrespondsintimecloselywiththeearlyresponse
seeninthethumb records in B and C: It thus supports theproposed interpretation
ofthe latter.
I0
r4
A
B
C
p-
D
I 9
100msec
Fig. 4. For legend see facing page.