J. Neurol. Neurosurg. Psychit., 1971, 34, 231-235 Hmstrings stretch reflex in humn spsticity DAVID BURKE', J. D. GILLIES2, AND JAMES W. LANCE From the Division of Neurology, The Prince Henry Hospitl, Sydney, nd the School of Medicine, University of New South Wles, Austrli In 16 ptients with spstic prlysis the hmstrings stretch reflex ws found to increse S U NI MARY s the velocity of stretch incresed, nd generlly to subside fter movement cesed. These effects re ttributble to the dynmic property of the primry spindle ending. The stretch reflex commonly ppered in only the lst third of the stretching movement nd ws mximl s the knee becme fully extended. This is consistent with the sttic properties of the primry nd secondry spindle endings, nd ccounts for the bsence of the clsp -knife phenomenon in the spstic hmstrings. The difference in the nture of the stretch reflex in spstic flexor nd extensor muscles is best explined by the differentil reflex effects of group II fferent fibres which fcilitte flexor motoneurones nd inhibit extensor motoneurones. There ppers to be little difference in the properties of muscle spindles of flexor nd extensor muscles or in their sensitivity to dynmic nd sttic fusimotor control (Brown, Crowe, nd Mtthews, 1965; Lennerstrnd, 1968; Lennerstrnd nd Thoden, 1968, 1968b). However, the reflex effects of the secondry endings of flexor nd extensor spindles differ. With extensor spindles, ctivtion of the secondry ending produces utogenic inhibition of extensor motoneurones, so tht the effects of the primry nd secondry endings re ntgonistic. With flexor spindle endings the effects re synergistic, since ctivtion of flexor secondry endings produces utogenic fcilittion (Hunt nd Perl, 196). The stretch reflexes of flexor nd extensor muscl_s should therefore respond in different mnner to chnge in muscle length. In recent study of the spstic qudriceps muscle it ws found tht the stretch reflex decresed s the muscle ws stretched, producing the clsp-knife phenomenon, presumbly s result of stimultion of secondry endings (Burke, Gillies, nd Lnce, 197). A similr nlysis of the stretch reflex of the hmstrings muscles in humn spsticity hs now been undertken. 'Commonwelth Postgrdute Scholr nd Adolph Bsser Reserch F low in Neurology. 2Reserch Scholr of the Ntionl Helth nd Medicl Reserch Council of Austrli. MATERIALS AND NIETHODS Sixteen subjects were exmined. Eight were prplegic or qudriplegic fter trum to the spinl cord, nd one ws prplegic s result of spinl cord ngiom. In five of the subjects, the spinl cord lesion ws cliniclly complete. Five subjects suffered from multiple sclerosis nd two from fmilil spstic prplegi. In ll ptients the clinicl condition ppered to be sttic. The subjects were exmined when lying prone. The electromyogrm () produced by pssive stretch of the hmstrings muscles ws recorded by belly/tendon surfce electrodes 1 cm prt, nd integrted (time constnt -2 sec). The position of the knee joint ws mesured by goniometer, whose output ws differentited (time constnt 5 msec) to produce voltge proportionl to ngulr velocity. The direct, integrted, joint ngle, nd ngulr velocity were recorded on four-chnnel Offner dynogrph. The direct ws monitored on n oscilloscope to detect rtefct. Joint ngle ws lso monitored so tht ny given muscle length could be reproduced. Two methods of liner stretching were used. To determine the effect of the length of the stretching movement, stretches were commenced from vrying degrees of knee flexion, ech movement ending with the knee fully extended. To determine the sensitivity of the stretch reflex t different muscle lengths, the stretching movement from flexion to full extension ws divided into three sequentil steps of equl mplitude. The velocity of stretch ws mintined pproximtely constnt during ech movement, nd ech sequence ws repeted t different velocities. 231 J Neurol Neurosurg Psychitry: first published s 1.1136/jnnp.34.3.231 on 1 June 1971. Downloded from http://jnnp.bmj.com/ on 26 September 218 by guest.
232 Sinusoidl movements were used to confirm the results of liner stretching. The centre of oscilltion ws vried systemticlly, while the velocity nd mplitude remined constnt. Amplitudes of pproximtely 2 nd 4 were studied over rnge of velocities. The pek integrted of the hmstrings ws plotted ginst velocity of stretch, nd the clculted line of best fit ws determined by regression nlysis of those movements which produced. The threshold velocity required to produce stretch reflex ws tken s the intercept of the line of best fit on the velocity xis. Seprte clcultions were mde for the dt obtined t ech strting ngle (initil muscle length). Anlysis of covrince ws performed to determine the significnce of ny chnge in the : velocity reltionship following chnge in the initil muscle length. Probbility vlues were clculted from the vrince rtio (F) distribution. RESULTS Dvid Burke, J. D. Gillies, nd Jmes W. Lnce STRETCH REFLEX IN SPASTIC HAMSTRINGS On clinicl exmintion in ll ptients, the resistnce to stretch progressively incresed s the hmstrings were stretched, ws mximl when the muscles were fully stretched, nd subsided fter movement hd cesed. The clsp-knife phenomenon ws not observed. On repeted testing, the stretch reflex ftigued until, in most ptients, stble bse-line ws reched. In few ptients spsms frequently interrupted the exmintion nd it ws therefore difficult to obtin stble bse-line becuse stretch reflexes were generlly incresed fter spsm. In the prone position these spsms commonly involved both flexor nd extensor muscles, nd the limb often becme rigid in extension for the durtion of the spsm. These spsms were more frequent in ptients with complete cord lesions, nd were precipitted by extending the knee. Flexing the knee to 9 ws usully sufficient to control the spsms. VELOCITY OF STRETCH The reltionship between the velocity of liner stretch nd hmstrings ws exmined t severl strting ngles between 3 nd 135 of flexion. In few ptients with mrked spsticity, even the slowest movement evoked stretch reflex, but in most subjects threshold velocity could be determined, below which no stretch reflex ws produced. In either instnce, the hmstrings stretch reflex incresed with incresing velocity of pssive stretch (Fig. 1). At velocities below 3 /sec, this reltionship ppered liner (Fig. 2), but in seven ptients fster velocities of stretch produced disproportiontely greter reflex response. In one ptient the stretch reflex ppered to rech plteu s movements becme fster, but this ws not observed in ny other ptient. Velocity Integrted ].5mv FIG. 1. Velocity sensitivity of the hmstrings stretch reflex. With incresing velocity of liner stretch, the hmstrings stretch reflex increses, s seen by the incresing response. As in ll other digrms, stretching is represented by n upwrd deflection of the trce. i 3' 2 Z 11 go o OU*u O s* 5 seconds o 1O 2 3 4 VELOCITY OF STRETCH (1. FIG. 2. Linerity of the : velocity reltionship. Ech symbol represents seprte ptient. In ech of the three ptients the reflex response ppers linerly relted to the stretching velocity. U 13/sec +f19~~e _~~~~ o L J Neurol Neurosurg Psychitry: first published s 1.1136/jnnp.34.3.231 on 1 June 1971. Downloded from http://jnnp.bmj.com/ on 26 September 218 by guest.
_~~~~"wnnnvmnnnn~~~~~~~~~~~~~.n ntililllulnlpu ~~~~~~~~~~~~~~~~~~~~~ Hmstrings stretch reflex in humn spsticity 233 A similr reltionship between velocity of stretch Within the rnge of pek velocities used, up to nd reflex ws found t ech strting ngle 2 /sec, the reltionship ws gin liner (Fig. 5). nd there ws no significnt difference between the reltionships t ech ngle (P > 2). The threshold INITIAL MUSCLE LENGTH With liner stretching velocity nd the slope of the : velocity reltionship were thus not influenced by chnge in the initil not lter the resulting stretch reflex, provided tht chnge in mplitude of the stretching movement did muscle length (Fig. 3). the movements were crried through until the knee During sinusoidl movements of the limbs, n ws fully extended (Fig. 3). With sinusoidl stretching, increse in mplitude of the cycle did not increse in stretch reflex ws observed with increse in the pek velocity of the movement (Fig. 4, b). increse the mount of provided tht the pek velocity remined constnt (Fig. 4b, c).. 35 3 - I I i * So - (5, 2 2 5 1 z }D 1n *o. :o Stortrtg.3" 6 ' 3 r 9 oo 1 2 3 o Velocity of stretch ( /sec) 2 4 VELOCITY OF STRETCH (/sec) FIG. 5. : velocity reltionship with sinusoidl stretching. Ech symbol represents seprte ptient. FIG. 3. Lck of effect of vrying initil muscle length on In ech of the four ptients, the pek produced t the : velocity reltionship. No significnt difference the most extended position of the knee ppers linerly in the reltionship hs been produced by strting the movement from different position. cycle. relted to the pek velocity of the sinusoidl stretching b c Ti me seconds Velocity -in~wv99#~w9nf- ~ UW-I4 U W I 2 /sec _:5tiL.lt; -*lli!, _ I, i f go Integrted I_N 4. O-5mV FIG. 4. Sinusoidl stretching of the hmstrings. () nd (b) illustrte tht the reflex depends on the velocity of stretch, the pek velocity of the sinusoidl movement being greter in (b). (b) nd (c) show tht doubling the mplitude of the sinusoidl cycle does not produce greter stretch reflex if the pek velocity remins constnt. In ech record, ll from the sme ptient, the stretch reflex is produced only when the muscles re lmost fully stretched. In (b), it cn be seen tht this dependence on the degree of stretch is grded phenomenon. J Neurol Neurosurg Psychitry: first published s 1.1136/jnnp.34.3.231 on 1 June 1971. Downloded from http://jnnp.bmj.com/ on 26 September 218 by guest.
234 With stepwise liner stretching t constnt velocity, ws usully produced only by the third step of the movement, which reched the fully stretched position (Fig. 6). Occsionlly, t high velocities of stretch, smll response could be obtined during the intermedite step. At no time ws there ny response during the first step. With sinusoidl movements, the stretch reflex ws mximl when the limb ws oscillting in the extended position. As the point of oscilltion ws moved lo less extended position, the stretch reflex diminished (Fig. 4). This effect ws observed with both mplitudes of movement nd t ll velocities. Time Velocity Integrted FIG. 6. Stepwise liner stretching stretching movements of pproxim nd constnt velocity. A significnt duced only in the lst step which stretched length. Dvid Burke, J. D. Gillies, nd Jmes W. Lnce Time Integrted,,,. ^l ^/ ^ **^s seconds.. e- ' DURATION OF STRETCH REFLEX In most ptients the stretch reflex died wy fter movement cesed, FIG. 7. Sttic stretch reflex. A sttic stretch reflex on lthough the muscle remined stretched. The time mintined stretch, subsiding when the knee ws flexed, tken for the to subside ws vrible, especilly fter spsms, but ws generlly I to 2 sec. In in ptient suffering from multiple sclerosis. two ptients, the decresed over 4 to 8 sec nd low voltge f- MG persistedl. In nother ptient reflex of the spstic hmstrings muscle hs been the stretch reflex ws well minttined fter cesstion shown to ugment linerly with incresing velocity of movement (Fig. 7). In these three ptients, the once threshold hd been exceeded. This reltionof the knee. Of the ship is similr to tht found t ll velocities of ctivity cesed on flexion three, one hd n incomplete triumtic lesion of the stretch in the spstic qudriceps muscle (Burke et l., spinl cord nd two hd multipl e sclerosis. 197) nd presumbly results from the dynmic sensitivity of the primry spindle ending (Jnsen nd DISCUSSION Mtthews, 1962; Brown et l., 1965; Lennerstrnd, 1968). The nonlinerity t velocities exceeding 3 / At velocities of stretch less thn 3 /sec the stretch sec in some subjects is unexplined but is unlikely to be of significnce, since such velocities exceed those of physiologicl movement. V.. 4-' f 9 o2mv.sec,..xcdsthe stretch reflex ws produced only in the lst J Neurol Neurosurg Psychitry: first published s 1.1136/jnnp.34.3.231 on 1 June 1971. Downloded from http://jnnp.bmj.com/ on 26 September 218 by guest. prt of the stretching movement, ppering erlier 1 3W7 if the velocity of stretch ws incresed. Within this lst prt of the stretching movement, the dependence on length ws grded phenomenon, s seen in Fig. e 4b, nd either the primry or the secondry spindle ending could be responsible for this effect, since both re sensitive to length (Jnsen nd Mtthews, 1962; Bessou nd Lporte, 1962; Lennerstrnd, f 9 1968). However becuse of the short rnge of movement over which the stretch reflex ws produced, the contribution of incresing muscle length could not be ssessed quntittively. The resistnce to pssive movement produced by the stretch reflex ws mximl s the hmstrings becme fully stretched, so tht no clsp-knife phenomenon ws noted. By wy of contrst, the 2mV clsp-knife phenomenon is prominent in the spstic qudriceps muscle, since the stretch reflex diminishes s muscle length increses (Burke et l., 197). The tely equl mplitude differing effects of muscle length re consistent with stretch reflex is pro- ctivity in group II fferent fibres from secondry pproches the fully spindle endings, fcilitting flexor reflexes nd inhibiting extensor reflexes (Hunt, 1952, 1954;
Hmstrings stretch reflex in humn spsticity Lporte nd Lloyd, 1952; Eccles nd Lundberg, 1959; Hunt nd Perl, 196). Eccles nd Lundberg (1959) were unble to demonstrte flexor reflex fferent effects from stimultion of lrge joint fferent nerve fibres of low threshold, lthough such effects could be obtined with stimuli two to four times threshold. Skoglund (1956) found tht physiologicl stimultion of the knee joint produced only smll nd inconsistent reflex effects. It is therefore unlikely tht joint fferent fibres significntly ffect the hmstrings stretch reflex. Since Golgi tendon orgns respond selectively to ctive contrction of muscle (Jnsen nd Rudjord, 1964; Houk nd Hennemn, 1967), nd hve the sme utogenic inhibitory effect on flexors s on extensors (Binconi, Grnit, nd Reis, 1964), ctivtion of these receptors could not explin the different chrcteristics of the hmstrings nd qudriceps stretch reflexes. The presence of sustined reflex in response to mintined stretch in three ptients cn be ttributed either to sttic fusimotor drive, incresing the sttic response of the primry nd secondry endings (Brown et l., 1965; Lennerstrnd nd Thoden, 1968b), or to disinhibition of the group II fferent pthwy (Eccles nd Lundberg, 1959b; Holmqvist nd Lundberg, 1959, 1961). Ptients with complete spinl cord lesions in whom one would expect disinhibition of the group II pthwy to be mximl (Holmqvist nd Lundberg, 1959) did not show sustined response to stretch, presumbly becuse sttic fusimotor ctivity is miniml (Alnes, Jnsen, nd Rudjord, 1965). It is therefore pprent tht disinhibition of the group II fferent pthwy is not in itself sufficient to produce sttic stretch reflex. In view of this, incresed ctivity in sttic fusimotor fibres ppers the more likely explntion of the sttic stretch reflex found in the three ptients described, ll of whom hd prtil upper motor neurone lesions. The uthors wish to thnk the Ntionl Helth nd Medicl Reserch Council of Austrli nd the Adolph Bsser Trust for their continuing support of this project. Finncil ssistnce from Mr. nd Mrs. Edwin Street, The Rockdle Lions Club, nd Cib Co. Pty. Ltd. is grtefully cknowledged. Mr. P. D. Neilson, Mr. K. Norcross, nd Mr. N. Skuse hve ssisted with technicl problems. Illustrtions were prepred by the Deprtment of Medicl Illustrtion, University of New South Wles. REFERENCES 235 Alnes, E., Jnsen, J. K. S., nd Rudjord, T. (1965). Fusimotor ctivity in the spinl ct. Act physiol. scnd., 63, 197-212. Bessou. P., nd Lporte, Y. (1962). Responses from primry nd secondry endings of the sme neuromusculr spindle of the tenuissimus muscle of the ct. In S.ymposium on Muscle Receptors, pp. 15-119. Edited by D. Brker, Hong Kong University Press: Hong Kong. Binconi, R., Grnit, R., nd Reis, D. J. (1964). The effects of flexor muscle spindles nd tendon orgns on homonymous motoneurones in reltion to v-bis nd curriztion. Act physiol. scnd., 61, 348-356. Brown, M. C., Crowe, A., nd Mtthews, P. B. C. (1965). Observtions on the fusimotor fibres of the tibilis posterior muscle of the ct. J. Physiol. (Lond.), 177, 14-159. Burke, D., Gillies, J. D., nd Lnce, J. W. (197). The qudriceps stretch reflex in humn spsticity. J. Neurol. Neurosurg. Psychit. 33, 216-223. Eccles, R. M., nd Lundberg, A. (1959). Synptic ctions in motoneurones by fferents which my evoke the flexion reflex. Arch. itl. Biol., 97, 199-221. Eccles, R. M., nd Lundberg, A. (1959b). Suprspinl control of interneurones mediting spinl reflexes. J. Physiol. (Lond.), 147, 565-584. Holmqvist, B., nd Lundberg, A. (1959). On the orgniztion of the suprspinl inhibitory control of interneurones of vrious spinl reflex rcs. Arch. itl. Biol., 97, 34-356. Holmqvist, B., nd Lundberg, A. (1961). Differentil suprspinl control of synptic ctions evoked by volleys in the flexion reflex fferents in lph motoneurones. Act. physiol. scnd., 54, Suppl. 186, 1-51. Houk, J., nd Hennemn, E. (1967). Responses of Golgi tendon orgns to ctive contrctions of the soleus muscle of the ct, J. Neurophysiol., 3, 466-481. Hunt, C. C. (1952). The effect of stretch receptors from muscle on the dischrge of motoneurones. J. Physiol. (Lond.), 117, 359-379. Hunt, C. C. (1954). Reltion of function to dimeter in fferent fibers of muscle nerves. J. gen. PhYsiol., 38, 117-131. Hunt, C. C., nd Pern, E. R. (196). Spinl reflex mechnisms concerned with skeletl muscle. Physiol. Rev., 4, 538-579. Jnsen, J. K. S., nd Mtthews, P. B. C. (1962). The centrl control of the dynmic response of muscle spindle receptors. J. Physiol. (Lond.), 161, 357-378. Jnsen, J. K. S., nd Rudjord, T. (1964). On the silent period nd Golgi tendon orgns of the soleus muscle of the ct. Act physiol. scnd., 62, 364-379. Lporte, Y., nd Lloyd, D. P. C. (1952). Nture nd significnce of the reflex connections estblished by lrge fferent fibers of musculr origin. Amer. J. Physiol., 169, 69-621. Lennerstrnd, G. (1968). Position nd velocity sensitivity of muscle spindles in the ct. I. Primry nd secondry endings deprived of fusimotor ctivtion. Act physiol. scnd., 73, 281-299. Lennerstrnd, G., nd Thoden, U. (1968). Position nd velocity sensitivity of muscle spindles in the ct. II. Dynmic fusimotor single-fibre ctivtion of primry endings. Act physiol. scnd., 74, 16-29. Lennerstrnd, G., nd Thoden, U. (1968b). Position nd velocity sensitivity of muscle spindles in the ct. IlI. Sttic fusimotor single-fibre ctivtion of primry nd secondry endings. Act physiol. scnd., 74, 3-49. Skoglund, S. (1956). Antomicl nd physiologicl studies of knee joint innervtion in the ct. Act physiol. scnd., 36, Suppl. 124, 1-11. J Neurol Neurosurg Psychitry: first published s 1.1136/jnnp.34.3.231 on 1 June 1971. Downloded from http://jnnp.bmj.com/ on 26 September 218 by guest.