Physiological mechanisms of rigidity Parkinson's disease · dorsiflexion stretch were studied in 17 patients with Parkinson's disease. Mostpatients showed Mostpatients showed increased

Journal of Neurology, Neurosurgery, and Psychiatry 1983;46:45-53

Physiological mechanisms of rigidity in Parkinson'sdiseaseA BERARDELLI,* AF SABRA, M HALLETT

From the Rehabilitation Engineering Center at Harvard-MIT, the Section ofNeurology, Department ofMedicine, Brigham and Women's Hospital and Department ofNeurology, Harvard Medical School, Boston,USA

SUMMARY Electromyographic responses of triceps surae and tibialis anterior produced bydorsiflexion stretch were studied in 17 patients with Parkinson's disease. Most patients showedincreased muscular activity when attempting to relax. A few patients showed an increase ofshort-latency reflexes when relaxed and when exerting a voluntary plantarflexion prior to thestretch. Many patients showed long-latency reflexes when relaxed and all but one showed long-latency reflexes with voluntary contraction; and these reflexes were often larger in magnitude andlonger in duration than those seen in normal subjects. Unlike the short-latency reflex, thelong-latency reflex did not disappear with vibration applied to the Achilles tendon. The long-latency reflexes and continuous responses to slow ramp stretches were diminished at a latencysimilar to the beginning of long-latency reflexes when the stretching was quickly reversed.Dorsiflexion stretch also frequently produced a shortening reaction in tibialis anterior. Of all theabnormal behaviour exhibited by the Parkinsonian patients only the long-latency reflex magnitudeand duration correlated with the clinical impression of increased tone. The mechanism of thelong-latency reflex to stretch which is responsible for rigidity is not certain, but the present resultsare consistent with a group II mediated tonic response.

One of the major manifestations of Parkinson'sdisease is rigidity. The only symptom unequivocallyproduced by rigidity is a feeling of stiffness. As aclinical sign, however, this term refers to thephenomenon of increased resistance when stretchinga muscle passively. Although some features of rigidityhave been characterised, the detailed physiology isstill unknown. Possible mechanisms include anexaggeration of the monosynaptic stretch reflex, anexaggeration of the long-latency stretch reflexes, thedevelopment of a tonic stretch reflex and the,development of a shortening reaction.The possibility of exaggeration of long-latency

stretch reflexes has received much recent attention.

Address for reprint requests: Mark Hallett, MD, Section ofNeurology, Brigham and Wonien's Hospital, 75 Francis Street,Boston, Ma 02115, USA.

* Present address: Laboratorio di Neurofisiologia, V ClinicaNeurologica, Universita di Roma, Italy.

Received 20 November 1982 and in revised form 24 June 1982

Accepted 3 September 1982

Lee and Tatton' observed an enhancement of thelong-latency stretch reflexes of the wrist flexors andextensors in subjects with Parkinson's disease. Theseresults have been confirmed by Mortimer andWebster23 in biceps brachii and by Chan et al4 intibialis anterior. Marsden et all ascribed an increaseof long-latency reflexes of the flexor pollicis longus tothe fact that subjects with Parkinson's disease are nottruly relaxed at rest and have only an apparentincrease of the long-latency reflexes.We have studied the EMG responses of triceps

surae and tibialis anterior to passive dorsiflexion ofthe ankle in a group of patients with Parkinson'sdisease. This attempt follows our recentdemonstration of long-latency stretch reflexes intriceps surae6 and seeks further understanding ofwhich mechanisms are responsible for the rigidity.

Materials and methods

The study was performed on 17 patients with Parkinson'sdisease ranging in age from 40-80 years, who gave infornedconsent to participate. The signs, symptoms, andmedications of the patients are noted in the table. Rigiditywas assessed clinically prior to the study. Methods for

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Table Clinical and physiological data

Patients Duration of Rigidity Background Magnitude LLR Medicanonsillness (yr) at rest torque

SLR* LLRt SLR* LLRt duration (rns)no torque torque

1 1½/2 Normal 6% 3 1 5 1 41 Sinemet 10/1003 x day2 3 Mild 6% 5 1 13 1 42 Sinemet25/2503 x day3 4 Mild 11% 81 0 78 2 23 Sinemet25/2506 x day4 14 Mild 10% 40 0 28 2 33 Sinemet 10/1006 x day

Artane 2 mg 3 x daySymmetrel 100mg 2 x dayInderal 40 mg s x day

5 1 Mild 12% 14 1 20 1 43 None6 2 Mild 9% 50 0 32 1 26 None7 2 Moderate 25% 8 2 23 0 0 Sinemet 25/2503 x day8 1 Moderate 20% 18 1 13 2 73 Sinemet 25/250 4 x day9 4 Moderate 10% 8 1 20 1 60 Lithium 300 mg 3 x day10 4 Moderate 12% 19 1 19 2 74 Sinemet 10/100 4 x day11 4 Moderate 8% 7 2 8 2 79 Sinemet 10/100 5 x day

Bromocriptine 2 5 mg s x day12 4 Moderate 4-5% 2 1 5 2 71 Sinemet 10/100 5 x day

Artane 1 mg 3 x day13 8 Moderate 12% 6 0 - - - L-Dopa 3 x day

Artane 2 mg 4 x day14 3 Moderate 19% 10 1 10 1 71 Sinemet 12 5/125 6 x day

Symmetrel 100 mg 2 x dayKemadrin 5 mg 4 x day

15 20 Severe - - - 18 2 68 Pagitone 1 25 mg2 x day16 4 Severe 20% 33 2 - - - Sinemet 10/1007 x day17 4 Severe 10% 34 2 77 2 38 Sinemet 10/100 6 x day

* The magnitude of the SLR for each patient is the value of the EMG at 3600'/s2 acceleration which is obtained from linear interpolation fromthe actual data points.t For the LLR, 0 means absent, 1 means normal for the amount of background contraction and 2 means abnormally large magnitude for at leastone acceleration value.- means not studied.

studying the EMG responses of triceps surae and tibialisanterior have been described in detail in an earlier paper.'Briefly, the subject sat in a chair with the knee flexed at 900with the foot strapped to a platform which was attached to thespindle of a torque motor. A strain gauge was incorporatedinto the platform so that the torque exerted by the subjecton the platform could be measured and this information wasmade available to the subject by deflection of a meterneedle. Using a PDP 11/10 computer and a feedback circuitthe platform could be programmed to make ankledisplacements at different velocities. The platform reachedthe specified velocity in approximately 50 ms. EMG withsurface electrodes was recorded from triceps surae andtibialis anterior. The EMG signals, angular position of theankle and the torque on the platform, were sampled by thecomputer at 2 ms intervals. The EMG was rectified andfiltered before collection. The latency of the EMG reflexeswas measured from the electronic command to move thepedal (thus clearly overestimating the biological latency).The durations were measured by visual inspection and theamount of EMG activity in each burst was measured byintegration. The integration values were normalised to theEMG activity produced with a maximal voluntary effort(method 2 from reference 6). Hence activity equallingmaximum voluntary effort was given a value of 100.The initial angle of the ankle was - 100 and at random

times the ankle was dorsiflexed to +50 at one of threespecified velocities, 1000, 1500 or 2000/s. Each velocity was

repeated 10 times and the results were averaged separately.Since peak velocity was attained more quickly with fastervelocities, acceleration was a better single descriptor of the

mechanical event than the specified velocity itself. Hencethe results are reported in terms of acceleration. Twoconditions were studied. In the first there was nobackground torque exerted by the patient on the platform.The subject sat in a chair and was asked to relax as much aspossible. In the second the subject voluntarily exerted aplantar flexing background torque onto the platform of 20%of his maximum force while waiting for the perturbation.The voluntary response to muscle stretch was studied

with the patient's foot relaxed on the platform. He wasgiven one of two tasks to perform when he perceived theperturbation (1) push (plantarflexion of the ankle) or (2)assist (dorsiflexion of the ankle). All the perturbations werefrom - 100 to 50 and the specified velocity was 150°/s.Vibration was applied at 100-150 Hz with a physical therapyvibrator (Foredom Electric Company Series 37) to theAchilles tendon prior to the dorsiflexion of the foot, withand without background force exerted by the subject. Inother experiments the ankle was displaced in twoconsecutive phases: (1) from -100 to 50 at 15°/s and thenfrom +5° to - 100 at 2000/s and (2) from - 100to +5° at 1500/sand then from +50 to -10° at 1500/s.

Results

STRETCH REFLEXES OF TRICEPS SURAE AT"REST"A short-latency reflex was present in all the patientsstudied (fig 1A), and this response increased inamplitude with increased acceleration of stretch. The

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(a) (b)~~~~~20`4. t\400@

5843'/Sec2 ] 5836/sec2

250 ms

Fig 1 EMG response oflateral gastrocnemius muscleforpatient 12 to rapid dorsiflexion stretch while thepatient was atrest (A) and while exerting 20% backgroundforce (B). Thetop trace is rectified EMG activity, the next trace is ankleangle and the next trace is acceleration ofankle. The tracesare the average of 10 single trials.

"magnitude" of the short-latency reflex wascalculated for each patient as the value of the EMGat 3600'/s2 acceleration obtained from linearinterpolation from the actual data points. Using thismethod the short-latency reflex was enhanced for 9out of 16 patients in comparison to normal subjectspreviously reported6 (fig 2). In 12 out of 16 patientsthe short-latency reflex was followed byEMG activitysimilar to the long-latency reflexes observed when anormal subject is voluntarily exerting a backgroundforce (figs 1A, 3). The amplitude of the long-latencyreflexes sometimes increased and sometimesdecreased with acceleration. It was not possible tostandardise a "magnitude" for the long-latencyreflexes since their behaviour was not monotonic. Forthis reason the long-latency reflexes were simplydescribed as absent, normal magnitude or largemagnitude, and the magnitude was considered largeif the long-latency reflexes exceeded normal for anyacceleration. In our patients with Parkinson's diseasethe triceps surae were not completely at restpreceding the stretch, but showed a continuous

background contraction. By integrating the EMGactivity in the first 100 ms of the record (prior to anyreflex response) the patients showed activity varyingbetween 4-5% to 25% of the maximal force (seetable). In order to assess the role of background forceon the results we carried out further experiments onnormal subjects. Background EMG activity at restwas usually less than 4% of maximal force, but couldbe as high as 7%. The short-latency reflex was presenteven if the muscle was totally relaxed and did notchange much with background force, but increasedslightly with background force up to 50% ofmaximum. The long-latency reflexes (one or morediscrete components) were absent at rest, appearedwith a background force between 5-10% ofmaximum, became larger in proportion tobackground force up to about 30% after which theydid not increase. Considering the normal results, allbut three patients demonstrated increasedbackground EMG activity at rest. In relation to theshort-latency reflex, the three patients with normalbackground had normal amplitude. Five patients hadmarkedly increased amplitude, more than would beexpected even if they were exerting 20% voluntaryforce, and in none of these cases was the backgroundcontraction more than 20%. In four patients theshort-latency reflex was increased, but within therange of a normal subject exerting torque. In relationto the long-latency reflexes, the three patients withnormal background activity all showed long-latencyreflexes at rest and their magnitude was usually withinthe range of amplitude of those of normal subjectsexerting 20% background force. In general the rangeof background EMG activity was less in thosepatients who did not show long-latency reflexes at rest(6-12%) and the magnitude in different patients wasonly loosely correlated with the amount ofbackground force.The latency of short-latency reflexes varied from

50-80 ms and shortened with faster stretching, andthe duration varied from 20 to 40 ms and both of these

Rest

II

6k4

2

0 10 20 30 40 50 60 70 80 90

Background forceo Normalm Abnormal

HIHIII I, II0 10 20 30 40 50 60 70 80 90

Magnitude of EMG

Fig 2 Number ofpatients showing different magnitudes of the short-latency stretch reflex while at restand while exerting20% background force. The light bars indicate normal behaviour and the dark bars indicate abnormal behaviour.

M? 8

0 6

'0- 4

- 2

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IJRest10 - Background torce

866

Ez 2

0Absent Normal Large

Fig 3 Number ofpatients showing different magnitudes oflong-latency stretch reflexes while at rest (light bars) andwhile exerting 20% background force (dark bars).

parameters are within the normal range. The long-latency reflexes when present appeared at latency of84-122 ms with durations of 30-75 ms.

STRETCH REFLEXES OF TRICEPS SURAE WITHBACKGROUND FORCEWhen the patient voluntarily exerted a backgroundforce of 20% of his maximum force, the short-latencyreflex was present at slightly shorter latency and withthe same duration of the same response evokedwithout background force (fig 1B). This responseincreased in magnitude with increased acceleration ofstretch but was not often increased in magnitude withrespect to the circumstance when the subject wasrequested to relax (fig 2). Three of 15 patients showedincreased magnitude of the short-latency reflex.Long-latency reflexes appeared at latencies of 80-110 ms and were present in all but one of the patients.The long-latency reflexes increased in magnitude incomparison to the long-latency reflexes observedwithout background force and were enhanced inmagnitude with respect to normal values in eight outof 15 patients (fig 3). In three of the patients withenhanced long-latency reflexes an enhancement ofshort-latency reflex was also present, while fourshowed no enhancement of the short-latency reflex(one was not studied). It can be noted also that two ofthe patients with an enhanced short-latency reflex didnot show enhanced long-latency reflexes. In normalsubjects it was usually possible to divide the long-latency reflexes into two discrete components, butthis was often difficult for the patients. Additionallythe long-latency activity in the patients oftencontinued without pause beyond a latency of 150-160ms into the time interval which we considered innormal subjects to be characterised by voluntaryactivity. With faster velocity of stretch, the long-latency reflexes disappeared in one patient whoshowed a very large short-latency reflex.

VOLUNTARY RESPONSEThe voluntary plantar flexion movement in responseto muscle stretch was studied in nine patients. A largeEMG response from triceps surae was present at alatency varying from 170-250 ms. The beginning ofthe voluntary response often came immediately aftera long-latency response without an intermediatepause separating these two bursts. In four patientsvoluntary dorsiflexion of the foot was performedfollowing the perturbation and an EMG responsefrom tibialis anterior appeared at a latency of 250-300ms.

EFFECT OF VIBRATIONThe effect of vibration applied to the Achilles tendonwas studied in seven patients (fig 4). When thepatients were trying to be relaxed the short-latencyreflex was abolished in all and the long-latencyreflexes when present, persisted although diminishedin amplitude. When a background force was exertedby the subject the short-latency reflex was markedlysuppressed or absent in all, but the long-latencyreflexes persisted in all but two patients. The long-latency reflexes in this circumstance were decreasedby vibration approximately 10% to 50% in thedifferent subjects.

RESPONSE OF TIBIALIS ANTERIORIn 11 of the 17 patients a large phasic EMG responsewas recorded from the tibialis anterior afterstretching the triceps surae (shortening reaction).

DOUBLE RAMP DISPLACEMENTIn the first series of experiments the first displacementwas a slow dorsiflexion (15°/s) in the attempt toinduce tonic EMG activity in triceps surae, and thesecond displacement was a fast plantar flexion (150-

At rest

No vibration

Vibration

With background force

250s 10.

250ms

Fig 4 Effect of vibration applied to the Achilles tendon onthe stretch reflex. In each ofthefour parts of the figure areshown rectified EMG (with identical scaling) from lateralgastrocnemius and ankle position. The displacement is 14°.Each trace is the average of 10 individual trials.

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100°/s) of the ankle. Fifteen patients were studied. Ineight patients the slow dorsiflexion elicited graduallyincreasing involuntary muscular activity (fig 5). In allthese patients a fast plantar flexion of the footabruptly abolished or markedly decreased the tonicEMG activity at a latency ranging in the differentpatients from 100 to 150 ms. In the remaining sevenpatients no EMG activity was induced by the slowdorsiflexion of the foot.

In the second series of these experiments the anklewas displaced quickly from -10° to 5° at 1500/s andthen quickly back to -10° at 150°/s (triangle stretch).Eight patients were studied. This type of stretchdiffered from the standard stretch mainly by virtue ofhaving no plateau phase; the dynamic dorsiflexionphase was similar. In all patients the short-latencyreflex was similar to that seen with the standardmaintained stretch, but the long-latency reflexes werediminished.

CLINICAL EVALUATIONThe table lists the clinical assessment of rigidity of thepatients together with the quantitative results ofankle stretching. The rigidity was classified in fourdegrees: absent, mild, moderate and severe, but forthe purposes of analysis the patients were divided intotwo groups (1) absent and mild, and (2) moderate andsevere. Chisquare tests were carried out to look forcorrelations between the degree of tone andbackground contraction (normal or elevated), short-latency reflex (normal or large), long-latency reflexes(present or absent), magnitude of long-latencyreflexes with background force (normal or large) andpresence or absence of shortening reaction.Correlations with the degree of tone were found onlyfor long-latency reflexes at rest (p < 0- 025) and

150

,-101,

500 ms

Fig 5 EMG response oflateral gastrocnemius muscle toabrupt plantarflexion for +50 to -10°following a slowdorsiflexion ramp stretch which began prior to the beginningofthe illustration at -10°. The top trace is rectified EMG inarbitrary units and the bottom trace is ankle position. Eachtrace is the average of10 trials.

magnitude of long-latency reflexes with backgroundforce (p < 0-01). The average duration of the long-latency reflexes with background force was 35 ms forthe group with absent-mild tone and was 67 ins for thegroup with moderate-severe tone and this was also asignificant difference (p < 0 01). This differencemight be even more extreme than it appears sincelong-latency reflexes often merged with subsequentlater activity so that the true duration might well belonger than what we have measured.

Discussion

SHORT- AND LONG-LATENCY STRETCH REFLEXESAndrews et al,' Dietrichson8 and McLellan9 havepreviously shown that phasic stretch reflexes arenormal or slightly increased in Parkinsonian patientswhich in general is in accord with the common clinicalfindings. An increase of the stretch reflexes can morefrequently be demonstrated during slow andmaintained stretching.78 This phenomenon can becalled an enhanced tonic stretch reflex and is theelectrophysiological correlate of the clinical sign ofrigidity. The observation of Lee and Tatton' thatsubjects with Parkinson's disease have an increase oflong-latency stretch reflexes is provocative because itsuggests a neuronal pathway apparently differentfrom the monosynaptic pathways that could sustainthe rigidity without enhancing the phasic stretchreflex. Subsequently, a direct correlation between theamount of rigidity measured in patients withParkinson's disease by quantitative slow stretches andthe magnitude of the long-latency responses of bicepsand triceps has been shown by Mortimer andWebster.23 Marsden et al suggested that the increaseof the long-latency reflexes of the flexor pollicislongus was due to the fact that rigid patients are nottruly relaxed at rest. On the other hand, Tatton et al'°reported that the increase of long-latency stretcheswas out of proportion to baseline activity.

Thirteen of 16 patients reported here showed anincrease of baseline EMG activity when they were atrest. This baseline activity is important to note, butwas not responsible alone for the clinical impressionof increased tone. Nine of the 16 showed an increasedshort-latency reflex at rest and five patients showedan increased short-latency reflex compared to normaleven when considering background activity. Three ofthese nine patients showed an increase of short-latency reflexes when exerting voluntary backgroundforce. However, these changes in short-latencyreflexes did not correlate with the clinical impressionof tone.The presence of an involuntary background

contraction before the stretch could only to someextent explain the presence of long-latency reflexes

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when the patients were requested to relax, since fourpatients had long-latency reflexes greater than thatseen even with background force. In addition, thepresence and the magnitude of the long-latencyreflexes were not always directly related to theamount of baseline activity. When the patients wereexerting background force, the magnitudes of thelong-latency reflexes in eight were greater than thatwhich could be explained by the level of backgroundforce. These increases in magnitude and also induration were correlated with increased tone inagreement with the previous observations ofMortimer and Webster.23The short-latency reflex certainly represents the

monosynaptic stretch reflex but the pathway for thelong-latency reflexes is not clear. A trans-corticalloop has been suggested'I s1-6 but spinal mechanismsalone can be responsible. '7 We have previouslysuggested6 that the long-latency reflexes of tricepssurae arise from serial responses to multiple spindledischarges, but other mechanisms are also possible.The behaviour of long-latency reflexes in patientswith rigidity reported here could be explained by atleast two hypotheses. The first is an enhancement ofproposed normal stretch reflex mechanisms resultingin an increased response to second and third spindlebursts. In favour of this hypothesis is that the short-and the long-latency reflexes sometimes wereincreased in the same patient. However, often thelong-latency reflexes were selectively enhanced inpatients with severe rigidity. The experiments usingvibration demonstrated that the mechanism of themonosynaptic short-latency reflex differed from themechanism of at least some part of the long-latencyreflexes; this fact suggests that these reflexes inParkinsonian patients are not completely generatedby a monosynaptic reflex mediated by IA fibres.The second hypothesis for the abnonnal long-

latency reflexes in Parkinson's disease is that a newphenomenon in patients with rigidity has beensuperimposed upon the normal responses. Thishypothesis can itself be divided into two possibilities.The first one is an enhanced polysynaptic response tothe same inputs active in normal subjects."' 8 Wecannot exclude this hypothesis definitely; however,the triangle stretch experiments which show areduction in the long-latency reflexes when thestretch is not maintained, suggest that the long-latency responses depend on continuing afferentinput. In addition, the vibration experiment can beconsidered negative evidence if one accepts thenotion that vibration has its effect by keeping the IAafferents so active that they cannot respond to phasicstretch. '9 The second possibility is that there is a newresponse to inputs not active in normal subjects. Inthis regard we are attracted to the possibility of group


II afferent input. Matthews20-23 showed that group IIfibres add to the excitatory influence in the stretchreflex, participating in the tonic stretch reflex of thedecerebrate cat. With the spike-averaging techniqueit has been shown that group II impulses exertmonosynaptic excitatory effects on alphamotoneurons in extensor muscles.24-27 All theseworks suggest that group II afferents have a rolebeyond the flexor reflex afferent system and canprobably participate in the stretch reflex. In additiontheir slow conduction velocity fits well with thelatency of the long-latency reflexes. Group IIafferents would not be expected to be stimulatedsignificantly by triangle stretches and indeed with thistype of stretch these reflexes are reduced. It was tosupport this hypothesis that we investigated the effectof vibration applied at high frequency to the Achillestendon. It has been shown that group II fibres are notsensitive to vibration in the cat;28 vibration in man hasclearly some effects, but these effects are probablyless at high frequency.29-32 In normal subjects6vibration of the Achilles tendon before the stretchsuppressed the short- and the long-latency reflexes.In patients with rigidity the short-latency reflex wasabolished but the long-latency reflexes persisted evenif decreased in magnitude. These arguments are notdefinitive by themselves, but other evidence in favourof group II mechanism being active in rigidity will bediscussed in relation to the tonic stretch reflex.

TONIC STRETCH REFLEXIncreased tone clinically is equivalent to a tonicstretch reflex physiologically. There has been no clearunderstanding about the physiology of the tonicstretch reflex in normal man since this reflex is absentin the normal relaxed state. Lance et al33 havesuggested that the tonic stretch reflex can be recordedduring isometric contraction or with reinforcementmanoeuvres, but this has not led to any clearerunderstanding of mechanism. Another view aboutthe tonic stretch reflex in man developed with thediscovery that the primary spindle endings incats28"343S and in man3' are sensitive to vibration andthat continuous vibration behaves like prolongedstretching and induces a tonic contraction of themuscle called a tonic vibration reflex. The tonicvibration reflex has been observed in decerebratecats20 and in spinalised animals after administrationof levodopa.37 In man the tonic vibration reflex hasbeen considered a polysynaptic spinal reflex,'8 " andnot a cortically mediated reflex.303' AlthoughMcLellan9 showed that the tonic vibration reflex isfacilitated in patients with rigidity, Lance et al32 andHagbarth29 reported that the tonic vibration reflex ofParkinsonian patients does not differ from that ofnormal subjects.


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We have been discussing the long-latency reflexesas a type of phasic stretch response which is later intime than the classic monosynaptic response, but thelong-latency reflexes could be viewed as thebeginning of a tonic stretch reflex. Our stretch isordinarily maintained for at least 3 s so that there isopportunity for tonic stretch reflexes to be manifest.Indeed for some patients these reflexes do have theappearance of continuous activity not divisible intocomponents and this activity might well continue intothe time period which we have not analysed becauseit corresponds with what might be voluntary activity.It is possible that patients manifesting enhancedlong-latency reflexes have a tonic stretch reflexsuperimposed upon the normal phasic long-latencyreflex mechanism. The results with triangle stretchessupports the idea of a tonic quality of the long-latencyreflexes.We investigated the stretch response in this group

of patients with slow stretching of triceps surae. Thistechnique which mimics the clinical method ofappraisal of tone is not equivalent to the tonic phaseof a step-like stretch, but like tonic stretch can beproductive of continuous EMG activity which is notseen in normal subjects. In half of the patients studiedthe slow stretching induced involuntary EMGactivity. In general these patients were the ones withgreater increased tone and larger long-latencyreflexes. A fast plantar flexion of the foot wassubsequently delivered in the attempt to measure thetime of disappearance of the continuous EMGresponse which would tell us the latency of thepathway supporting the activity. In all the patients thetime was in the latency range of the long-latencyreflexes. This suggests that activity is not supportedby the monosynaptic pathway but instead bypathways compatible with long-latency phenomena.As noted above, it is possible that in Parkinson'sdisease there is a new mechanism superimposed onthe normal which might be mediated by group IIafferents. The data from animals would certainlysuggest that enhanced response to group II afferentscould be responsible for tonic stretch reflexes andreflexes to slow continuous stretch. In favour of thishypothesis is the work of Dietrichson8 showing thatthe increased tonic reflex response in Parkinsonianpatients depend on the integrity of small-sized nervefibres, either static fusimotor or group II afferents.

Conclusion

The notion that rigidity is simply a result of enhancedsupraspinal drive on alpha motor neurons, 40 or aresult of alpha and gamma motor neurons being co-activated,73240 is not supported by our finding of apoor correlation between the level of background

EMG activity at rest and the clinical impression oftone. The notion that rigidity stems from enhancedfusimotor activity,45"8 seems to have been disprovedby the findings of Wallin et al49 and Burke et al50 withmicroneurography. These findings suggest thatrigidity arises from a change of central nervous systemreflex responsiveness.Two examples of increased reflex mechanisms in

Parkinson's disease are the shortening reaction andthe monosynaptic reflex. The shortening reaction actsin an opposite direction to what is necessary toproduce the clinical impression of increased tone, andindeed there is no relationship between thisphenomenon and degree of rigidity as has beenshown also by Mortimer and Webster.23 The short-latency reflex does act in the correct direction to whatis necessary to produce increased tone but it is onlyenhanced in a few patients and it does not correlatewith clinical impression.

Long-latency reflexes are remarkably prominent inParkinsonian patients, appearing commonly at rest,are often increased in amplitude and are frequentlylong in duration merging with subsequent activitywhich may be voluntary. Their magnitude and dura-tion correlate well with clinical impression of rigidity.The long-latency reflexes have the appearance andbehaviour of a tonic response and the continuousEMG produced by slow ramp stretches is supportedby pathways with latencies similar to the long-latencyreflexes. Hence these reflexes seem to play a role intonic stretch behaviour of the Parkinsonian patient.The mechanism of the abnormal long-latency reflexesneeds further investigation, but the observationsabout them at the present time are compatible with agroup II mediated tonic stretch response.

The work was supported by a grant to theRehabilitation Engineering Center by the NIHR (23-P-5584/1) and a grant from the Whittaker HealthSciences Fund of MIT. R Ackerman providedtechnical support. Alfredo Berardelli was supportedby a fellowship from Consiglio-Nazionale DelleRicherche (CNR), Nato, Italy and from the Brighamand Women's Hospital Amyotrophic LateralSclerosis Research Fund.

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Physiological mechanisms of rigidity Parkinson's disease · dorsiflexion stretch were studied in 17 patients with Parkinson's disease. Mostpatients showed Mostpatients showed increased