76ournal ofNeurology, Neurosurgery, and Psychiatry 1993;56:776-781

Soleus H-reflex tests and clinical signs of theupper motor neuron syndrome

J H TM Koelman, L J Bour, A A J Hilgevoord, G J van Bruggen,B W Ongerboer de Visser

Soleus H-reflex tests are used for eluci-dating pathophysiological mechanisms inmotor control. The cumulative vibratoryinhibition of the soleus H-reflex, theratio of the reflex to direct musclepotential (H to M ratio) and the recoverycurve of the soleus H-reflex were studiedin 38 patients with varying signs of theupper motor neuron syndrome for apossible relation with clinical features.The results were compared with thoseobtained from a group of healthyvolunteers. The magnitude of vibratoryinhibition decreased with increase ofhypertonia. The H to M ratio increasedas the activity of the tendon reflex wasenhanced and correlated to a lesserdegree with muscle tone. Both the H toM ratio and late facilitation of the soleusH-reflex recovery curve were elevated inclonus. The findings suggest that altera-tions in the results of soleus H-reflextests relate to specific clinical features ofthe upper motor neuron syndrome.Possible pathophysiological implicationsare discussed.

(7 Neurol Neurosurg Psychiatry 1993;56:776-781)

Departmentsof ClinicalNeurophysiology andNeurology, AcademicMedical Centre,Meibergdreef 9, 1105AZ-AmsterdamJ H T M KoelmanL J BourA A J HilgevoordG J van BruggenB W Ongerboer deVisserCorrespondence to:Professor Ongerboer deVisser, Department ofClinical Neurophysiology(D2), Academic MedicalCentre, Meibergdreef 9,1105 AZ-Amsterdam,The Netherlands.Received 25 June 1992and in revised form24 September 1992.Accepted 15 October 1992

The H-reflex is evoked by stimulation of 1 afibres from muscle spindles and appears atlower stimulus intensities and at longerlatency than a direct muscle potential evokedby stimulation of motor nerve fibres. I

Different soleus H-reflex tests may be usedfor the study of central mechanisms in motorcontrol of the leg.2 In the upper motor neuronsyndrome various alterations of these tests arefound. Compared with healthy controlssuppression of the H-reflex during vibrationis decreased in most patients whereas theratio between the maximal soleus H-reflexresponse and muscle potential (H to M ratio)is increased.Y Furthermore, changes in theH-reflex recovery curve obtained by pairedstimuli to the posterior tibial nerve arefound.67 In the upper motor neuronsyndrome the various clinical characteristics,such as weakness, loss of dexterity, hyper-reflexia, clonus, hypertonia, and the extensorplantar response, may occur independentlyand in different combinations to a largeextent.8 As such, a relation between specificclinical features and alterations in the resultsof H-reflex tests may further contribute inelucidating underlying pathophysiologicalmechanisms. The relation between the

various clinical signs and these neuro-physiological alterations, however, is largelyunknown or in some cases conflicting.24 Weinvestigated whether in a heterogeneousgroup of patients with an upper motorneuron syndrome changes in vibratoryinhibition of the soleus H-reflex, H to Mratio, and the recovery curve of the reflexwere related to specific clinical features.

Subjects and methodsThirty eight selected patients aged 18-75years (mean 47 years) participated in thestudy. Evident clinical features of an uppermotor neuron lesion were present in thelower limb, with or without upper motor neu-ron signs in the upper limb. None of thepatients had a lower motor neuron compo-nent to their disease. Nine patients had acerebral lesion: ischaemic infarction in six;arteriovenous malformation in one; infantileencephalopathy in one; and penetrating headinjury in one. Fifteen patients had a myelopa-thy: slowly progressive multiple sclerosis infive; transverse myelitis in two; cervicalspondylosis in three; traumatic myelopathy inthree; and two intradural spinal meningeomain two. Fourteen patients had a clinical pic-ture of a slowly progressive spastic parapare-sis, seven with a positive family history.Duration of the disease varied from twomonths to 45 years (mean 7-5 years). Thecontrol group consisted of 48 healthy subjectsaged 20-70 years (mean 38 years).

At the time of investigation none of thepatients had received medical treatmentknown to influence spasticity. All subjectsgave informed consent. The clinical examina-tion was performed just before the neuro-physiological testing. Clinical examinationand neurophysiological testing were perform-ed independently by different investigators.

Clinical examination consisted of theassessment of four elementary features of theupper motor neuron syndrome-that is,hypertonia, muscle strength, tendon reflexactivity, and the plantar response. Presenceand severity of signs were categorised in astandardised fashion. An increase in calf mus-cle tone was investigated by passive dorsiflex-ion of the ankle joint and was gradedaccording to the Ashworth scale9: 0-normaltone; 1-slightly increased tone giving a catchon abrupt passive stretch of the triceps suraemuscle; 2-increased tone; 3-severelyincreased tone; and 4-passive movement ofthe ankle joint hardly possible. Strength of

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triceps surae was judged according to theMedical Research Council scale10 and gradedin four categories: 0-normal (MRC 5); 1-slight weakness (MRC 4); 2-moderate weak-ness (MRC 2 or 3); and 3-severe weakness(MRC 0 or 1). Achilles tendon reflexes weregraded as 0-diminished or absent; 1-normal;2-increased; 3-ankle clonus (that is, fourreflex contractions or more produced by ten-don percussion or abrupt ankle dorsiflexion).Plantar reflexes were graded as 0-flexor; 1-equivocal; and 2-extensor.

EXPERIMENTAL PROCEDURERecording and stimulation techniques for thesoleus H-reflex have been described previous-ly.511 During all tests subjects were seated in areclining chair in a standardised position.5H-reflexes were elicited only when no soleusactivity was detected by electromyography.Reflex responses elicited by 1 ms squarecurrent pulses to the posterior tibial nerve inthe popliteal fossa were amplified with a bandpass filter of-3 dB at 2 Hz and 10 kHz anddigitally stored in a PDP 11/73 minicomputerwith a sample frequency of 10 kHz. The timeinterval between successive recordings was atleast 30 seconds.512 For the construction ofan H-reflex recruitment curve as a function ofstimulus intensity (figure la) the increment in

Figure 1 Example ofresults ofsoleus H-reflextest-in patient No 38(table 1). (a) Recruitmentcurves ofsoleus H-reflexresponse (H) and muscle(M) potential (peak-peakvalues) without vibrationofAchilles tendon and withvibration, producing onlyslight H-reflex suppression.All values expressed aspercentages ofmaximumM potential. (b)Cumulative vibratoryeffect on H-reflex (peak-peak values) as function ofstimulus intensity. Amountofsuppression is equal to100% minus cumulativevibratory index.

100

75

50

25

H-reflex recruitment curve

Stimulus intensity (mA)

100

75

50

25

0

Cumulative vibratory effect

B

intensity of successive stimuli was small atlow intensities but gradually enlarged at high-er intensities. Each recruitment curve consist-ed of 12 or more H-reflexes at differentintensities. Simultaneously with the H-reflexrecruitment curve, a recruitment curve ofdirect soleus muscle potentials was construct-ed also as a function of stimulus intensity(figure la). Peak-peak values of the maxi-mum H-reflex response and maximummuscle potential were used to calculate the Hto M ratio.

Vibration of the Achilles tendon with afrequency of 100 Hz and an undampedamplitude of 1 mm was applied by a Bruelland Kjaer 4809 vibrator. The cumulativevibratory index was used as a quantitativemeasure for the vibratory effects on theH-reflex (figure lb).5 This index was definedas the surface under the H-reflex recruitmentcurve obtained during vibration up to acertain stimulus intensity divided by thesurface under the H-reflex recruitment curveobtained without vibration up to the samestimulus intensity times 100%. The index atthe stimulus intensity that yielded themaximum H-reflex response was used in thecalculations.7

H-reflex recovery curves were constructedby application of paired pulses of equalintensity. The stimulus intensity at which theH-reflex reached half its maximum value wasused (figure 2).7 Time intervals betweenconditioning and test stimuli were 100, 200,250, 300, 400, and 500 ms and at 1, 3, 10,and 30 seconds. Early facilitation and inhibi-tion were not examined. The recovery curveswere plotted as the ratio in percentagebetween the area values of the test and theconditioning H-reflex response against thetime interval between the two stimuli. Twocharacteristic values were used for statisticalanalysis: firstly, the local maximum of the testH-reflex occurring in the late facilitatory

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Figure 2 Recovery curve ofsoleus H-reflex response(area values) at 0-5Hmaximal stimulus intensity in

I I I patient No 38 (table 1). All values of reflex response to test20 40 60 80 stimulus (S2) presented as percentages ofpreceding H-

reflex to conditioning (Sl) stimulus. In faciitatory periodStimulus intensity (mA) test reflex reached 100% ofconditioning H-reflex.

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Koelman, Bour, Hilgevoord, van Bruggen, Ongerboer de Visser

phase at a stimulus time interval ranging from50 to 320 ms and, secondly, the localminimum of the test H-reflex found in thelate inhibitory phase of the recovery curve ata stimulus time interval ranging from 320 to1000 ms.

Variables of the soleus H-reflex tests usedhave previously been shown to discriminatemost productively between patients withupper motor neuron lesions and controlsubjects.7

STATISTICAL ANALYSISAnalysis of variance (BMDP statistical soft-ware package 7D) was performed with use ofa priori contrasts tests for studying correlationbetween clinical signs and neurophysiologicaldata in patients. Differences in neurophysio-logical variables in the different groups ofpatients were examined with pairwise t tests,significance levels were adjusted for the num-ber of paired comparison tests (Bonferroni).Within the groups of patients linear (step-wise) regression analysis (BMDP 1R,2R) wasperformed to examine correlation betweenneurophysiological variables and betweenneurophysiological variables and age.

ResultsCLINICAL SIGNSTable 1 shows the results of the clinicalassessment in the patients. Sixteen patientsshowed a mild clinical picture of an upper

motor neuron lesion with normal strength (0,MRC 5) or slight weakness (1, MRC 4)combined with normal or slightly elevatedmuscle tone (Ashworth 0 or 1). Of thesepatients plantar responses were extensor in13, equivocal in two, and flexor in one;clonus was present in three and absent in 13.Seven patients showed a severe clinicalpicture with moderate (2, MRC 2 or 3) or

severe paresis (3, MRC 0 or 1) combinedwith severely increased tone (Ashworth 3 or

4). Plantar responses were extensor in six andequivocal in one, and clonus was present infour and absent in three patients. The 15other patients had a clinical picture in-between the former two groups, with plantarresponses extensor in 13 and flexor in two. Inthe patients as a whole the following clinicalcharacteristics were found: tone was normal(Ashworth 0) in six, slightly elevated(Ashworth 1) in 13, moderately elevated(Ashworth 2) in 1 1, strongly elevated(Ashworth 3) in six, and passive movementwas hardly possible (Ashworth 4) in twopatients. For statistical analysis patients withAshworth 3 and 4 were combined because ofthe small number with Ashworth 4. Strengthwas normal (0, MRC 5) in 14 patients, weak-ness was slight (1, MRC 4) in nine, moderate(2, MRC 2 or 3) in 11, and severe (3, MRC0 or 1) in four patients. Tendon reflexes werenormal in 12, increased in 13, and there was

clonus in 13 patients. Plantar responses wereextensor in 32, equivocal in only three, and

Table I Clinical signs and results ofsoleus H-reflex tests in patients with the upper motor neuron syndrome

CumulativeMuscle H toM vibratory Late Late

Age Musclet Tendon* tone Plantar§ ratio index facilitation inhibitionPatient (years) Lesion* strength reflex (Ashworth) response (%) (%) (%) (%)

1 25 1 0 2 1 2 85 34 55 192 41 1 2 2 4 2 63 100 85 573 47 1 2 2 3 2 76 43 87 74 59 1 1 3 1 2 100 83 91 535 27 1 3 3 2 2 72 47 94 436 59 1 1 1 1 2 27 82 40 327 37 1 2 3 3 2 89 57 104 778 39 1 1 2 2 2 49 66 55 279 34 1 3 2 3 2 68 112 120 2810 55 1 2 2 1 2 48 45 78 5811 75 1 2 1 1 2 8 59 95 2612 69 1 2 1 1 2 51 58 60 3613 33 1 1 2 0 2 37 40 41 1814 50 1 0 1 1 2 24 42 95 7315 64 1 0 1 0 2 41 11 66 3716 50 2 2 3 2 2 87 69 100 6217 57 2 3 1 2 2 7 51 83 4018 65 2 0 1 2 0 63 101 74 4719 67 2 2 1 2 2 97 99 39 2520 59 2 3 3 3 2 64 36 71 4921 18 2 2 2 2 0 93 48 65 1022 25 2 1 3 1 2 74 25 117 2223 61 2 1 1 0 1 58 62 41 2224 22 2 0 2 0 0 75 40 109 125 31 3 2 3 4 2 94 69 63 5126 50 3 0 2 1 2 100 61 89 6527 44 3 0 3 2 2 88 104 111 3328 49 3 0 2 2 2 102 105 137 129 51 3 2 3 3 1 102 74 90 5430 52 3 0 3 3 2 83 72 48 2531 74 3 1 1 0 2 29 41 82 3932 52 3 1 3 1 2 106 90 57 4833 44 3 0 1 0 2 88 42 5 334 45 3 0 2 1 2 47 22 63 3435 50 3 1 2 1 1 18 28 142 4136 43 3 0 1 1 2 76 10 60 4737 31 3 0 3 2 2 93 48 94 3338 59 3 0 3 2 2 99 74 103 8

* 1 = Myelum; 2 = cerebral; 3 = spastic paraplegia.t0 = MRC5; 1 = MRC4;2 = MRC2or3;3 = MRC0or1.t 1 = Normal; 2 = increased; 3 = clonus.§ 0 = Flexor; 1 = equivocal; 2 = extensor.

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flexor in only three patients. The plantarresponse was therefore not included in thecorrelation analysis. The only appreciabledifference in clinical characteristics betweenpatients with a cerebral lesion, myelopathy,and spastic paraparesis was that paresis wasmore severe in patients with a myelopathythan in patients with a slowly progressivespastic paraparesis.

CLINICAL SIGNS AND NEUROPHYSIOLOGICALFEATURESTable 1 also shows the results of the H-reflextests. Figure 3 shows vibratory effects incontrols and patients grouped according tomuscle tone. In the patients a moderate butsignificant correlation was found betweendegree of hypertonia and vibratory effects onthe H-reflex expressed by the cumulativevibratory index (r = 0-46, p < 0 01). A differ-ence in the index existed between the patientswith normal (Ashworth 0, mean 39%, range1 1%-61%) and the ones with moderatelyelevated tone (Ashworth 2, mean 74%, range47%-104%, p < 0-05 for comparing six pairsof means). Patients with severe hypertoniashowed no further increase in the index(mean 70%, range 36%- 11%). The cumula-tive vibratory index did not correlate with lossof muscle strength (r = 0d14, p = 0A40) orenhancement of tendon reflexes (r = 0-15,p = 0-38).

Figure 4 shows H to M ratios in controlsand patients grouped according to tendonreflex activity. In the patients a moderatelycorrelated increase of the H to M ratio withenhancement of tendon reflex activity wasfound (r = 0 55, p < 0-001). In all 13 patientswith ankle clonus the H to M ratio was 64%or greater with a mean value of 88% (range64%-106%), which was significantly morethan the mean in patients with normalAchilles tendon reflexes (mean 47%, range7%-96%, p < 0.01 for comparing three pairsof means). A weakly correlated increase of the

Figure 3 Correlationbetween musde tone andcumulative vibratoryindex. *Indicates differencein index between controlsand patients with normaltone (P < 0 05);*"indicates difference inindex between patientswith normal and patientswith moderately elevatedtone (p < 005 forcomparing six pairs ofmeans); mean (SD).

Controls

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H to M ratio with increase of muscle tonewas found (r = 0 34, p < 0 05). There was norelation between the H to M ratio and loss ofmuscle strength (r = - 0d16, p = 0 34). Inpatients the H to M ratio also correlated withage (r = - 0-35, p < 0 05). When forwardstepwise regression analysis was performedwith age and tendon reflex activity for the Hto M ratio, however, partial correlation of agewas - 0-07 (p = 0 66). Thus the correlationbetween the H to M ratio and age was almostfully determined by decreased tendon reflexactivity found at advanced ages. In thepatients a small correlation existed betweenthe H to M ratio and the cumulative vibratoryindex (r = 0-35, p <005).

Figure 5 shows findings of the late facilita-tion of the recovery curve in controls andpatients grouped according to tendon reflexactivity. Late facilitation increased withenhancement of tendon reflex activity (r =0 40, p < 0-05). In patients with clonus thelate facilitation was increased (mean 88%,range 48%-117%) compared with patientswho had normal tendon reflexes (mean 62%,range 5%-95%, p < 0 05, for comparingthree pairs of means). The late facilitation didnot correlate significantly with muscle tone(r = 0-23, p = 0-16) or loss of musclestrength (r = 0-09, p = 0 60). In the patientsthere was no correlation between the H to Mratio and the late facilitation of the recoverycurve (r = 0-01, p = 0-93). The late inhibi-tion did not correlate significantly with tone(r = 0-25, p = 0.13), muscle strength (r =0-25, p = 0-13), or activity of tendon reflexes(r = 0-08, p = 0 64).

Patients with normal tone or normaltendon reflexes were compared with controlsubjects. There was no difference in the H toM ratio in the patients with normal tendonreflexes and the control subjects (mean 48%,range 6%-99%) (figure 4). In control sub-jects vibratory effects on the H-reflex (mean19%, range 0%-60%) were more pronounced

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100 -

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Figure 4 Correlation between tendon reflex activity andH toM rcdifference between H to M ratio in patients with normal tendon refleclonus (p < 0-01 for comparing three pairs ofmeans); mean (SD).

(p < 0 05) than vibratorywith normal tone (figure 3,in patients with normal(figure 5) was higher than i(mean 42%, range 8%-920/was also the case for lapatients with normal reflex36% (range 3%-73%) an(mean was 17% (range 2%-4No significant difference

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Controls

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Figure S Correlation between tendon reflexes and late facilitation.between late facilitation in controls and patients with normal tendon**indicates difference between patients with normal tendon reflexes aclonus (p < 0-05for comparing three pairs of means); mean (SD).

eX DiscussionClQnus In healthy subjects vibration of the Achilles

tendon, which strongly activates primaryspindle endings, suppresses or abolishes theH-reflex for the duration of the vibration.3 13-16This action is supposed to be predominantlydue to an autogenic axoaxonal presynaptic

*...*inhibition of Ia terminals, although other0.1 mechanisms have been suggested as

well.3"'4 17-19 In patients with acute spinal orcerebral lesions, flaccid paralysis, and

* areflexia vibratory inhibition is enhanced,202'whereas in most patients with longer standinglesions and spasticity inhibition of the soleusH-reflex during vibration of the Achilles ten-don is decreased.45720-2 Studies relatingdiminished vibratory inhibition to specificclinical signs of the upper motor neuron syn-drome are scarce. Delwaide mentioned no

r= 0.55 (P < 0 001) relation between the classic vibratory indexand muscle tone, but subgroups of spastic

atio. *Indzcates patients were small and did not includexes and patients with patients with normal tone and more clinical

details were not provided.2 On the otherhand, Taylor et al found a correlationbetween vibratory inhibition and spasticity,

effects in patients when spasticity was defined as the combina-). Late facilitation tion of hypertonia and hyperreflexia.4 Iles andtendon reflexes Roberts reported that in a small selected

in control subjects group of patients with upper motor neuron/o, p < 0 05). This lesions studied during active dorsiflexion ofite inhibition; in the foot a decrease of suppression of vibratoryces the mean was inhibition correlated more with severity ofd in controls the weakness than with spasticity.2' We found a14%, p < 0.01). moderate but significant correlation betweens in neurophysio- vibratory inhibition and hypertonia. In con-present between trast to other studies our cumulative mea-sion, myelopathy, surement of vibratory effects integrates the

vibratory inhibition at multiple stimulusintensities. It seems to have some greater dis-criminative power5 than the classic ratio

lex between the maximum H-reflex response andi Clonus maximum muscle potential.' Our findings

may indicate a quantitative relation betweendecrease of tonic regulation of presynapticinhibition and increase of muscle tone up tomoderate levels. Decrease of presynaptic inhi-bition could result in an increased afferentinput to the soleus motor neuron pool con-

T- tributing to enhanced resistance to passivestretch characteristic of hypertonia.24 As such

... our findings would support the view that

.. hypertonia is associated with the release of acentral gain controlling mechanism in whichthe ability to modulate reflex transmission islost.25

* Although there are differences in electrical-* ly and mechanically elicited reflexes,26 a posi-

tive correlation between the H to M ratio andenhancement of tendon reflex activity wasfound. The H to M ratio correlated to a lesserdegree with muscle tone. Clearly enlarged Hto M ratios were found in all patients withclonus and probably indicate that in clonus

r = 0*40 (P < 0 05) enhancement of motor neuron excitability isgenerally present. These results could beaccounted for by mechanisms other than

Ireflexes (p <0d05) direct increases in motor neuron excitability,,nd patients with as, for example, increases in transmission

through the stretch reflex arc secondary to

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Soleus H-reflex tests and clinical signs of the upper motor neuron syndrome

reduced presynaptic inhibition on 1 a afferentterminals.

Postsynaptic late facilitation in the recoverycurve correlated slightly with enhancement oftendon reflex activity, independently ofincreased H to M ratios. Late facilitationoccurs at time intervals of about 250 msbetween the conditioning and the teststimulus and is followed by a late inhibitoryperiod at stimulus time intervals up to 1second and afterwards by complete recoveryof H-reflex features.2728 The late facilitationmay be partly due to cutaneous afferents.293'Its potentiation in spasticity, Parkinsonianrigidity, and dystonia673-33 suggests that thepolysynaptic pathways are affected, either inthe spinal cord or along long-loop pathways.33Potentiation of late facilitation in patientswith an upper motor neuron syndrome seemsunrelated to altered tone,'2 unlike that whichis thought to occur in dystonia.733 In clonus,however, the late facilitation was elevated.Thus in clonus interneuronal hyperactivityand increased motor neuron excitability maybe combined. Both are consistent with con-clusions based on direct recordings from Iaafferents, that spinal mechanisms rather thanincreased fusimotor drive are involved inclonus.'34

In our study we found that in patients withthe upper motor neuron syndrome alterationsin results of the soleus H-reflex test mayoccur independently from each other to alarge extent and that they relate to specificclinical features of the upper motor neuronsyndrome. The fact that our findings wereobtained in a heterogenous groups of patientsmay validate our results. We cannot, how-ever, fully exclude the possibility that alter-ations in the tests are influenced more byunderlying pathology than clinical character-istics. Further studies in distinct groups ofpatients with the same kind of upper motorneuron disease are necessary to clarify this.We thank AAM Hart from the laboratory of medical physicsfor his advice on the statistical analysis of data, DA Kropveldfor computer assistance, Dr J Stam for his helpful suggestionsand careful reading of the manuscript.JHTMK was supported by a grant from the Prinses Beatrix

Fonds, AAJH was supported by the Netherlands Organizationfor Scientific Research (NWO).

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