effects ofthe jendrassik manoeuvre muscle spindle...

Jourrnal of Neuirology, Neurosurgery, and Psychiatry, 1975, 38, 1143-1153

Effects of the Jendrassik manoeuvre on musclespindle activity in man'

K-E. HAGBARTH, G. WALLIN, D. BURKE,2 AND L. LOFSTEDT

From the Department of Clinical Neurophysiology, University Hospital, Uppsala, Sweden

SYNOPSIS Twenty-eight mechanoreceptive units identified as primary or secondary spindle affer-ents were sampled from muscle nerve fascicles in the median, peroneal, and tibial nerves of healthyadult subjects. The responses of these units to sustained passive muscle stretch, to passive stretchingmovements, to tendon taps, and electrically-induced muscle twitches were studied while the subjectperformed repeated Jendrassik manoeuvres involving strong voluntary contractions in distantmuscle groups. The manoeuvres had no effect upon the afferent spindle discharges as long as therewere no EMG signs of unintentional contractions occurring in the receptor-bearing muscle and no

mechanotransducer signs of unintentional positional changes altering the load on that muscle.Unintentional contractions in the receptor-bearing muscle frequently occurred during the manoeu-

vres, however, and then coactivation of the spindle afferents was observed. Multiunit afferentresponses to Achilles tendon taps, led off from tibial nerve fascicles, were in a similar way un-

influenced by the Jendrassik manoeuvres, even when these resulted in marked reinforcement of thecalf muscle tendon jerk. The results provide no evidence for fusimotor sensitization of spindles inmuscles remaining relaxed during the Jendrassik manoeuvre, and reflex reinforcement occurringwithout concomitant signs of active tension rise in the muscles tested is presumed to depend upon

altered processing of the afferent volleys within the cord.

In the initial study dealing with recordingsfrom muscle spindle afferent nerve fibres inman, Hagbarth and Vallbo (1968) noted amarked enhancement of the activity in thesefibres during voluntary isometric contraction ofthe leg or arm muscles in which the receptorswere located. These findings have been verifiedin many subsequent studies and evidence hasaccumulated in favour of the suggestion thatvoluntary movements in man are organizedaccording to the principle of alpha-gammacoactivation, the fusimotor drive being directedto the same muscle or muscle portion as theskeletomotor outflow and being powerful enoughto overcome the spindle unloading effect ofthe contraction in surrounding extrafusal fibres(Vallbo, 1970b, 1971, 1974; Hagbarth et al.,1970b, 1975a).1 The investigation was supported by the Swedish Medical ResearchCouncil (Project no. B75-04X-2881-06A).2 C. J. Martin Research Fellow of the National Health and MedicalResearch Council of Australia.(Accepted 7 May 1975.)

As long as the receptor-bearing muscles re-mained relaxed, the Swedish investigators foundin awake human subjects no evidence forvarying fusimotor tonus-that is, the dynamicand static spindle responses to passive stretchwere not appreciably influenced by the Jendrassikmanoeuvre (Hagbarth and Vallbo, 1968) or bychanges in the attentive state of the subject(Vallbo, 1972), and no reduction in afferentstretch responses was seen after lidocaine blocksof the muscle nerve proximal to the recordingsite (Hagbarth et al., 1970b, 1975a; Wallin et al.,1973).

Diverging results were recently reported byBurg et al. (1973, 1974) who during the Jendras-sik manoeuvre found an acceleration of spindleafferent activity in remote relaxed muscles andan irregular spontaneous spindle discharge whichvaried in frequency with the subject's degree ofattention. These findings seem to imply that inawake human subjects intrafusal fibres areexposed to a sustained fusimotor outflow varying

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in strength during various manoeuvres withoutconcurrent changes in the skeletomotor outflowto the receptor-bearing muscles.The intraneural recording technique provides

means of analysing fusimotor system dys-functions in various motor disorders, but suchpathophysiological studies must be based onfirmly established data concerning fusimotorsystem involvement in normal movements. Thus,a reinvestigation was made to check whetherthe findings ofBurg et al. (1974) could be verifiedand accepted as valid evidence that in healthysubjects the fusimotor system may act diffuselyto produce a widespread increase in receptorsensitivity in muscles in which the extrafusalfibres are 'at rest'.

MATERIAL AND METHODS

Data were obtained from 21 experiments in 18subjects aged 25-48 years with no evidence of neuro-logical disease.

MULTI- AND SINGLE-FIBRE RECORDINGS Neural ac-tivity was recorded with tungsten microelectrodesinserted manually through the skin into appropriatemuscle nerve fascicles. Details of the recording pro-cedure, of the storage and display systems and ofamplifiers, filters and noise reducing circuits havebeen described previously (Hagbarth et al., 1970a,1975a). Recordings were made from muscle nervefascicles of the median nerve at the elbow levelinnervating the long finger flexor muscles (fourexperiments), fascicles of the tibial nerve in the pop-liteal fossa innervating triceps surae (seven experi-ments) and fascicles of the peroneal nerve at thelevel of the fibular head innervating the anteriortibial and peroneal muscles (10 experiments). Theways of assessing that the electrode had impaled apure muscle nerve fascicle have been described else-where (Hagbarth et al., 1975a), a main criterion be-ing the multiunit afferent discharges appearing in re-sponse to passive muscle stretch and tendon taps withconcurrent lack of afferent responses to skin strok-ings and other superficial cutaneous stimuli. In 11experiments a mean voltage integrator (time constant0.05-0.1 s) served to give a quantitative measure ofthe multiunit stretch- and tap responses during thereinforcement tests. Within the muscle nerve fasciclesexplored, the discharges of individual mechano-receptive fibres could often be discerned, and asjudged by their receptive characteristics the unitssampled in this way were classified as group Ia,group Ib, and group II muscle afferent fibres (see

below). The effects of remote muscle contractionswere studied on 30 identified muscle afferent fibres.An instantaneous frequency meter of similar typeto that described by Green (1967) was used in theanalysis of the single unit data. In some experimentsthe output of the instantaneous frequency meter wasfed into an RC low pass filter of time constant 0.5 sin order to smooth out the variability in the frequencyplot and produce a continuous line representing meanfrequency.

JOINT ANGLE, TORQUE, AND EMG RECORDINGS Inexperiments on the median nerve the subject wasseated with the arm outstretched, the hand supportedand the fingers fixed to the rotating plate of a hy-draulic device with which controlled passive stretchof the finger flexor muscles could be performed insteps of variable speed and amplitude. In experimentson the tibial and peroneal nerves the subject waslying on one side with the knee extended and thefoot fixed to the rotating plate of the hydraulicdevice. A potentiometer on the pivot of the rotatingplate measured the angle of the metacarpophalangealand ankle joints. A strain gauge bridge mounted onthe rotating plate measured changes in torque, thesensitivity of the bridge being adjusted in such away that small changes in torque down to 0.05 Nmcould be readily discerned. Further details are givenby Hagbarth et al. (1975a). The electromyogram(EMG) of the receptor-bearing muscles was recordedoccasionally with surface electrodes, but usually witha pair of tungsten needle electrodes insulated towithin 5 mm of the tip. Care was taken to ensurethat as far as possible the EMG activity thus re-corded came from the receptor-bearing muscle.During replay and analysis the direct EMG signalswere displayed usually at gains of 500 ,uV/cm or200 ,V/cm. In most experiments, the EMG activitywas monitored on a loudspeaker and integratedusing a mean voltage 'integrator' of time constant0.1-0.2 s. These measures aided identification of lowamplitude distant potentials which were difficult todistinguish from background noise in the directrecording.

REINFORCEMENT MANOEUVRES The reinforcementmanoeuvre used to test the effects of remote musclecontraction consisted of either firm clenching of onefist or the classical Jendrassik manoeuvre, involvingforced separation of interlocked clenched hands. Inexperiments on the median nerve, only the formermanoeuvre was performed, using the free hand. Nodifferences were found between these manoeuvresand, hereafter, both are referred to as the 'Jendrassikmanoeuvre'. The time course of the manoeuvre wasusually determined from EMG recordings obtained

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TABLE 1NUMBER OF JENDRASSIK MANOEUVRES

Testing conditions Manoeuvres Afferent fibres(no.) (no.)

1. At constant lengthDefinite spindle

Ia 25 8II 26 6

Probable spindlela 12 6II 2 1

Tendon organIb 5 1

2. During passive stretchDefinite spindle

Ia 30 10II 4 3

Probable spindleIa 2 2

Tendon organlb 5 2

3. During electric twitchDefinite spindle

Ia 19 54. During tendon jerks

Definite spindleTa 5 21 2 1

on the basis of their discharge during the rising phaseof electrically-induced muscle twitches.The single unit responses to reinforcement manoe-

uvres were assessed under four testing conditionsdesigned to detect changes in dynamic and staticproperties. The manoeuvres were performed withthe receptor-bearing muscles maintained at constantlength, during controlled stretching movements,during tendon taps, and during electrically-inducedmuscle twitches. In experiments on the tibial nerve,the effects of reinforcement on the afferent volleyproduced by percussion of the Achilles tendon werestudied. These experiments allowed correlation ofthe afferent volley with the resulting reflex contrac-tion at measured levels of percussion force.Each afferent fibre was usually subjected to a

number of Jendrassik manoeuvres, but not to allof the four testing conditions. Table 1 shows thenumbers of Jendrassik manoeuvres and the numbersof single afferent fibres tested under each of the fourtesting conditions. Altogether, 127 manoeuvres havebeen performed on the 28 spindle afferent fibres.

RESULTS

with surface electrodes over the forearm flexormuscle group. Subjects were instructed to remainrelaxed in all muscles other than those taking partin the manoeuvre. Compliance with this request waschecked for the receptor-bearing muscles by therecordings of EMG and torque described earlier.

UNIT CLASSIFICATION AND TESTING OF REINFORCEMENTEFFECTS Of the 30 mechanoreceptive units analysedin the present study, 28 fulfilled the criteria of musclespindle afferent fibres as described by Vallbo(1970a). Of these 28 fibres, 18 were also testedusing electrically-induced muscle twitches or mech-anically-induced tendon jerks, and on the basis oftheir discharge during the relaxation phase of thetwitch they were classified as 'definite spindleafferents', whereas the other 10 units were denotedas 'probable spindle afferents'. The electrically-induced twitches were usually delivered throughneedle EMG electrodes, but in a few experimentsthe stimulus was delivered through the micro-electrode which was then switched for recording(blocking time approximately 10 ms, cf. Fig. 7).Depending on their regularity of discharge and theirsensitivity to the velocity of stretching movements,spindle afferent fibres were further classified as

probably group Ia (21 fibres) or probably group II

(seven fibres), although a clear distinction was some-times difficult. Two afferent fibres were regarded as

group Ib afferent fibres from Golgi tendon organs

SPINDLE RECEPTOR SENSITIVITY The 28 spindleafferent fibres had a wide spectrum of receptorsensitivity to active or passive displacement. Atseemingly constant muscle length, some fibresmaintained a relatively stable, mean dischargefrequency, but others proved extremely sensitiveto minor disturbances, a sensitivity whichmade it crucial that equally sensitive meas-ures be used to monitor possible disturbingforces. Examples of this high sensitivity areshown in Fig. 1 for two group Ta fibres. In A,the illustration on the left shows a pronouncedafferent discharge in response to stretching at arate and amplitude which were just above thesubject's threshold for perception. The illustra-tion on the right shows spindle acceleration dueto fusimotor activation occurring in weak iso-metric contractions, and high sensitivity to thesmall internal length changes that occur onrelaxation after an isometric contraction (cf.Vallbo, 1970b). In Fig. lB the frequency plotof another group Ta fibre contains slow periodicirregularities that correspond closely to therespiratory oscillations which became visible inthe torque recording only when displayed at highgain. Indeed, on conversion of the frequencyplot into a continuous line plot (middle trace),an almost perfect mirror image of the torque

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GFIG. Muiscle spind/le sensi-tivitY. A: responIses to stretch-lng movenments of small

20/s amplitude (left) and to wveakisometr-ic calf muiscle conitrac-tions (right) of a gastroc-

Nm niemiuns group Ia fibre (twitchtest in C). On the left stretcli-inig mnovemelits of less thani 2(lower trace) ev'oke a promi-

0.3 Nm nelnt spinidle discharge visiblein the ielurogr-am (upper trace)ancd the instantanieous fre-

10/s quencvX plot (middle trace). Asini subsequent Figuires, passive

0 stretch of the receptor-bearinigm1u.scle is inidicated bv a dowmi-vwar-d deflectioni of the gonIio-mmIeter record. Oti the right awveak voluntary comitractiolirecorcled lin the torque sigmial

-Il-i- 1 Nm (third trace) amid the imitegratelgastrocmieiniuls EA4G (lowesttrace) provokes an imicreasedspindle discharge. Relaxationi

alter the contractioti produlces a brief high Jiequenicy burst of impulses. A simwilar sequence is seemi in the subse-quent much weaker unintentional contractioni. B: both illustrationis are from a tibialis aniter-ior group Ia aJfe_rentfibre (twitch test in D) with subject at rest and niuscle at conistamit length. Slow periodic fluctuatiomis are seeniin the frequenicy plot (lowest trace) closely parallelling the respiratory oscillations recordled at high gain ini thetorque signal (upper trace). In the middle trace the output of the frequencyvneter was stmioothed to give a con-tin2uous linie plot, thus highlightinig the similarity of the irregularities ini torque amid frequency. C anld D: twitclitests of the fibres iii A and B respectively showimig torque (lower traces) amid mieurogr-amlt (upper traces). Ini eachcase five sweeps have beemi suiperim1posed. Neural silemice durimig the risimig phase of the contraction amid dischargeomi the relaxationi phase idenitify the units as spindle afferenit fibres. In D the veir1 earl/v neural spike probablYrepresenits direct stimulation of the fibre.

record is obtained, allowing for the phase lagintroduced by the conversion.

EFFECTS OF REINFORCEMENT ON SINGLE AFFERENT

FIBRES Table 2 details the number of musclenerve afferent fibres that were not influenced bythe Jendrassik manoeuvre, and, for those thatwere influenced, the accompanying changes in

the EMG and torque records. In 15 afferentfibres the reinforcement manoeuvre had no effecton the discharge frequency, whether the manoe-

uvre was performed with the receptor-bearingmuscle at constant length (Fig. 2A, B), or per-

formed during controlled muscle stretch(Fig. 2C), during electrically-induced twitches(Fig. 2D) or during tendon percussion. In theremaining 15 fibres changes in discharge fre-

quency were observed during reinforcementmanoeuvres. However, the responses of most ofthese fibres were not reproducible (see Table2). The variability of response from one test tothe next was especially pronounced for thoseafferent fibres which exhibited the extremesensitivity to displacement referred to above. Inthree fibres the reinforcement led to a decreasein frequency in some tests. Only four spindleafferent fibres increased their discharge frequencyin every reinforcement manoeuvre with whichthey were tested. In all cases, however, wherea change of discharge frequency occurred dur-ing the Jendrassik manoeuvres, simultaneouscontractions or changes in the load on thereceptor-bearing muscles were detected (seeTable 2). Furthermore, the degree and direction

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TABLE 2EFFECTS OF JENDRASSIK MANOEUVRFS

Unit Ilassi/ictiot, Verve Units (no.) Unitnluencedl Influenced(no.)

Vnubcr Typc of changc EAIG ± Torque Torqie on/Y

1. Deftilite spindle+ (2) 1

I. Peroneal 9 2 7 0,+ (4) 40±os,- (I1) 1

Tibial 4 2 2 + (1) l

11 Peroneal 4 2 2 (, + (2) 1 1Tibial 2 2 0

2. Probable spindle1a Peroneal 2 2 0

Tibial 2 2 0

Median 4 2 2 f + (1)

II ~~~~~Peroneal 0I 0,- II3. Tendon orci n

lbhIeroneal I 0INledian I (1)

30 (15) 5 1

The symbols +, -, 0 indicate an increase, a decrease, or no change in frequency. Nine fibres gave variable responses to different manoeuvres.The figzures in parentheses indicate the number of fibres which gave each particular response. The columns 'ENIG Torque' anid 'Torque onlyindicate whether those fibres which changed frequencv did so with detectable EMG in the receptor-bearing inuscle, or svith torque changesin the ibsence of recordable EMG.

FIG. 2 Lack of cffrc'40/s Of rein/orccnitent. A ait(I20/s s5/s B) repieselit r-espectit'elv

0 0 aftinger flexor groulp Ia0.3 Nm 3 Nm fibr-e anid a gastr'oc-- o nemtiuils groiup 11 fibre,

withii muscles mtiainitaiiedat comistalit lemigth.Traces are, frontt aboe,/r-equenci', torqulie, tmtte-uriatecl EMIG. Tinie

20/sa _ _ O 0 . 3 N(course oj the reicifjbrce-0.3 Nm meacit iniamtoeucr-e ts tn-

o (ldicated by the solid bar.L.M1 ~~~~~~InA a dleflectiomi in

°6°° tot)rqlie preced(eI theactctal mnamioeui're, biit

__ ccorrespontdedl itith theslibject 's prepat-atiomi

ori- the manioeuivre. C: respomise of a tibialis anitet iot grolip Ia aftereiet fibie dllrinig passive stretch. Tracesare, from aboe, frequency, joimit positioit, integrated EMG, fimiget flexor EMG (reinfbircenment mtiarker). D: a

perotteus mu(scle group Ia ajffrenit fibre dischai-gitg durinig the relaxation phases of electrically-inlduced pet-ottleusmuiscle twitches. The torqtie changes procituced hb' 12 twitches it ls hav-e beemi stiperimilposedl ill the uippertrace. The nieural i-espouises elicited by the first foiur twitches are stipet-imalposed in the secotid trace, those hbi thenext fout- twitches in the third trace, anld those bh' the last folur twitches int the lowest trace. A Jeldraassik mniamloe-uivre was perform-teed dta-intg twitches 5-8 (thi-cl ti-ace); twitches 1-4 atud 9-12 (sccond aimd lowtest traces) seticimigas comitrols. Dia-imig teinifoiceiient there is ito inlcrease itt niimnibei- of potentials, alid thic potentials (lo tiot OccuIearlier in thle relaxation2 phase.



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FIG. 3 Changes in' spindle dis-charge with coactivation of theextrafusal muscle. A and B are

20/' from a peronieus group Ia fibre.00 Traces are from above, frequency,0 joint position, integrated EMG

of the peronieus, anld EMGof the finger flexor muscles (re-iniforcement marker). In A, spindleactivationi coitncides wit/h the onsetof the manoeuvre but outlasts eachmanoeuvre anid correlates moreclosely with the unintentional cont-

1o/S tractioni that developed in theperoneal muscles. hi B the uti-intenttional conttractiont that devel-

0.5No~~~~~~~~~. sNm oped during thev eitiforcemestiIincreases spintdle frequency anid_1111111111F 11_ chansges the patternt of responise to

the stretching movements so that_____________________________ the spindle also discharges during

*muscle shortening. In C, the dis-charge of a tibialis anterior group II fibre increased slightly clurinig a Jenidrassik manoeuvre (indicated by thesolid bar) but this was correlated with a slight increase in torque (second trace) and the appearance of EMGpotentials from a single motor unit in tibialis aniterior muscle (third trace).

FIG. 4 Changes in spindledischarge cor-related withtorque changes. Tibialis ani-

0.3 Nm terior group Ia aJqfrent fibrewith nmuscle at constant lenigth(same uniit as in Fig. lB anid

I 0/s D). Traces are from above,-o torque, smoothed frequency

(as in Fig. IB), frequency,anid EMG of fitger flexormuscles (reiniforcement mar-

ker). In A, one Jelndrassik manioeuvre offour is associated with a significanit inicrease in discharge frequencybut this is correlated with ani increase in torque. The unit almost ceases firing whent torque falls at the end of themanoeuvre. In B, discharge frequency decreases in two manoeuvres, in parallel with torque. Prominent chanigesin torque andfrequency, indicated by the ar-row, occur before the first manoeuvre as the subject preparedfor it.

of the changes in firing frequency could always by the recordings in Fig. 3. The EMG potentialsbe correlated with the degree and direction of in A and B were visible in the direct EMGthe changes in the extrafusal muscle. recording only as a slight thickening of the back-

In the manoeuvres where a spindle response ground noise level, although their presence waswas accompanied by EMG activity in the more obvious when monitored on a loudspeakerreceptor-bearing muscle, the increase in fibre and displayed at lhigh gain after initegration (asfrequency was better correlated with the time in the Figure). In C the extrafusal contractioncourse of the EMG events than with the dura- was weak, as seen in the torque and EMGtion of the manoeuvre (Fig. 3). The necessity records. Indeed, the needle EMG electrodesfor careful monitoring of EMG is exemplified recorded potentials from only one motor unit

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.5s Nm

FIG. 5 Lack of effect of reinforcement on multiunit intrafascicular responses to stretch.Integrated multiunit afferent activity (upper trace) in response to stretch at 60°/s (A) and7.5°/s (B) from fascicles in the peroneal nerve supplying the anterior tibial muscle. Jointposition is seen in the second trace; third trace is integrated EMG in A and torque in B.The reinforcement manoeuvre is indicated by finger flexor EMG (lowest trace).

FIG. 6 Integrated neural re-

sponse recorded from a tibialnerve fascicle to gastrocnemius

1 Nm during percussion of Achillestendon. Five control tendon tapssuperimposed in A and five

-=- during a Jendrassik manoeuvrein B. Upper trace: torque

2 mV changes produced by percussionand by reflex contraction.Middle trace: integrated

neurogram, showing the afferent response to percussion, a small reflex efferent neural volley (only visible in B),and asynchronous afferent activity during relaxation ofthe reflex contraction. In both A and B the middle tracehas been delayed by 5 ms relative to the upper and lower traces so that the early afferent volley can be seenclearly. Lower trace: gastrocnemius EMG. Reinforcement results in a larger reflex contraction (EMG andtorque) for a constant percussion force. The afferent volley produced by percussion is not increased.

and, although more units were probably active,the coactivation may not have been recognizedhad surface electrodes been used and torquemeasurements not been available.

In those manoeuvres where a spindle responseoccurred without detectable EMG activity thechanges in discharge frequency could be cor-related with changes in torque. With some of

these manoeuvres the torque changes may havebeen due to active contraction of the receptor-bearing muscles not detected since the EMGelectrodes were not appropriately positioned torecord the potentials of the contracting muscleportions. However, in other manoeuvres (Fig. 4),the frequency changes were due to passivechanges in the receptor-bearing muscles result-

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FI_c. 7 Activationi of a Golgi telndoni orgaln10/s by Jendrassik mantoetuvres. Group lb fibre ino the deep fin1ger flexor mIuscle. Traces in

RAMA A and B are, from above, frequency,smoothed frequency (as in Fig. IB anidFig. 4), joinit positio7t (B only), integratedfinger flexor EMG. Durationi of reinforce-incelt mantoeuvres in7dicated by the solid bars.A: the subject tentsed the finger flexors Uf1-initenttiontally wheni preparing for the first

10/S l_ 9 | 1 _ manoeuvre intdicated by arrow, aiid did nloto- t1 l ln _| relax fully betweeni manioeuvres. Firin7g rate

_ 6s X _l ~~~~~~~~~~ofthe Uswtit iticreased with conltrac tionI.IIIIu IinI strenzgth. B: the subject tenised the finger

180 flexors durinig the conttrol passive stretch at_7.5 ls. Reintforcemenit accentuated the failure

033Nm of , elaxationi so that a higher firing rate,_was reached durinig mtiuscle stretch. Note thatcagainl the change in the integrated EMGpreceded the actual manoeulvre, coinciding

with the request to prepare for the manoeutre (indicated by arrow). C: unlit idenltificatioli usinig ani electrically-intduiced muscle twitch. Fibre discharges during the rising phase anid platealu of the twitch. Note that the stimuluhswas delivered throuigh the miticroelectrode, which wvas themi switched fir recording (blocking timne approximnatelY/0 ins). Upper trace: neurogram; lower trace: torque.

FIG. 8 Ilicri-ease in syvmpathetic eficrentactivity iniduced by reiniforcenmenit manoe-uvre. Muscle nerve sympathetic outtflow? ina perotieal muscle nerve fascicle shown asinitegrated nielural activity (middle trace),in a mnildly, hypertensive subject. Upper-

_ trace: respiratory mnovements; lower trace:*11I I Iintraarterial blood pressure. Reiniforceenticit

consisted of force~fd clenching of onie fist* * ~~~~~~~~~~~~~~~~~(indicatedbyv the solid bar) anid is associate(l

I ~~~~~~~~~Withchaniges in respiratoryv rhythin ai0(1blood pressure. The previouslY scantY pulsesynichr-onous mieurtal discharges bec-ontieprominienit during the manoeuvre.

inig fromi body displacemient or contractionl EFFECTS OF REINFORC'EMENT'ON MIULTItIJNIT IN IRA-of synergistic or antagonistic muscles. In Fig. FASCICULAR RECORDINGS Sinice data obtainied4 discharge frequency is positively correlated from single afferent nierve fibres miay be biasedwith the mechanical evenits as seeni in the by sampling errors, the effects of reiniforcemenlttorque recording. In different manoeuvres the manoeuvres were also studied in multiunlit initra-discharge frequency of this fibre increased, de- fascicular recordings--which are largely dominii-creased or did niot alter, largely parallelling the ated by la afferent fibres (Hagbarth anid Vallbo.extent and directioni of the change in torque. 1968; Wallin et al., 1973). Provided the subject

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remained relaxed, no evidence of increased neuralactivity attributable to the manoeuvres was seen,whether the appropriate muscle was at constantlength or being subjected to controlled passivestretch. In Fig. 5 the lack of effect of reinforce-ment on integrated neural activity is shownduring passive stretching at fast rates (A) andrelatively slow rates (B).

In Fig. 6 percussion of the Achilles tendonelicited an afferent neural discharge and a reflexcontraction of the triceps surae. The reinforce-ment manoeuvre performed in B produced in-creases in reflex torque and reflex EMG but noincrease in size of the afferent neural volley.This particular intrafascicular recording sitewas dominated by discharges in a relativelysmall number of fibres, and with careful filter-ing the discharges of a single la afferent fibrecould be discriminated. The reinforcementmanoeuvre also failed to affect the responseof this fibre to tendon percussion, although,as may be expected, a greater discharge was seenduring the relaxation phase of the enhancedreflex contractions.

EFFECTS OF REINFORCEMENT ON FIBRES OF NON-SPINDLE ORIGIN Occasionally neural activityother than that of muscle spindle origin wasseen to be modified during the performance ofa Jendrassik manoeuvre. Figure 7 illustratespotentials of a group lb afferent fibre from aGolgi tendon organ in the flexor digitorum pro-fundus muscle. During the reinforcement, thesubject unintentionally tensed the forearmmuscles, thus producing a greater dischargefrequency of the lb afferent fibre.

It has long been recognized that muscle workproduces vasoconstriction in resting muscles. Ina number of intrafascicular recording sites pulse-synchronous sympathetic vasoconstrictor activitywas seen, at times obscuring the afferent poten-tials. Figure 8 illustrates how fist clenchingcauses a marked enhancement of the sympa-thetic efferent activity recorded in a peronealmuscle nerve fascicle of a subject with mildhypertension. In some of the most forcefulJendrassik manoeuvres performed in the presentstudy the subjects sometimes held their breathand made an expiratory effort against closedglottis as in the Valsalva manoeuvre. As de-scribed in full elsewhere (Delius et al., 1972) and

confirmed in the present study, this type ofmanoeuvre is particularly potent in enhancingthe sympathetic pulse synchronous outflow tothe muscles.

DISCUSSION

It has been suggested previously that 'there isa marked increase of muscle spindle activity ina relaxed muscle during contraction of a remotemuscle' (Burg et al., 1974) and that this fusi-motor sensitization of the end organs contributesto the reflex reinforcement produced by theJendrassik manoeuvre. It has been further sug-gested that such effects are mediated at least inpart by selective activation of dynamic fusi-motor fibres (Szumski et al., 1974). With carefulmonitoring of the state of the extrafusal muscle,the present study has been unable to confirmthese assertions. Any change in spindle activitywas always accompanied by EMG or torquechanges involving the extrafusal muscle. Usingdifferent means of testing the position-and velo-city sensitivity of spindles, effects attributable toselective activation of static or dynamic fusi-motor fibres have been sought, but withoutsuccess.Were reinforcement manoeuvres capable of

selectively activating muscle spindles, then suchmanoeuvres could conceivably be used in futurestudies as a means of identification of a spindle.In the present study, however, only 5000 of thespindles tested altered discharge frequency dur-ing reinforcement manoeuvres, and in most ofthese the effects were variable, a decrease infrequency being occasionally recorded. Further-more, neural activity of other than spindle originwas seen to be affected by reinforcement manoe-uvres. Thus it is clear that a change in firingfrequency in response to the Jendrassik manoe-uvre is not a specific characteristic of musclespindles, and this criterion cannot be used as ameans of identification of spindles.Marked changes in sympathetic vasocon-

strictor outflow to the muscles may accompanyreinforcement manoeuvres. Indeed, in someintrafascicular recording sites the pulse syn-chronous sympathetic bursts have obscuredthe afferent activity primarily under study.Sympathetic stimulation is capable of modifyingspindle function in the cat (Hunt, 1960) and in

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man it has been suggested that adrenaline'sensitizes' muscle spindles, thus aggravatingspontaneous tremor and increasing the spindleresponse to vibration (Hodgson et al., 1969).However, the occurrence of profound changesin sympathetic outflow unaccompanied bychanges in muscle spindle activity, as seen inthis and earlier studies, provides evidence thatthe physiological effects of the sympatheticnervous system on spindle function in man arenegligible.

MECHANISMS OF REFLEX REINFORCEMENT In re-laxed muscles no evidence of increased dynamicspindle sensitivity has been found to accompanytendon jerk reinforcement. As suggested in Fig.6, the reflex enhancement noted during suchcontractions is due, not to a greater afferent in-put, but to altered processing ofthe afferent volleywithin the cord (cf. Clare and Landau, 1964).

Other mechanisms could, however, contributeto reflex reinforcement. Wartenberg (1953) hasadvocated that a deliberate weak contraction ofthe muscle to be tested is the best method ofreflex reinforcement. The present study suggeststhat few untrained persons would be able torelax completely in all distant muscles whenbeing encouraged to perform a forceful Jendras-sik manoeuvre. Therefore, many clinical re-inforcement tests are probably associated withunintentional contractions in the muscle to betested. We have observed that weak voluntarycontractions may be accompanied not only byincreased static spindle firing but also by in-creased dynamic spindle responses to tendonpercussion (unpublished observations). This,however, should not be taken as conclusiveevidence of an increased dynamic fusimotorinfluence. Any contraction alters the mechanicalstate of the muscle and it is conceivable that anincreased afferent percussion discharge is simplya reflection of a more effective transmission ofthe tendon percussion wave to the spindlereceptors.

PRINCIPLE OF ALPHA-GAMMA COACTIVATIONThe significance of the present results extendsbeyond the mere Jendrassik manoeuvre. Thefindings of Burg et al. (1974) implied an excep-tion to the principle of alpha-gamma co-activation in motor control. This principle

was established for human motor acts bystudies of isometric and isotonic voluntary con-tractions (Hagbarth and Vallbo, 1968; Vallbo,1970b, 1971, 1972, 1974). More recently, theprinciple has been shown to apply to rapidalternating movements (Hagbarth et al., 1975a)and the involuntary tremulous movements ofpatients with Parkinson's disease (Hagbarth et al.,1975b). In the present study, evidence has beenpresented that the unintentional postural adjust-ments and 'associated' movements that mayaccompany the performance of a consciouslydirected motor act are also carried out accordingto the principle of alpha-gamma coactivation.Although animal experiments have shown thatdifferential effects on the skeletomotor and fusi-motor systems can occur in conditioned move-ments (Buchwald and Eldred, 1962) and can beinduced by stimulation of different regions of thecortex, basal ganglia, and brain stem, the signifi-cance of these findings to the normal control ofmovements, particularly in man, is conjectural.Thus far, the recordings of spindle afferentactivity in awake human subjects have pro-vided increasing evidence that the supraspinalinfluences which control movement and postureare directed to the skeletomotor and fusimotorsystems in parallel. To date, the segmental phasicstretch reflex represents the only documentedexception to the principle of alpha-gamma co-activation (Burg et al., 1973, 1974; Hagbarthet al., 1975b).

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Vallbo, A. B. (1971). Muscle spindle response at the onsetof isometric voluntary contractions in man. Joutrnal ofPhysiology, 218, 405-431.

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Wallin, B. G., Hongell, A., and Hagbarth, K-E. (1973).Recordings from muscle afferents in Parkinsonian rigidity.In New Developments in EMG and Clinical Neurophysiology,vol. 3, pp. 263-272. Edited by J. E. Desmedt. Karger:Basel.

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