J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.32.6.541 on 1 December 1969. Downloaded from

J. Neurol. Neurosurg. Psychiat., 1969, 32, 541-547

Methods of tendon jerk reinforcement The role of muscle activity in excitability

KENNETH H. OTT1 AND M. MICHAEL GASSEL2 From the Department ofNeurology, University of California School ofMedicine, San Francisco, California, U.S.A.

This study was designed to reconcile the following the tendon tap was about 55 msec. This delay was clinical observations: subjects with anxiety repre- measured before each experiment. The solenoid driven sented in muscle tension generally have hyperactive reflex hammer had a built-in microswitch which closed tendon jerks. Yet, muscle tension evidenced by in- the circuit on percussion and triggered the sweep of the electromyograph. A regular and stabilized blow was complete relaxation frequently results in reflex delivered. A control series of maximal was depression and the can only be elicited at a frequency of one every 10 seconds. Initially elicited by having the subject 'relax'. Under con- 20 reflexes were averaged by computer (CAT 1000) in guest. Protected by copyright. sideration were the observations by Hoffmann (1922) establishing the control and test values. In later studies and by Hagbarth (1962) that a moderate amount of it was usually feasible to average just eight reflexes, when voluntary activity facilitates the monosynaptic control variations were small. The controls were repeated reflex in the muscle tested. A problem to be inves- at intervals during the investigation and are indicated in tigated was the relationship of the facilitation the graph at the appropriate test intervals. produced the The amplitude of a series of ankle jerk reflexes was by Jendrassik manoeuvre, during measured during minimal, moderate, and intense degrees forceful contraction of distant muscles masses, to of isometric contraction of the ipsilateral and contra- that produced by voluntary activity in the same lateral triceps surae, and ipsilateral pre-tibial groups. muscle. Numerous other techniques have been The electrical activity from these muscles was recorded reported to be useful in facilitating reflexes, ostensibly with non-insulated subcutaneous needle electrodes. The through an effect on muscle activity. Cutaneous potentials were amplified, displayed, and photographed stimuli, such as needleprick, cold or warm baths, on the DISA 3-channel electromyograph. The audio- pinching, electrical shock, or manipulation of amplifier of the electromyograph was utilized to allow muscles have been variously reported to reinforce the subject to maintain constancy of the desired degree of activity. the tendon jerks. It has been suggested that the The ankle jerk was also conditioned by the Jendrassik effectiveness of these manoeuvres is related to the manoeuvre. The manoeuvre consisted of brisk and strong distraction of attention, assisting the relaxation of contraction of the subject's interlocked fingers on the muscles held in high tension (Wartenberg, 1945). command 'Pull', and the quick relaxation with the com- mand 'Release'. Duration of the manoeuvre was about

METHODS two seconds, with the onset and termination marked on http://jnnp.bmj.com/ the photographic recording. Fifteen normal subjects were examined. Subjects were Finally, the recovery of the ankle jerk reflex after placed in a prone position with legs extending over the nociceptive cutaneous stimulation was measured. A end of the couch. The legs were supported firmly in a DISA Multistim stimulator was utilized with a maximal heavy metal frame which was fixed to a metal stand voltage output, via transformer, of 250 V. Single 3 msec separate from the couch. The leg frame was adjustable in duration pulses were delivered to the skin through sub- height and angle. An automatic solenoid hammer was cutaneous stainless steel needle electrodes placed 2 cm attached to the leg frame by a metal supporting device apart. The conditioning shock was followed at intervals with two complex joints. These joints permitted move- ranging from 20 to 8,000 msec by the ankle jerk reflex. on September 23, 2021 by ment of the hammer in all directions and made it possible Skin sites stimulated in this investigation were the to position the hammer at a fixed distance (3 cm) directly ipsilateral mid buttock and ipsilateral mid anterior arm. over the Achilles tendon. The solenoid was triggered from the stimulator (DISA Multistim) and the delay to RESULTS 'Medical Student; USPHS Research Fellowships FR-05355-07 and NB-5101-13. The ankle jerk reflex was facilitated by mild degrees 2This work was supported by NIH Grant NB-07562. of activity in the ipsilateral triceps surae; moderate 541 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.32.6.541 on 1 December 1969. Downloaded from

542 Kenneth H. Ott and M. Michael Gassel

1.1 _ - z \ ACTIVITY IN TRICEPS SURAE L 92 \ 0----I IPSILATERAL

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0.6 +++ 0.1 mvI INCREASING ACTIVITY IN TRICEPS SURAE (+_+++) 100 MSEC guest. Protected by copyright. FIG. la. Average amplitude of 20 ankle jerk reflexes during minimal (+), moderate (+ 4-), and intense (+ + 4 ) levels of voluntary activitv on the ipsilateral (O ) and contralateral (0) triceps surae in a representative subject. These averaged values have been normalized to control values. The insets are electromyograms (EMGs) ofthe three levels ofactivity. levels of activity resulted in no change or mild Jendrassik manoeuvre and that of voluntary activity depression, while more intense contraction markedly (see Fig. 1). Maximal facilitation of tendon jerks inhibited the ankle jerk. was achieved by simultaneous performance of the Minimal activity in the contralateral triceps surae Jendrassik manoeuvre with maintained minimal produced no change in the reflex, moderate activity voluntary activity in the muscle tested. Computer evoked little or no facilitation, and a mild degree of averages of the amplitudes of the reflexes during facilitation occurred with intense activity in the the combined manoeuvres were variable. It was contralateral triceps surae. therefore necessary to photograph long series of Figure 1 illustrates representative effects on the individual records, because of the considerable ankle jerk at each of three levels of activity in the variability of the frequency of motor unit discharge ipsilateral and in the contralateral triceps surue. during the Jendrassik manoeuvre (Fig. 3). The most There was considerable variation in the extent of regular change was the striking decrease in the ankle facilitation between subjects and to lesser extent in jerk with the decrease in motor unit activity during the same subject on differernt occasions. The con- performance of the Jendrassik manoeuvre. The http://jnnp.bmj.com/ clusions are based upon investigative sessions lasting conclusions regarding occlusive interaction were one and a half to two hours. Four of 15 volunteers based upon those studies in which there was no were studied on two or more occasions. change in tonic motor unit firing. Activity in antagonist pre-tibial muscle inhibited It was possible to add facilitatory and inhibitory the reflex, and inhibition increased with increasing effects in some dexterous subjects. Simultaneous degrees of antagonist activity. Concurrent activity performance of the Jendrassik manoeuvre, main- in the ipsilateral triceps surae and pre-tibial muscles tained tonic activity of mild degree in the agonist, usually resulted in inhibition, although of less and activity in the antagonist resulted in mitigation on September 23, 2021 by marked degree than with antagonist action alone of the facilitation. In a number of subjects inhibition (Fig. 2). by antagonist activity was prepotent. The extent of facilitation produced by the Jendras- The effect of cutaneous stimulation upon the sik manoeuvre was of about the same order as that ankle jerk was evaluated initially by pinprick of evoked by mild activity in the agonist. There was widespread skin areas. The ankle jerk was highly occlusive interaction between the facilitation of the variable. Therefore, the skin was stimulated through J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.32.6.541 on 1 December 1969. Downloaded from

Methods oftendon jerk reinforcement: the role ofmuscle activity in reflex excitability 543

.A VOLUNTARY ACTIVITY

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11 FIG. lb. Computer (CAT 1000) average of 20 ankle jerk reflexes during minimal (upper trace), moderate (middle trace), and sub- maximal voluntary activity (lower trace) in the ipsilateral triceps surae.

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subcutaneous electrodes fixed in place, which made augmented the ankle jerk in the same muscle. The it possible to deliver a regular and unvarying condi- immediate consideration was to determine the tioning stimulus with a single shock to the skin. The extent to which the reflex enhancement was localized stimulus was followed by an ankle jerk at regulated to the active muscle, or represented the local reflec- intervals. The motoneurone excitability changes tion of a more generalized facilitation with muscle were then evaluated by the classical recovery curve activity as produced in the Jendrassik manoeuvre. was that the tonic activation of the of the monosynaptic reflex. It found slight http://jnnp.bmj.com/ There was striking facilitation of the ankle jerk triceps surae which facilitated the ankle jerk maxim- with single-shock cutaneous stimulation of both the ally produced no contralateral reflex reinforcement. ipsilateral mid anterior arm and mid buttock. This Indeed, facilitation first appeared during maximal began at 20 to 60 msec and ended at about 200 to tonic contraction of the contralateral triceps surae 250 msec, when it was followed by a mild and vari- at a level of activity which, in the ipsilateral muscle, able degree of inhibition before the reflex returned produced depression of the reflex. The facilitation to control levels. There was no muscle discharge of the ankle jerk with intense activity only of the

evoked by the single-shock stimulus. Ten normal contralateral triceps surae could be related to the on September 23, 2021 by subjects were studied and representative recovery generalized facilitation of monosynaptic reflexes by curves of the monosynaptic reflex are illustiated in distant muscle activity as in the Jendrassik man- Fig. 4. oeuvre; however, group lB tendon afferents excited by the intense activity likewise facilitate contra- DISCUSSION lateral triceps surae motoneurones (Perl, 1958). There is evidence bearing on the mechanism by It would appear that in this large extensor muscle which tonic voluntary activity in the triceps surae mass voluntary activation is manifested by an J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.32.6.541 on 1 December 1969. Downloaded from

544 Kenneth H. Ott and M. Michael Gassel

+ order when flexion 1.5r activated by the polysynaptic reflex, by voluntary activity, or with the mono- + synaptic reflex. They also reported interaction 1.25k + between voluntary and reflex activation. It does not, uX of course, follow that voluntary activation is pro- -a A ++A A A A 1.0k A duced solely by an increase in excitability of the

I motoneurone pool. The specific and discrete move- 0.75[- ments possible in muscles, such as those of the hands, presupposes this is a regular mechanism; specific patterns of inhibition and activation must o.5L be involved. A-CONTROL The inhibition of the ankle jerk with intense or J - JENDRASSIK MANOEUVRIE sometimes with only moderate muscle activity +, ++, +++ - INCREASING ACTIVITY OF could be related to a number of factors. There is TRICEPS SURAE occlusion of the reflex with active motor units and (-+ ACTIVITY OF TRICEPS SU)RAE with those in the refractory phase afterdischarge. AND ANTEROLATERAL MUUSCLES The increase of muscle tension with strong tonic +- + ACTIVITY AND JENDRAISSIK MANOEUV'E activity provides a stimulus to group lB tendon afferents, with resulting autogenic inhibition. Re- FIG. 2. The averaged amplitude of 2(g ankle jerk reflexes current inhibition through recurrent collaterals is conditioned by various means are pPlotted serially with also undoubtedly operative. It is of interest that corresponding controls. The effect on reflex amplitude is significant recurrent inhibition does not occur withguest. Protected by copyright. illustrated with increasing levels of v Voluntary activity in single unit firing. Recunent collaterals produce a the ipsilateral triceps surae, JencIrassik manoeuvre, widespread inhibition affecting flexors and extensors simultaneous and ipsilateral agonist antagonist activity, in local spinal segments. However, the inhibition and minimal agonist activity and the Je?ndrassik manoeuvre concurrently performed. does not spread to affect the contralateral moto- neurones (Holmqvist, 1961); and this may account, in part, for the facilitation with maximal activity increase in the subliminal fringe of the motoneurone in the contralateral triceps surae at a level of activity pool innervated, as tested by the amplitude of the which produced pronounced depression of the monosynaptic reflex, as well as by motoneurone ipsilateral ankle jerk. discharge. Not only is voluntary activation asso- The inhibition of the reflex with activity of the ciated with an increase in motonei urone excitability, antagonist muscles was occasionally striking. In but conversely changes in motoneurone excitability some subjects even slight activity in the antagonist produce a modulation of motor unit firing during overcame potent facilitation. This effect may be tonic activation (Gassel and Ott, 1S)69). This suggests related to reciprocal innervation. It is also possible that voluntary activation is effecte( dthrough changes that group IA fibres are excited indirectly through in excitability of the motoneuronte pool. Evidence fusimotor activation, which could produce direct of the reactivity of tonic motor un:it discharge in the inhibition of the extensor motoneurones (Eccles, triceps surae to changes in mc)toneurone excit- Fatt, and Landgren, 1956). Group 1B fibres from ability was obtained by comparinjg the effects upon pre-tibial flexors produced no effect on ankle http://jnnp.bmj.com/ motoneurone discharge, to the r-ecovery curve of extensors (Eccles, Eccles, and Lundberg, 1957). monosynaptic reflex, which had earlier been estab- The extent of the facilitation by the Jendrassik lished by the same segmental stinnulus. In general, manoeuvre was of about the same order as that it was found that conditionin, g stimuli which evoked with slight activity of the muscle tested. inhibited the monosynaptic reflex also depressed There was occlusive interaction between the facilita- tonic voluntary activity, and thlat stimuli which tion of the Jendrassik manoeuvre and that of augmented the ankle jerk also facil:itated tonic firing, voluntary activity. Maximal facilitation of tendon although there was sometimes inhibition which jerks was achieved by simultaneous performance of on September 23, 2021 by preceded or followed facilitation (Gassel and Ott, the Jendrassik manoeuvre with maintained minimal 1969). It had earlier been establisi hed that slight or voluntary activity in the muscle tested. The occlusive moderate voluntary activity decrea ases the threshold interaction is not unexpected, as both the Jendrassik and augments the monosynaptic reflex from the manoeuvre (Gassel and Diamantopoulos, 1964b) same muscle (Hoffmann, 1922; Hagbarth, 1962). and voluntary activity in the muscle tested by the Ashworth, Grimby, and KugeltxDrg (1967) found monosynaptic reflex (see above) produce a direct that motor units were usually recruited in the same effect on the excitability of the motoneurone pool. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.32.6.541 on 1 December 1969. Downloaded from

Methods of tendon jerk reinforcement: the role ofmuscle activity in reflex excitability 545

CONTROL 5.0 mv

5.0 mv

0.1 mY

0.1 mS ANTEROLATERAL MUSCLES guest. Protected by copyright. r 100 MSEC

tJENDRASSIK MANOEUVRE ANKLE JERK

FIG. 3. DISA recording of a single ankle jerk reflex with moderate voluntary activity in ipsilateral triceps surae and during simultaneous performance of the Jendrassik manoeuvre. Upper and middle traces are parallel EMGs from the triceps; the lower trace is the EMG from the ipsilateral pre-tibial muscles. The amplification of the middle and lower traces is 50 x that in the upper trace. The Jendrassik manoeuvre is marked on the lower trace. Inset is a control reflex, unconditioned bAy voluntary activity or the Jendrassik manoeuvre.

3 ARM http://jnnp.bmj.com/ FIG. 4. The recovery curve of the mono- LL A synaptic reflex (anklejerk) testedfrom a W population oftriceps surae motoneurones i I ~~~IIII A IT.S. CL with conditioning stimulus to the ipsilateral :I- mid anterior arm and mid buttock. Each graphic point represents the averaged value ofeight reflexes normalized to 1.4- controls. BUTTOCK on September 23, 2021 by 1.2 n s A / N.M.

I 2080I40 60 II o 20 40 60 80 100 200 600 1000 8000 M. SEC J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.32.6.541 on 1 December 1969. Downloaded from

546 Kenneth H. Ott and M. Michael Gassel The importance of muscle tension in reflex activity present study. Patterns of excitability change, pre- is well established and it has even been suggested dominantly extensor facilitation, were evoked from that some level of muscle activity is a prerequisite widespread cutaneous areas of the upper and lower for the evocation ofa reflex. Certainly, monosynaptic extremities, back, and face; that evoked on stimula- reflexes are reduced or absent in the extreme relaxa- tion of the ipsilateral arm and buttock is illustrated tion of sleep; however, during the various stages of in Fig. 4. sleep, there are complex influences on spinal moto- Clearly, stimulation of cutaneous afferents can neurones excitability. There is a tonic inhibition of facilitate monosynaptic reflexes without effecting the monosynaptic reflex throughout desynchronized discharge of motoneurones. The influence on sleep and a phasic inhibition during rapid eye motoneurone excitability of a cutaneous stimulus movements (REM) (Gassel, Marchiafava, and will depend upon the character of the stimulus, the Pompeiano, 1964). The tonic inhibition is a result of timing of the ankle jerk after the conditioning descending impulses producing post-synaptic in- stimulus, as well as the area of the skin stimulated. hibition and the phasic change attributable to pre- synaptic inhibition (Gassel, Marchiafava, and Pompeiano, 1965). During REM myoclonic twitches SUMMARY occur predominantly and are related to descending facilitatory volleys which mitigate the phasic The role of muscle activity in reflex excitability was inhibition of the monosynaptic reflex. There is also investigated in 15 normal subjects, utilizing a a particular depression of fusimotor activity during regulated system for eliciting the ankle jerk and desynchronized sleep and during spindle bursts of recording muscle activity from agonist and ant-

synchronized sleep (Gassel and Pompeiano, 1965). agonist. Minimal degrees of voluntary activity inguest. Protected by copyright. The antagonistic influences converge on the moto- the same muscle facilitated the ankle jerk; greater neurone pool where a quantitative interaction degrees produced inhibition. Facilitation first occurs, reflected in the response of the subliminal appeared during maximal contraction of the contra- fringe whose excitability is evaluated by changes in lateral triceps surae at a level of activity which, in the amplitude of the monosynaptic reflex. the ipsilateral muscle, produced depression of the The tendon jerks are evoked without preceding reflex. Occlusion was demonstrated between facili- muscle activity in a vast majority of normal subjects, tations by voluntary activity in the muscle tested and it can be demonstrated that the augmentation and by the Jendrassik manoeuvre. Activity in of tendon jerks with the Jendrassik manoeuvre antagonist muscles inhibited the reflex, overcoming occurs without associated activity in the muscle potent facilitation. Maximal facilitation of tendon tested (Gassel and Diamantopoulos, 1964a). jerks is achieved by simultaneous performance of The primary response on stimulation of cutaneous the Jendrassik manoeuvre with maintained minimal afferents is ipsilateral withdrawal involving excita- voluntary activity in the muscle tested. Single-shock tion of flexor and inhibition of extensor moto- stimulation of widespread areas of the skin can neurones. However, this response is not invariable facilitate monosynaptic reflexes without effecting and the occasional occurrence of extensor responses discharge of motoneurones. The precise pattern of on stimulation of ipsilateral cutaneous were excitabilitychangewitha cutaneous stimulus depen4ds early reported by Brown and Sherrington (1912), upon the character of the stimulus, the timing of the ankle after the and Creed, Denny-Brown, Eccles, Liddell, and jerk conditioning stimulus, as well as http://jnnp.bmj.com/ Sherrington (1932). Hagbarth (1952) found that the area of the skin stimulated. The mechanisms of extensor muscles were excited by stimulation of the various means of facilitation oftendonjerks were skin areas located directly over the muscle, in spinal discussed as was the interaction of these augmenta- and decerebrate cats. Kugelberg, Eklund, and tions with that produced by voluntary muscle Grimby (1960) studied the nociceptive reflexes of activity. the lower limb in humans after delivering trains of cutaneous stimuli; reflex responses were sometimes REFERENCES

recorded in the gastrocnemius on strong stimula- on September 23, 2021 by tion of the skin of the dorsum of the foot or of the Ashworth, B., Grimby, L., and Kugelberg, E. (1967). Comparison buttock. of voluntary and reflex activation of motor units; functional Single-shock stimulation of areas of the organization of motor neurones. J. Neurol. Neurosurg. skin in normal human subjects produces a reliable Psychiat., 30, 91-98. pattern of excitability in the surae Brown, T. G., and Sherrington, C. S. (1912). The rule of reflex change triceps response in the limb reflexes ofthe manunal and its exceptions. motoneurones (Gassel and Ott, 1969). There was no J. Physiol. (Lond.), 44, 125-130. muscle discharge in the course of the Creed, R. S., Denny-Brown, D., Eccles, J. C., Liddell, E. G. T., and excitability Sherrington, C. S. (1932). Reflex Activity of the . changes evoked by the single-shock stimulus in the Clarendon Press: Oxford. J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.32.6.541 on 1 December 1969. Downloaded from

Method of tendonjerk reinforcement: the role of muscle activity in reflex excitability J I 547

Eccles, J. C., Fatt, P., and Landgren, S. (1956). Central pathway for -, and Pompeiano, 0. (1965). Fusimotor function during sleep in direct inhibitory action of impulses in largest afferent unrestrained cats. An account of the modulation of the fibres to muscle. J. Neurophysiol., 19, 75-98. mechanically and electrically evoked monosynaptic reflexes. Ibid., 103, 347-368. A. actions on Eccles, R. M., and Lundberg, (1957). Synaptic -, and Ott, K. H. (1969). Nature (Lond.), in press. motoneurones caused by impulses in Golgi tendon organ Hagbarth, K.-E. (1952). Excitatory and inhibitory skin areas for afferents. J. Physiol. (Lond.), 138, 227-252. flexor and extensor motoneurones. Acta physiol. scand., 26, Gassel, M. M., and Diamantopoulos, E. (1964a). The Jendrassik Suppl. no. 94. maneuver. I. The pattern of reinforcement of monosynaptic -(1962). Post-tetanic potentiation of myotatic reflexes in man. reflexes in normal subjects and patients with spasticity or J. Neurol. Neurosurg. Psychiat., 25, 1-10. rigidity. Neurology (Minneap.), 14, 555-560. Hoffmann, P. (1922). Untersuchungen uber die Eigenreflexe (Sehnen- reflexe) menschlicher Mfuskeln. Springer: Berlin. - (1964b). The Jendrassik maneuver. II. An analysis of the Holmqvist, B. (1961). Crossed spinal reflex actions evoked by volleys mechanism. Ibid., 14, 640-642. in somatic afferents. Acta physiol. scand., 52, Suppl. no. 181. Kugelberg, E., Eklund, K., and Grimby, L. (1960). An electro- Marchiafava, P. L., and Pompeiano, 0. (1964). Tonic and phasic inhibition of spinal reflexes during deep, desynchronized myographic study of the nociceptive reflexes of the lower limb. sleep in unrestrained cats. Arch. ital. Biol., 102, 471-499. Mechanism of the plantar responses. Brain, 83, 394410. Perl, E. R. (1958). Crossed reflex effects evoked by activity in myelin- , ,-(1(1965). Modulation of the recurrent discharge of ated afferent fibers of muscle. J. Neurophysiol., 21, 101-112. alpha motoneurons in decerebrate and spinal cats. Ibid., 103, Wartenberg, R. (1945). The Examination of Reflexes. Year Book 1-24. Publishers: Chicago, Ill. guest. Protected by copyright. http://jnnp.bmj.com/ on September 23, 2021 by